Endangered and Threatened Wildlife and Plants; Threatened Status for the Northern Mexican Gartersnake and Narrow-Headed Gartersnake, 38677-38746 [2014-14615]
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Vol. 79
Tuesday,
No. 130
July 8, 2014
Part II
Department of the Interior
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Fish and Wildlife Service
50 CFR Part 17
Endangered and Threatened Wildlife and Plants; Threatened Status for the
Northern Mexican Gartersnake and Narrow-Headed Gartersnake; Final Rule
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Federal Register / Vol. 79, No. 130 / Tuesday, July 8, 2014 / Rules and Regulations
DEPARTMENT OF THE INTERIOR
Fish and Wildlife Service
50 CFR Part 17
[Docket No. FWS–R2–ES–2013–0071:
4500030113]
RIN 1018–AY23
Endangered and Threatened Wildlife
and Plants; Threatened Status for the
Northern Mexican Gartersnake and
Narrow-Headed Gartersnake
telephone: 602–242–0210; facsimile:
602–242–2513.
FOR FURTHER INFORMATION CONTACT:
Steve Spangle, Field Supervisor, U.S.
Fish and Wildlife Service, Arizona
Ecological Services Field Office, 2321
West Royal Palm Road, Suite 103,
Phoenix, AZ 85021; telephone: 602–
242–0210; facsimile: 602–242–2513.
Persons who use a telecommunications
device for the deaf (TDD) may call the
Federal Information Relay Service
(FIRS) at 800–877–8339.
SUPPLEMENTARY INFORMATION:
AGENCY:
Executive Summary
We, the U.S. Fish and
Wildlife Service (Service), determine
threatened species status under the
Endangered Species Act of 1973 (Act),
as amended, for the northern Mexican
gartersnake (Thamnophis eques
megalops) and the narrow-headed
gartersnake (Thamnophis
rufipunctatus), native species from
Arizona and New Mexico in the United
States. We also finalize a rule under
authority of section 4(d) of the
Endangered Species Act of 1973, as
amended (Act), that provides measures
that are necessary and advisable to
provide for the conservation of the
northern Mexican gartersnake. Both
species are listed as threatened
throughout their range, which, for the
northern Mexican gartersnake, also
includes the Mexican states of Sonora,
Chihuahua, Durango, Coahuila,
Zacatecas, Guanajuato, Nayarit, Hidalgo,
´
Jalisco, San Luis Potosı, Aguascalientes,
´
Tlaxacala, Puebla, Mexico, Veracruz,
´
and Queretaro. The effect of this
regulation will be to add these species
to the lists of Endangered and
Threatened Wildlife and Plants.
DATES: This rule becomes effective
August 7, 2014.
ADDRESSES: This final rule is available
on the internet at https://
www.regulations.gov (Docket No. FWS–
R2–ES–2013–0071) and https://
www.fws.gov/southwest/es/arizona.
Comments and materials we received, as
well as supporting documentation we
used in preparing this rule, are available
for public inspection at https://
www.regulations.gov. All of the
comments, materials, and
documentation that we considered in
this rulemaking are available by
appointment, during normal business
hours at: U.S. Fish and Wildlife Service,
Arizona Ecological Services Field
Office, 2321 West Royal Palm Road,
Suite 103, Phoenix, AZ 85021;
Why we need to publish a rule. Under
the Endangered Species Act, a species
may warrant protection through listing
if it is endangered or threatened
throughout all or a significant portion of
its range. Listing a species as an
endangered or threatened species
requires issuing a rule. This rule will
finalize the listing of the northern
Mexican gartersnake (Thamnophis
eques megalops) and narrow-headed
gartersnake (Thamnophis rufipunctatus)
as threatened species, initiated with our
proposed listing rule published on July
10, 2013 (78 FR 41500), and finalize a
rule under authority of section 4(d) of
the Act that provides measures that are
necessary and advisable to provide for
the conservation of the northern
Mexican gartersnake.
The basis for our action. Under the
Endangered Species Act, we can
determine that a species is an
endangered or threatened species based
on any of five factors: (A) The present
or threatened destruction, modification,
or curtailment of its habitat or range; (B)
Overutilization for commercial,
recreational, scientific, or educational
purposes; (C) Disease or predation; (D)
The inadequacy of existing regulatory
mechanisms; or (E) Other natural or
manmade factors affecting its continued
existence. We have determined that
predation from and competition with
nonnative species such as bass
(Micropterus sp.), flathead catfish
(Pylodictis sp.), channel catfish
(Ictalurus sp.), Chihuahuan catfish
(Ictalurus chihuahua), bullheads
(Ameiurus sp.), sunfish (Lepomis sp.),
and crappie (Pomoxis sp.), brown trout
(Salmo trutta), American bullfrogs
(Lithobates catesbeiana), and crayfish
(northern (virile) crayfish (Orconectes
virilis) and red swamp crayfish
(Procambarus clarkia)) are the most
significant threat affecting these
gartersnakes across their range.
Throughout the remainder of this final
rule, the nonnative species identified
immediately above will be referred to
Fish and Wildlife Service,
Interior.
ACTION: Final rule.
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SUMMARY:
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collectively as ‘‘harmful nonnative
species.’’ Large-scale wildfires and land
uses that divert, dry up, or significantly
pollute aquatic habitat have also been
found to be significant threats.
Collectively, these threats have
adversely affected gartersnake
populations, and most of their native
prey species, such that the gartersnakes’
resiliency, redundancy, and
representation across their ranges have
been significantly compromised.
Peer review and public comment. We
sought comments from independent
specialists to ensure that our
designation is based on scientifically
sound data, assumptions, and analyses.
We invited these peer reviewers to
comment on our listing proposal. We
also considered all other comments and
information received during the
comment period on the proposed listing
rule. All comments are available at
https://www.regulations.gov (Docket No.
FWS–R2–ES–2013–0071).
Previous Federal Action
Please refer to the proposed listing
rule for the northern Mexican
gartersnake and narrow-headed
gartersnake (78 FR 41500; July 10, 2013)
for a detailed description of previous
Federal actions concerning this species.
We will also be finalizing the
designation of critical habitat for the
northern Mexican gartersnake and
narrow-headed gartersnake in a separate
rule in the future. Information regarding
designation of critical habitat for these
species is available at https://
www.regulations.gov (Docket No. FWS–
R2–ES–2013–0022).
Background
Northern Mexican Gartersnake
Subspecies Description
The northern Mexican gartersnake
ranges in color from olive to olivebrown or olive-gray with three lightercolored stripes that run the length of the
body, the middle of which darkens
toward the tail. This species may
inhabit the same area as other native
gartersnake species and can be difficult
for people without specific expertise to
identify. The snake may reach a
maximum known length of 44 inches
(in) (112 centimeters (cm)). The pale
yellow to light-tan lateral (side of body)
stripes distinguish the northern
Mexican gartersnake from other
sympatric (co-occurring) gartersnake
species because a portion of the lateral
stripe is found on the fourth scale row,
while it is confined to lower scale rows
for other species. Paired black spots
extend along the olive dorsolateral
fields (region adjacent to the top of the
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snake’s back) and the olive-gray
ventrolateral fields (region adjacent to
the area of the snake’s body in contact
with the ground). The scales are keeled
(possessing a ridge down the center of
each scale). A more detailed subspecies
description can be found in our
September 26, 2006 (71 FR 56227), or
November 25, 2008 (73 FR 71788) 12month findings for this subspecies, or
by reviewing Rosen and Schwalbe
(1988, p. 4), Rossman et al. (1996, pp.
171–172), Ernst and Ernst (2003, pp.
391–392), or Manjarrez and Garcia
(1993, pp. 1–5).
Taxonomy
The northern Mexican gartersnake
(Thamnophis eques megalops) is a
member of the family Colubridae and
subfamily Natricinae (harmless livebearing snakes) (Lawson et al. 2005, p.
596; Pyron et al. 2013, p. 31). The
taxonomy of the genus Thamnophis has
a complex history, partly because many
of the species are similar in appearance
and arrangement of scales and many of
the early museum specimens were in
such poor and faded condition that it
was difficult to study them (Conant
2003, p. 6).
Prior to 2003, Thamnophis eques was
considered to have three subspecies, T.
e. eques, T. e. megalops, and T. e.
virgatenuis (Rossman et al. 1996, p.
175). In 2003, an additional seven new
subspecies were identified under T.
eques: (1) T. e. cuitzeoensis; (2) T. e.
patzcuaroensis; (3) T. e. insperatus; (4)
T. e. obscurus; (5) T. e. diluvialis; (6) T.
e. carmenensis; and (7) T. e. scotti
(Conant 2003, p. 3). Common names
were not provided, so in this final rule,
we use the scientific name for all
subspecies of Mexican gartersnake other
than the northern Mexican gartersnake.
These seven new subspecies were
described based on morphological
differences in coloration and pattern,
have highly restricted distributions, and
occur in isolated wetland habitats
within the mountainous Transvolcanic
Belt region of southern Mexico, which
contains the highest elevations in the
country (Conant 2003, pp. 7–8).
Additional information regarding this
subspecies’ taxonomy can be found in
de Queiroz et al. (2002, p. 323), de
Queiroz and Lawson (1994, p. 217),
Rossman et al. (1996, pp. xvii–xviii,
171–175), Rosen and Schwalbe (1988,
pp. 2–3), Liner (1994, p. 107), and
Crother et al. (2012, p. 70). A
description of the taxonomy of the
northern Mexican gartersnake is found
in our September 26, 2006 (71 FR
56227) and November 25, 2008 (73 FR
71788) 12-month findings for this
subspecies.
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Habitat and Natural History
Throughout its rangewide
distribution, the northern Mexican
gartersnake occurs at elevations from
130 to 8,497 feet (ft) (40 to 2,590 meters
(m)) (Rossman et al. 1996, p. 172) and
is considered a ‘‘terrestrial-aquatic
´
generalist’’ (Drummond and Marcıas´
Garcıa 1983, pp. 24–26). The northern
Mexican gartersnake is a riparian
obligate (generally found in riparian
areas when not engaged in dispersal,
gestation, or hibernation behaviors) and
occurs chiefly in the following general
habitat types: (1) Small, often isolated
wetlands (e.g., cienegas (mid-elevation
wetlands with highly organic, reducing
(basic or alkaline) soils), or stock tanks
(small earthen impoundment)); (2) largeriver riparian woodlands and forests;
and (3) streamside gallery forests (as
defined by well-developed broadleaf
deciduous riparian forests with limited,
if any, herbaceous ground cover or
dense grass) (Hendrickson and Minckley
1984, p. 131; Rosen and Schwalbe 1988,
pp. 14–16). Emmons and Nowak (2013,
p. 14) found this subspecies most
commonly in protected backwaters,
braided side channels and beaver
ponds, isolated pools near the river
mainstem, and edges of dense emergent
vegetation that offered cover and
foraging opportunities when surveying
in the upper and middle Verde River
region. Additional information on the
habitat requirements of the northern
Mexican gartersnake within the United
States and Mexico can be found in our
2006 (71 FR 56227) and 2008 (73 FR
71788) 12-month findings for this
subspecies and in Rosen and Schwalbe
(1988, pp. 14–16), Rossman et al. (1996,
p. 176), McCranie and Wilson (1987, pp.
11–17), Ernst and Ernst (2003, p. 392),
and Cirett-Galan (1996, p. 156).
The northern Mexican gartersnake is
surface active at ambient (air)
temperatures ranging from 71 degrees
Fahrenheit (°F) to 91 °F (22 degrees
Celsius (°C) to 33 °C) and forages along
the banks of waterbodies (Rosen 1991,
p. 305, Table 2). While conducting
visual surveys, Rosen (1991, pp. 308–
309) found that northern Mexican
gartersnakes spent up to 60 percent of
their time moving, 13 percent of their
time basking on vegetation, 18 percent
of their time basking on the ground, and
9 percent of their time under surface
cover. However, preliminary telemetry
data from a population of northern
Mexican gartersnakes at the Bubbling
Ponds State Fish Hatchery show
individuals were surface active during
16 percent of telemetry observations,
not surface active during 64 percent of
telemetry observations, and surface
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activity was undetermined for 20
percent of the telemetry observations
(Boyarsky 2013, pers. comm.); at
Tavasci Marsh along the upper Verde
River, they were inactive 60 percent of
the time (Emmons 2013b, pers. comm.).
In the northern-most part of its range,
the northern Mexican gartersnake
appears to be most active during July
and August, followed by June and
September (Emmons and Nowak 2013,
p. 14). Northern Mexican gartersnakes
may use different sites as hibernacula
during a single cold-season and will
bask occasionally (Emmons 2014, pers.
comm.).
Although considered a highly aquatic
species, the northern Mexican
gartersnake uses terrestrial habitat for
hibernation (Young and Boyarski 2012b,
pp. 25–28), gestation, seeking mates,
and dispersal. Along the middle Verde
River preliminary telemetry data for the
northern Mexican gartersnake found
that the species may travel at least 528
feet (161 m) from the nearest water and
as much as 0.4 mi (0.6 km) in a single
day (total distance traveled) (Emmons
2014, pers. comm.). Terrestrial habitat
use in open, grassland-dominated
landscapes with scattered livestock
tanks, such as in southern Arizona, may
reflect that greater distances are traveled
as suggested by the observation of a
large female northern Mexican
gartersnake observed in O’Donnell
Canyon, which was far from source
populations and may have been
dispersing overland (Rosen and
Schwalbe 1988, p. 14). Preliminary data
from the population at Bubbling Ponds
State Fish Hatchery show that home
ranges vary from 1.7 acres (0.7 ha) to
10.4 acres (4.2 ha), with a mean home
range size of 6.2 acres (2.51 ha) (Young
and Boyarski 2012b, p. 23).
The northern Mexican gartersnake is
an active predator and depends on
smaller animals for its prey base (Rosen
and Schwalbe 1988, pp. 18, 20).
Northern Mexican gartersnakes forage
along vegetated banklines, searching for
prey in water and on land, using
different strategies (Alfaro 2002, p. 209),
or may forage along the edges of open
water and thick stands of vegetation
such as cattails. Generally, its diet
consists of native amphibians and
fishes, such as adult and larval
(tadpoles) native leopard frogs (e.g.,
lowland leopard frog (Lithobates
yavapaiensis) and Chiricahua leopard
frog (Lithobates chiricahuensis)), as well
as juvenile and adult native fish species
(e.g., Gila topminnow (Poeciliopsis
occidentalis occidentalis), desert
pupfish (Cyprinodon macularius), Gila
chub (Gila intermedia), and roundtail
chub (Gila robusta)) (Rosen and
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Schwalbe 1988, p. 18). Drummond and
´
´
Marcıas-Garcıa (1983, pp. 25, 30) found
that as a subspecies, Mexican
gartersnakes fed primarily on frogs. The
northern Mexican gartersnake may
congregate at ephemeral amphibian
breeding ponds to exploit high-density
prey populations as observed at New
Mexican spadefoot toads (Spea
multiplicata) breeding sites (d’Orgeix et
al. 2013, pp. 213–215). Auxiliary prey
items may also include young
Woodhouse’s toads (Anaxyrus
woodhousei), treefrogs (Family Hylidae),
earthworms, deermice (Peromyscus
spp.), lizards of the genera Aspidoscelis
and Sceloporus, larval tiger salamanders
(Ambystoma tigrinum), and leeches
(Rosen and Schwalbe 1988, p. 20; Holm
and Lowe 1995, pp. 30–31; Degenhardt
et al. 1996, p. 318; Rossman et al. 1996,
p. 176; Manjarrez 1998, p. 465).
Salamanders (Ambystoma spp.) may be
particularly important as prey for
northern Mexican gartersnake
populations in northern Mexico, both at
lower elevations and along the Sierra
Madre Occidental (Lemos-Espinal 2013,
pers. comm.).
In situations where native prey
species are rare or absent, this snake’s
diet may be almost completely
comprised of nonnative species,
including larval and juvenile bullfrogs
(Lithobates catesbeianus), mosquitofish
(Gambusia affinis) (Holycross et al.
2006, p. 23), or subadult green sunfish,
bluegill, or largemouth bass (Emmons
and Nowak 2013, p. 5; Emmons 2013a,
pers. comm.). The most recent
observations of northern Mexican
gartersnakes attempting to eat predatory
fish was discussed in Emmons and
Nowak (2013, p. 6) where they found
fish inside traps with gartersnakes, and
the fish appeared to have been partially
consumed and then regurgitated. These
observations suggest that, while
northern Mexican gartersnakes may
attempt to eat predatory fish (at least in
the artificial confines of a wire trap),
they may often be spontaneously
regurtitated, potentially causing harm to
the snake (Nowak and Santana-Bendix
2002, p. 24), and may not be compatible
prey for northern Mexican gartersnakes.
Interestingly, in a 2012 trapping effort
along the upper Santa Cruz River,
minnow traps that become self-baited
with bullfrogs, mosquitofish, or
macroinvertebrates captured snakes, but
those which contained green sunfish or
largemouth bass never caught a single
northern Mexican gartersnake (Lashway
2012, p. 6).
Chinese mystery snails
(Cipangopaludina chinensis) have also
been reported as a prey item for
northern Mexican gartersnakes at the
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Page Springs and Bubbling Ponds State
Fish Hatcheries in Arizona, but some
predation attempts on snails have
proven fatal for gartersnakes because of
their lower jaw becoming permanently
lodged in the snails’ shell (Young and
Boyarski 2012a, p. 498). VenegasBarrera and Manjarrez (2001, p. 187)
reported the first observation of a snake
in the natural diet of any species of
Thamnophis after documenting the
consumption of a Mexican alpine
blotched gartersnake (Thamnophis
scalaris) by a Mexican gartersnake (T.
eques; subspecies not reported); a
behavior termed ophiophagy.
Ophiophagy has not been specifically
reported in northern Mexican
gartersnakes, although they are a
subspecies of the Mexican gartersnake.
´
´
Marcıas-Garcıa and Drummond (1988,
pp. 129–134) sampled the stomach
contents of Mexican gartersnakes and
the prey populations at (ephemeral)
Lake Tecocomulco, Hidalgo, Mexico.
Field observations indicated, with high
statistical significance, that larger
Mexican gartersnakes fed primarily
upon aquatic vertebrates (fishes, frogs,
and larval salamanders) and leeches,
whereas smaller Mexican gartersnakes
fed primarily upon earthworms and
´
´
leeches (Marcıas-Garcıa and Drummond
´
´
1988, p. 131). Marcıas-Garcıa and
Drummond (1988, p. 130) also found
that the birth of newborn T. eques
tended to coincide with the annual peak
density of annelids (earthworms and
leeches). There is also preliminary
evidence that birth may coincide with a
pronounced influx of available prey in
a given area, especially with that of
explosive breeders, such as toads, but
more research is needed to confirm such
a relationship (Boyarski 2012, pers.
comm.). Positive correlations were also
made with respect to capture rates
(which are correlated with population
size) of T. eques to lake levels and to
prey scarcity; that is, when lake levels
were low and prey species scarce,
Mexican gartersnake capture rates
´
´
declined (Marcıas-Garcıa and
Drummond 1988, p. 132). While prey
scarcity could have driven snakes to
become active or take shelter
underground, their results suggest the
importance of available water and an
adequate prey base to maintaining
viable populations of Mexican
´
´
gartersnakes. Marcıas-Garcıa and
Drummond (1988, p. 133) found that,
while certain prey items were positively
associated with size classes of snakes,
the largest of specimens consume any
prey available.
Native predators of the northern
Mexican gartersnake include birds of
prey, other snakes (kingsnakes
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(Lampropeltis sp.), whipsnakes (Coluber
sp.), regal ring-necked snakes
(Diadophis punctatus regalis), etc.),
wading birds, mergansers (Mergus
merganser), belted kingfishers
(Megaceryle alcyon), raccoons (Procyon
lotor), skunks (Mephitis sp.), and
coyotes (Canis latrans) (Rosen and
Schwalbe 1988, pp. 18, 39; Brennan et
al. 2009, p. 123). Historically, large,
highly predatory native fish species
such as Colorado pikeminnow
(Ptychocheilus lucius) may have preyed
upon northern Mexican gartersnake
where the subspecies co-occurred.
Native chubs (Gila sp.) may also prey on
neonatal gartersnakes, but has not been
documented in the literature to our
knowledge.
Sexual maturity in northern Mexican
gartersnakes occurs at 2 years of age in
males and at 2 to 3 years of age in
females (Rosen and Schwalbe 1988, pp.
16–17). Northern Mexican gartersnakes
are viviparous (bringing forth living
young rather than eggs). Mating has
been documented in April and May
followed by the live birth of between 7
and 38 newborns (average is 13.6) in
June, July, and August (Rosen and
Schwalbe 1988, p. 16; Nowak and
Boyarski 2012, pp. 351–352; Boyarski
2013, pers. comm.). However, field
observations in Arizona provide
preliminary evidence that mating may
also occur during the fall, but further
research is required to confirm this
hypothesis (Boyarski 2012, pers.
comm.). Unlike other gartersnake
species, which typically breed annually,
one study suggests that only half of the
sexually mature females within a
population of northern Mexican
gartersnake might reproduce in any one
season (Rosen and Schwalbe 1988, p.
17). We found no information on the
longevity of northern Mexican
gartersnakes but presume they may live
as long as 10 years in the wild.
Historical Distribution
Within the United States, the northern
Mexican gartersnake historically
occurred predominantly in Arizona at
elevations ranging from 130 to 6,150 ft
(40 to 1,875 m). It was generally found
where water was relatively permanent
and supported suitable habitat. The
northern Mexican gartersnake has been
documented historically in every county
and nearly every subbasin within
Arizona, but its historical distribution
was essentially the southern two-thirds
of Arizona. It was known from several
perennial or intermittent creeks,
streams, and rivers as well as lentic
(still, non-flowing water) wetlands such
as cienegas, ponds, or stock tanks.
Records documenting northern Mexican
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gartersnake exist within the following
subbasins in Arizona: Colorado River,
Bill Williams River, Agua Fria River,
Salt River, Tonto Creek, Verde River,
Santa Cruz River, Cienega Creek, San
Pedro River, Babocomari River, and the
Rio San Bernardino (Black Draw)
(Woodin 1950, p. 40; Nickerson and
Mays 1970, p. 503; Bradley 1986, p. 67;
Rosen and Schwalbe 1988, Appendix I;
1995, p. 452; 1997, pp. 16–17; Holm and
Lowe 1995, pp. 27–35; Sredl et al.
1995b, p. 2; 2000, p. 9; Rosen et al.
2001, Appendix I; Holycross et al. 2006,
pp. 1–2, 15–51; Brennan and Holycross
2006, p. 123; Radke 2006, pers. comm.;
Rosen 2006, pers. comm.; Holycross
2006, pers. comm.; Cotton et al. 2013, p.
111). Numerous records for the northern
Mexican gartersnake (through 1996) in
Arizona are maintained in the Arizona
Game and Fish Department’s (AGFD)
Heritage Database (1996a).
Historically, the northern Mexican
gartersnake had a limited distribution in
New Mexico that consisted of scattered
locations throughout the Upper Gila
River watershed in Grant and western
Hidalgo Counties, including the Upper
Gila River, Mule Creek in the San
Francisco River subbasin, and the
Mimbres River (Price 1980, p. 39;
Fitzgerald 1986, Table 2; Degenhardt et
al. 1996, p. 317; Holycross et al. 2006,
pp. 1–2).
One record for the northern Mexican
gartersnake exists for the State of
Nevada, opposite Fort Mohave, in Clark
County along the shore of the Colorado
River that was dated 1911 (De Queiroz
and Smith 1996, p. 155). The subspecies
may have occurred historically in the
lower Colorado River region of
California, although we were unable to
verify any museum records for
California. Any populations of northern
Mexican gartersnakes that may have
historically occurred in either Nevada or
California were likely associated
directly with the Colorado River, and
we believe the northern Mexican
gartersnake to be currently extirpated in
Nevada and California.
Within Mexico, northern Mexican
gartersnakes historically occurred
within the Sierra Madre Occidental and
the Mexican Plateau in the Mexican
states of Sonora, Chihuahua, Durango,
Coahuila, Zacatecas, Guanajuato,
Nayarit, Hidalgo, Jalisco, San Luis
´
Potosı, Aguascalientes, Tlaxacala,
´
Puebla, Mexico, Veracruz, and
´
Queretaro, comprising approximately 85
percent of the total rangewide
distribution of the subspecies (Conant
1963, p. 473; 1974, pp. 469–470; Van
Devender and Lowe 1977, p. 47;
McCranie and Wilson 1987, p. 15;
Rossman et al. 1996, p. 173; Lemos-
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Espinal et al. 2004, p. 83). We are not
aware of any systematic, rangewide
survey effort for the northern Mexican
gartersnake in Mexico. Therefore, we
use other related ecological surrogates
(such as native freshwater fish) to
inform discussion on the status of
aquatic communities and aquatic habitat
in Mexico, and therefore on the likely
status of northern Mexican gartersnake
populations. We believe that
gartersnakes and native fish are closely
ecologically connected because of the
high level of dependency of the
gartersnakes on the fish as a food
source. This discussion is found below
in the subheadings pertinent to Mexico.
Current Distribution and Population
Status
Data on population status of northern
Mexican gartersnakes in the United
States are largely summarized in
unpublished agency reports. In our
literature review we found that
reductions in range and population
densities have affected the status of the
northern Mexican gartersnake
significantly in the last 30 years. We
found that, in as much as 90 percent of
the northern Mexican gartersnakes’
historical distribution in the United
States, the subspecies occurs at low to
very low population densities or may
even be extirpated. For example,
Holycross et al. (2006, p. 66) detected
the northern Mexican gartersnake at
only 2 of 11 historical localities within
the northern-most part of its range in the
United States. The degraded status of
the northern Mexican gartersnake, in a
rangewide context, is primarily the
result of predation by and competition
with harmful nonnative species, that
have been legally released, illegally
released, or have naturally dispersed
(explained below). However, ecological
circumstances and potential threats vary
from site to site, and the same threats do
not affect every population with the
same magnitude across their range.
Regardless of how they got into the
wild, harmful nonnative species are
now widespread and present throughout
the range of the northern Mexican
gartersnake. Land uses that result in the
dewatering of habitat, combined with
increasing drought, have destroyed
significant amounts of habitat
throughout the northern Mexican
gartersnake’s range and have, therefore,
reduced its distribution within several
subbasins.
Where northern Mexican gartersnakes
are locally abundant, they are usually
reliably detected with significantly less
effort than populations characterized as
having low densities. Northern Mexican
gartersnakes are well-camouflaged,
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secretive, and can be very difficult to
detect in structurally complex, dense
habitat (Emmons and Nowak 2013, p.
13) or where they occur at very low
population densities, which
characterizes most occupied sites in
lotic habitat. We considered factors such
as the date of the last known records for
northern Mexican gartersnakes in an
area, as well as records of one or more
native prey species in making a
conclusion on occupancy of the
subspecies. We used the year 1980 to
qualify occupancy because the 1980s
marked the first systematic survey
efforts for northern Mexican
gartersnakes across their range in the
United States (see Rosen and Schwalbe
(1988, entire) and Fitzgerald (1986,
entire)) and the last, previous records
were often dated several decades prior
and may not accurately represent the
likelihood for current occupation.
Several areas where northern Mexican
gartersnakes were known to occur have
received no, or very little, survey effort
in the past several decades. Variability
in survey design and effort makes it
difficult to compare population sizes or
trends among sites and between
sampling periods. For each of the sites
discussed in Appendix A (available at
https://www.regulations.gov, Docket No.
FWS–R2–ES–2013–0071), we have
attempted to translate and quantify
search and capture efforts into
comparable units (i.e., person-search
hours and trap-hours) and have
cautiously interpreted those results.
Because the presence of suitable prey
species in an area may provide evidence
that the northern Mexican gartersnake
may still persist in low density where
survey data are sparse, a record of a
native prey species was considered in
our determination of occupancy of this
subspecies.
Currently, there are only five northern
Mexican gartersnake populations in the
United States, where the subspecies
remains reliably detected and is
considered viable, and all are located in
Arizona. The five known populations
are: (1) The Page Springs and Bubbling
Ponds State Fish Hatcheries along Oak
Creek, (2) lower Tonto Creek, (3) the
upper Santa Cruz River in the San
Rafael Valley, (4) the Bill Williams
River, and (5) the upper and middle
Verde River. In New Mexico, the
northern Mexican gartersnake was last
documented in 2013 along the Gila
River in the vicinity of the Highway 180
crossing (Hotle 2013, entire) and is
considered to occur in extremely low
population densities within its
historical distribution along the Gila
River and Mule Creek. While
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historically known to occur on tribal
lands, the status of the northern
Mexican gartersnake on tribal lands,
such as those owned by the White
Mountain or San Carlos Apache Tribes,
is poorly known due to limited survey
access. As stated previously, less is
known specifically about the current
distribution of the northern Mexican
gartersnake in Mexico due to limited
access to information on survey efforts
and field data from Mexico.
In Table 1 below, we summarize the
population status of northern Mexican
gartersnakes at all known 29 historical
localities throughout their United States
distribution, as supported by museum
records or reliable observations. We
categorized each population as either
likely viable, likely not viable, or likely
extirpated based on the historical survey
records, suitable habitat, presence of
native prey species, and the presence of
harmful nonnative species. For a
detailed discussion that explains the
rationale for site-by-site conclusions on
occupancy, please see Appendix A
(available at https://www.regulations.gov,
Docket No. FWS–R2–ES–2013–0071).
General rationale is provided in the
introductory paragraph to this section,
‘‘Current Distribution and Population
Status.’’
TABLE 1—CURRENT POPULATION STATUS OF THE NORTHERN MEXICAN GARTERSNAKE IN THE UNITED STATES
[References for This Information Are Provided in Appendix A]
Last record
Suitable
physical
habitat
present
Native prey
species
present
Harmful
nonnative
species
present
Gila River (NM, AZ) .....................................................................
2013 .............
Yes ...............
Yes ...............
Yes ...............
Spring Canyon (NM) ...................................................................
1937 .............
Yes ...............
Possible .......
Likely ............
Mule Creek (NM) .........................................................................
1983 .............
Yes ...............
Yes ...............
Yes ...............
Mimbres River (NM) ....................................................................
Likely early
1900s.
1904 .............
Yes ...............
Yes ...............
Yes ...............
Lower Colorado River (AZ) .........................................................
Yes ...............
Yes ...............
Yes ...............
Bill Williams River (AZ) ................................................................
Agua Fria River (AZ) ...................................................................
2012 .............
1986 .............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Little Ash Creek (AZ) ...................................................................
1992 .............
Yes ...............
Yes ...............
Yes ...............
Lower Salt River (AZ) ..................................................................
1964 .............
Yes ...............
Yes ...............
Yes ...............
Black River (AZ) ..........................................................................
1982 .............
Yes ...............
Yes ...............
Yes ...............
Big Bonito Creek (AZ) .................................................................
1986 .............
Yes ...............
Yes ...............
Yes ...............
Tonto Creek (AZ) ........................................................................
Upper Verde River (AZ) ..............................................................
Oak Creek (AZ) ...........................................................................
(Page Springs and Bubbling Ponds State Fish Hatcheries) .......
Spring Creek (AZ) .......................................................................
2005 .............
2012 .............
2012 .............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
1986 .............
Yes ...............
Yes ...............
Yes ...............
Sycamore Creek (Yavapai/Coconino Co., AZ) ...........................
1954 .............
Yes ...............
Possible .......
Yes ...............
Upper Santa Cruz River/San Rafael Valley (AZ) ........................
Redrock Canyon (AZ) ..................................................................
2013 .............
2008 .............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Yes ...............
Sonoita Creek (AZ) .....................................................................
2013 .............
Yes ...............
Possible .......
Yes ...............
Scotia Canyon (AZ) .....................................................................
2009 .............
Yes ...............
Yes ...............
No ................
Parker Canyon (AZ) ....................................................................
1986 .............
Yes ...............
Possible .......
Yes ...............
Las Cienegas National Conservation Area and Cienega Creek
Natural Preserve (AZ).
Lower Santa Cruz River (AZ) ......................................................
2012 .............
Yes ...............
Yes ...............
Possible .......
1956 .............
Yes ...............
Yes ...............
Yes ...............
Buenos Aires National Wildlife Refuge (AZ) ...............................
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Location
2000 .............
Yes ...............
Yes ...............
Yes ...............
Bear Creek (AZ) ..........................................................................
1987 .............
Yes ...............
Yes ...............
Yes ...............
San Pedro River (AZ) ..................................................................
1996 .............
Yes ...............
Yes ...............
Yes ...............
Babocomari River and Cienega (AZ) ..........................................
1986 .............
Yes ...............
Possible .......
Yes ...............
Canelo Hills-Sonoita Grasslands Area (AZ) ................................
2012 .............
Yes ...............
Yes ...............
Yes ...............
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Population
status
Likely not viable.
Likely extirpated.
Likely not viable.
Likely extirpated.
Likely extirpated.
Likely viable.
Likely not viable.
Likely not viable.
Likely extirpated.
Likely not viable.
Likely not viable.
Likely viable.
Likely viable.
Likely viable.
Likely not viable.
Likely extirpated.
Likely viable.
Likely not viable.
Likely not viable.
Likely not viable.
Likely not viable.
Likely not viable.
Likely extirpated.
Likely not viable.
Likely not viable.
Likely not viable.
Likely not viable.
Likely not viable.
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38683
TABLE 1—CURRENT POPULATION STATUS OF THE NORTHERN MEXICAN GARTERSNAKE IN THE UNITED STATES—
Continued
[References for This Information Are Provided in Appendix A]
Location
Last record
Suitable
physical
habitat
present
Native prey
species
present
Harmful
nonnative
species
present
Population
status
San Bernardino National Wildlife Refuge (AZ) ...........................
1997 .............
Yes ...............
Yes ...............
Yes ...............
Likely not viable.
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Notes: ‘‘Possible’’ means there were no conclusive data found. ‘‘Likely extirpated’’ means the last record for an area pre-dated 1980, and existing threats suggest the species is likely extirpated. ‘‘Likely not viable’’ means there is a post-1980 record for the species, it is not reliably found
with minimal to moderate survey effort, and threats exist which suggest the population may be low density or could be extirpated, but there is insufficient evidence to support extirpation. ‘‘Likely viable’’ means that the species is reliably found with minimal to moderate survey effort, and the
population is generally considered to be somewhat resilient.
We conclude that as many as 24 of 29
known northern Mexican gartersnake
localities in the United States (83
percent) are likely not viable and may
exist at low population densities that
could be threatened with extirpation or
may already be extirpated. In most
localities where the species may occur
at low population densities, existing
survey data are insufficient to support a
conclusion of extirpation. Only five
populations of northern Mexican
gartersnakes in the United States are
considered likely viable where the
species remains reliably detected. In our
November 25, 2008, 12-month finding,
we evaluated the total number of stream
miles in the United States that
historically supported the northern
Mexican gartersnake that are now
permanently dewatered (except in the
case of temporary flows in response to
heavy precipitation), and we concluded
that the subspecies has been extirpated
from or occurs at low densities in as
much as 90 percent of its historical
range in the United States (73 FR 71788,
pp. 71792–71793). As shown in Table 1,
harmful nonnative species are present
in all but one northern Mexican
gartersnake locality in the United States.
The northern Mexican gartersnake is
listed as threatened throughout its range
in Mexico by the Mexican Government.
However, our understanding of the
northern Mexican gartersnake’s specific
population status throughout its range
in Mexico is less precise than that
known for its United States distribution
because survey efforts are less and
available records do not exist or are
difficult to obtain for many regions.
Some specific geographic distribution
records for the Mexican states of Sonora,
´
Chihuahua, and San Luis Potosı were
presented in Lemos-Espinal (2013, pers.
comm.). Lemos-Espinal (2013 pers.
comm), a Mexican herpetologist whose
work is focused on the states of Sonora,
Chihuahua, and Coahuila, commented
that the number and magnitude of
threats are not equal across the
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subspecies’ range in Mexico. Habitat
alteration or removal, as a circumstance
of human population growth in Mexico,
is reported as a primary concern for
populations that occur in the Sierra
Madre Occidental (Lemos-Espinal 2013,
pers. comm.). In other regions of
Mexico, such as the states of Sonora and
Chihuahua, Lemos-Espinal (2013, pers.
comm.) observed the northern Mexican
gartersnake to be quite common.
Another gartersnake researcher from
Mexico has observed the decline or
disappearance of some populations in
central Mexico (Manjerrez 2008).
Narrow-Headed Gartersnake
Species Description
The narrow-headed gartersnake is a
small to medium-sized gartersnake with
a maximum total length of 44 in (112
cm) (Painter and Hibbitts 1996, p. 147).
Its eyes are set high on its unusually
elongated head, which narrows to the
snout, and it lacks striping on the
dorsum (top) and sides, which
distinguishes its appearance from other
gartersnake species with which it could
co-occur (Rosen and Schwalbe 1988, p.
7). The base color is usually tan or greybrown (but may darken) with
conspicuous brown, black, or reddish
spots that become indistinct towards the
tail (Rosen and Schwalbe 1988, p. 7;
Boundy 1994, p. 126). The scales are
keeled. Degenhardt et al. (1996, p. 327),
Rossman et al. (1996, pp. 242–244), and
Ernst and Ernst (2003, p. 416) further
describe the species.
Taxonomy
We recognize the narrow-headed
gartersnake, Thamnophis rufipunctatus,
as a monotypic species (no currently
recognized subspecies exist). The
narrow-headed gartersnake is a member
of the family Colubridae and subfamily
Natricinae (harmless live-bearing
snakes) (Lawson et al. 2005, p. 596). The
taxonomy of the genus Thamnophis has
a complex history partly because many
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of the species are similar in appearance
and scutelation (arrangement of scales)
and because many of the early museum
specimens were in such poor and faded
condition that it was difficult to study
them (Conant 2003, p. 6). There are
approximately 30 species described in
the gartersnake genus Thamnophis
(Rossman et al. 1996, pp. xvii–xviii).
Two large overlapping clades (related
taxonomic groups) of gartersnakes have
been identified called the ‘‘Mexican’’
and ‘‘widespread’’ clades, supported by
allozyme and mitochondrial DNA
genetic analyses (de Queiroz et al. 2002,
p. 321). The narrow-headed gartersnake
(Thamnophis rufipunctatus) is a
member of the ‘‘Mexican’’ clade and is
most closely related taxonomically to
the southern Durango spotted
gartersnake (Thamnophis nigronuchalis)
(de Queiroz and Lawson 1994, p. 217;
de Queiroz et al. 2002; p. 321).
Due to the narrow-headed
gartersnake’s morphology and feeding
habits, there has been considerable
deliberation among taxonomists about
the correct association of this species
within seven various genera over time
(Rosen and Schwalbe 1988, pp. 5–6);
chiefly, between the genera
Thamnophis (the ‘‘gartersnakes’’) and
Nerodia (the ‘‘watersnakes’’) (Pierce
2007, p. 5). Chaisson and Lowe (1989,
pp. 110–118) argued that the pattern of
ultrastructural (as revealed by an
electron microscope) pores in the scales
of narrow-headed gartersnakes provided
evidence that the species is more
appropriately placed within the genus
Nerodia. However, De Queiroz and
Lawson (1994, p. 217) rejected this
premise using mitochondrial DNA
(mtDNA) genetic analyses to refute the
inclusion of the narrow-headed
gartersnake in the genus Nerodia and
maintain the species within the genus
Thamnophis.
The narrow-headed gartersnake was
first described as Chilopoma
rufipunctatum by E. D. Cope (in Yarrow,
1875). Recently, Thamnophis
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rufipunctatus nigronuchalis and T. r.
unilabialis were recognized as
subspecies under T. rufipunctatus and
comprised what was considered the T.
rufipunctatus complex (Rossman et al.
1996, p. 245). However, Rossman et al.
(1996, pp. 244–246) elevated T. r.
nigronuchalis to full species designation
and argued that recognition of T. r.
unilabialis be discontinued due to the
diagnostic differences being too difficult
to discern. Wood et al. (2011, p. 14)
used genetic analysis of the T.
rufipunctatus complex to propose the
elevation of these three formerly
recognized subspecies as three distinct
species, as a result of a combination of
interglacial warming, ecological and
life-history constraints, and genetic
drift, which promoted differentiation of
these three species throughout the
warming and cooling periods of the
Pleistocene epoch (Wood et al. 2011, p.
15). We use these most recent and
complete data in acknowledging these
three entities as unique species: T.
rufipunctatus (along the Mogollon Rim
of Arizona and New Mexico, the
narrow-headed gartersnake, which is the
subject of this rule), T. unilabialis
(Chihuahua, eastern Sonora, and
northern Durango, Mexico), and T.
nigronuchalis (southern Durango,
Mexico).
Several common names have been
used for this species including the redspotted gartersnake, the brown-spotted
gartersnake, and the currently used,
narrow-headed gartersnake (Rosen and
Schwalbe 1988, p. 5). Further
discussion of the taxonomic history of
the narrow-headed gartersnake is
available in Crother (2012, p. 71),
Degenhardt et al. (1996, p. 326),
Rossman et al. (1996, p. 244), De
Queiroz and Lawson (1994, pp. 213–
229), Rosen and Schwalbe (1988, pp. 5–
7), and De Queiroz et al. (2002, p. 321).
Habitat and Natural History
The narrow-headed gartersnake,
distributed across the Mogollon Rim of
Arizona and New Mexico, is widely
considered to be one of the most aquatic
of the gartersnakes (Drummond and
Marcias Garcia 1983, pp. 24, 27;
Rossman et al. 1996, p. 246). This
species is strongly associated with clear,
rocky streams, using predominantly
pool and riffle habitat that includes
cobbles and boulders (Rosen and
Schwalbe 1988, pp. 33–34; Degenhardt
et al. 1996, p. 327; Rossman et al. 1996,
p. 246; Nowak and Santana-Bendix
2002, pp. 26–37; Ernst and Ernst 2003,
p. 417). Rossman et al. (1996, p. 246)
also note the species has been observed
using lake shoreline habitat in New
Mexico. Narrow-headed gartersnakes
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occur at elevations from approximately
2,300 to 8,000 ft (701 to 2,430 m),
inhabiting Petran Montane Conifer
Forest, Great Basin Conifer Woodland,
Interior Chaparral, and the Arizona
Upland subdivision of Sonoran
Desertscrub communities (Rosen and
Schwalbe 1988, p. 33; Brennan and
Holycross 2006, p. 122).
An extensive evaluation of habitat use
of narrow-headed gartersnakes along
Oak Creek in Arizona is provided in
Nowak and Santana-Bendix (2002, pp.
26–37). In the upper reaches of Oak
Creek, occupied habitat is found in a
steep-walled, confined canyon with
shallow, braided stream segments,
minimal silt, and good canopy coverage,
vegetated islands and significant
amounts of aquatic vegetation (Nowak
and Santana-Bendix 2002, pp. 29–30).
In the middle reaches of Oak Creek,
occupied habitat is found in a wider
canyon with less stream braiding,
deeper pools, more silt, and high
canopy coverage and stream-side
vegetation, but less aquatic vegetation
(Nowak and Santana-Bendix 2002, pp.
30–31). In the lower reaches of Oak
Creek, historically occupied habitat
occurred outside of the canyon proper,
with predominant pool-run sequences,
rare channel braiding, much silt,
significantly less canopy coverage or
streamside vegetation and few areas
with aquatic vegetation (Nowak and
Santana-Bendix 2002, p. 31).
Nowak and Santana-Bendix (2002, pp.
29–31) found the most narrow-headed
gartersnakes in the upper reaches of Oak
Creek, followed by the middle reaches;
no narrow-headed gartersnakes were
found in the lower reaches. Nowak and
Santana-Bendix (2002, p. 33) found that,
in general, narrow-headed gartersnakes
in Oak Creek were more likely to be
found within reaches without crayfish
and without silt. Population densities of
warm-water predatory fish increase on a
gradient from the upper to the lower
reaches of Oak Creek, while the inverse
is true for native fish populations, and
their presence confounds the analysis of
physical habitat preference of narrowheaded gartersnakes. Rosen and
Schwalbe (1988, p. 35) found that the
relative abundance of narrow-headed
gartersnakes may be highest at the
conjunction of cascading riffles with
pools, where waters were deeper than
20 in (0.5 m) in the riffle and deeper
than 40 in (1 m) in the immediately
adjoining area of the pool. However,
more than twice the number of snakes
was found in pools rather than riffles,
but this observation may not translate
for smaller streams. Despite their highly
aquatic behavior, narrow-headed
gartersnakes in Oak Creek have been
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shown to use upland habitat within 328
feet (100 m) during early fall and spring
months, strongly associate with
boulders in the floodplain during
summer months, and use upland habitat
up to 656 feet (200 m) out of the
floodplain as hibernation sites (Nowak
2006, pp. 20, 26).
Bank-line vegetation is an important
component to suitable habitat for this
species (Nowak and Santana-Bendix
2002, pp. 26–37). Narrow-headed
gartersnakes will usually bask in
situations where a quick escape can be
made, whether that is into the water or
under substrate such as rocks (Fleharty
1967, p. 16). Common plant species
associations include Arizona alder
(Alnus oblongifolia) (highest correlation
with occurrence of the narrow-headed
gartersnake), velvet ash (Fraxinus
pennsylvanica), willows (Salix ssp.),
canyon grape (Vitis arizonica),
blackberry (Rubus ssp.), Arizona
sycamore (Platanus wrightii), Arizona
black walnut (Juglans major), Freemont
cottonwood (Populus fremontii),
Gambel oak (Quercus gambelii), and
ponderosa pine (Pinus ponderosa)
(Rosen and Schwalbe 1988, pp. 34–35).
Rosen and Schwalbe (1988, p. 35) noted
that the composition of bank-side plant
species and canopy structure may be
less important to the species’ needs than
was the size class of the plant species
present; narrow-headed gartersnakes use
shrub- and sapling-sized plants for
thermoregulating (basking) at the
waters’ edge (Degenhardt et al. 1996, p.
327), as well as islands within the
stream channel that are created by sedge
(Carex spp.) tussocks (Nowak and
Santana-Bendix 2002, p. 34).
Narrow-headed gartersnakes may
opportunistically forage within dammed
reservoirs formed by streams that are
occupied habitat, such as at Wall Lake,
New Mexico, (located at the confluence
of Taylor Creek, Hoyt Creek, and the
East Fork Gila River) (Fleharty 1967, p.
207) and most recently at Snow Lake in
2012 (located near the confluence of
Snow Creek and the Middle Fork Gila
River) (Hellekson 2012b, pers. comm.)
in New Mexico, but records from
impoundments are rare. The species
evolved in the absence of such habitat,
and impoundments are generally
managed as sport fisheries (Wall Lake
and Snow Lake are) and often maintain
populations of harmful nonnative
species that are incompatible with
narrow-headed gartersnakes.
The narrow-headed gartersnake is
surface-active generally between March
and November (Nowak 2006, p. 16).
Little information on suitable
temperatures for surface activity of the
narrow-headed gartersnake exists;
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however, it is presumed to be rather
cold-tolerant based on its natural history
and foraging behavior that often
involves clear, cold streams at higher
elevations. Along Oak Creek in Arizona,
Nowak (2006, Appendix 1) found the
species to be active in air temperatures
ranging from 52 to 89 °F (11 to 32 °C)
and water temperatures ranging from 54
to 72 °F (12 to 22 °C). Jennings and
Christman (2011, pp. 12–14) found body
temperatures of narrow-headed
gartersnakes along the Tularosa River
averaged approximately 68 °F (20 °C)
during the mid-morning hours and 81 °F
(27 °C) in the late afternoon during the
period from late July and August.
Variables that affect their body
temperature include the temperature of
the microhabitat used and water
temperature (most predictive), but slope
aspect and the surface area of cover
used also influenced body temperatures
(Jennings and Christman 2011, p. 13).
Narrow-headed gartersnakes have a
lower preferred temperature for activity
as compared to other species of
gartersnakes (Fleharty 1967, p. 228),
which may facilitate their highly aquatic
nature in cold streams.
Narrow-headed gartersnakes
specialize on fish as their primary prey
item (Rosen and Schwalbe 1988, p. 38;
Degenhardt et al. 1996, p. 328; Rossman
et al. 1996, p. 247; Nowak and SantanaBendix 2002, pp. 24–25; Nowak 2006, p.
22). They are believed to be mainly
visual hunters (Hibbitts and Fitzgerald
2005, p. 364) heavily dependent on
visual cues when foraging based on
comparative analyses among other
species of gartersnakes (de Queiroz
2003, p. 381). Unlike many other
species of gartersnakes that are active
predators (actively crawl about in search
of prey), narrow-headed gartersnakes are
considered to be ambush predators (sitand-wait method) (Brennan and
Holycross 2006, p. 122; Pierce et al.
2007, p. 8). The specific gravity (ratio of
the mass of a solid object to the mass of
the same volume of water) of the
narrow-headed gartersnake was found to
be nearly 1, which means that the snake
can maintain its desired position in the
water column with ease, an adaptation
to facilitate foraging on the bottom of
streams (Fleharty 1967, pp. 218–219).
Native fish species most often
associated as prey items for the narrowheaded gartersnake include Sonora
sucker (Catostomus insignis), desert
sucker (C. clarki), speckled dace
(Rhinichthys osculus), roundtail chub
(Gila robusta), Gila chub (Gila
intermedia), and headwater chub (Gila
nigra) (Rosen and Schwalbe 1988, p. 39;
Degenhardt et al. 1996, p. 328).
Nonnative predatory fish species in
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their fingerling size classes are also used
as prey by narrow-headed gartersnakes,
including brown trout (Rosen and
Schwalbe 1988, p. 39; Nowak and
Santana-Bendix 2002, p. 24; Nowak
2006, pp. 22–23), green sunfish
(Fleharty 1967, p. 223), and smallmouth
bass (Micropterus dolomieu) (M. Lopez,
2010, pers. comm.). Reports suggest that
brown trout are consumed more
frequently than smallmouth bass. Trout
species are commonly stocked in, or
near, occupied narrow-headed
gartersnake habitat. Fleharty (1967, p.
223) reported narrow-headed
gartersnakes eating green sunfish. But
nonnative fish with spiny dorsal fins are
not generally considered suitable prey
items due to the risk of injury to the
gartersnake during ingestion and
because of where they tend to occur in
the water column (see discussion in the
subsection ‘‘Fish’’ under the subheading
‘‘Decline of the Gartersnake Prey Base’’
and Nowak and Santana-Bendix (2002,
p. 24)).
Although the narrow-headed
gartersnake has been reported to also
prey upon amphibians such as frogs,
tadpoles, and salamanders (Stebbins
1985, p. 199; Deganhardt et al. 1996, p.
328; Ernst and Ernst 2003, p. 418), we
believe these are not important items in
their diet. Despite several studies
focusing on the ecology of narrowheaded gartersnakes in recent times,
there are no other records of narrowheaded gartersnakes, under current
taxonomic recognition, feeding on prey
items other than fish. Fitzgerald (1986,
p. 6) referenced the Stebbins (1985)
account as the only substantiated
account of the species eating something
other than fish as prey, apparently as
the result of finding a small salamander
larvae in the stomach of an individual
in Durango, Mexico. Formerly
recognized as a subspecies of
Thamnophis rufipunctatus, that
individual is now recognized as T.
unilabialis (Wood et al. 2011, p. 3). We
found one account of narrow-headed
gartersnakes consuming red-spotted
toads in captivity (Woodin 1950, p. 40).
Amphibian larvae (i.e. Hyla sp.,
Anaxyrus sp., Ambystoma sp.) are
generally available to narrow-headed
gartersnakes as prey, yet observations of
narrow-headed gartersnakes using them
are rare. Therefore, we do not consider
amphibians as ecologically important
prey for this species.
Native predators of the narrowheaded gartersnake include birds of
prey, such as black-hawks (Etzel et al.
2014, p. 56), other snakes such as regal
ring-necked snakes (Brennan et al. 2009,
p. 123), wading birds, mergansers,
belted kingfishers, raccoons (Rosen and
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38685
Schwalbe 1988, p. 39), and possibly
other generalist mammalian predators.
Historically, large, highly predatory
native fish species, such as Colorado
pikeminnow, may have preyed upon
narrow-headed gartersnakes where the
species co-occurred. Native chubs (Gila
spp.) may also prey on neonatal
gartersnakes.
Sexual maturity in narrow-headed
gartersnakes occurs at 2.5 years of age in
males and at 2 years of age in females
(Deganhardt et al. 1996, p. 328).
Narrow-headed gartersnakes are
viviparous. Narrow-headed gartersnakes
breed annually, and females give birth
to 4 to 17 offspring from late July into
early August, perhaps earlier at lower
elevations (Rosen and Schwalbe 1988,
pp. 35–37). Narrow-headed gartersnakes
may live as long as 10 years in the wild
(Rosen and Schwalbe 1988, p. 38).
Historical Distribution
The historical distribution of the
narrow-headed gartersnake ranged
across the Mogollon Rim and along
associated perennial stream drainages
from central and eastern Arizona,
southeast to southwestern New Mexico
at elevations ranging from 2,300 to 8,000
ft (700 to 2,430 m) (Rosen and Schwalbe
1988, p. 34; Rossman et al. 1996, p. 242;
Holycross et al. 2006, p. 3). The species
was historically distributed in
headwater streams of the Gila River
subbasin that drain the Mogollon Rim
and White Mountains in Arizona, and
the Gila Wilderness in New Mexico.
Major subbasins in its historical
distribution included the Salt and Verde
River subbasins in Arizona, and the San
Francisco and Gila River subbasins in
New Mexico (Holycross et al. 2006, p.
3). Holycross et al. (2006, p. 3) suspect
the species was likely not historically
present in the lowest reaches of the Salt,
Verde, and Gila Rivers, even where
perennial flow persists. Numerous
records for the narrow-headed
gartersnake (through 1996) in Arizona
are maintained in the AGFD’s Heritage
Database (1996b). The narrow-headed
gartersnake as currently recognized does
not occur in Mexico.
Current Distribution and Population
Status
Population status information
suggests that the narrow-headed
gartersnake has experienced significant
declines in population density and
distribution along streams and rivers
where it was formerly well-documented
and reliably detected. Many areas where
the species may occur likely rely on
emigration of individuals from occupied
habitat into those areas to maintain the
species, provided there are no potential
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barriers to movement, such as extensive
stretches of dewatered habitat, or high
densities of harmful nonnative species.
Holycross et al. (2006, entire) represents
the most recent, comprehensive survey
effort for narrow-headed gartersnakes in
Arizona. Narrow-headed gartersnakes
were detected in 5 of 16 historical
localities in Arizona and New Mexico
surveyed by Holycross et al. (2006) in
2004 and 2005. Population densities
have noticeably declined in many
populations, as compared to previous
survey efforts (Holycross et al. 2006, p.
66). Holycross et al. (2006, pp. 66–67)
compared narrow-headed gartersnake
detections based on results from their
effort and that of previous efforts in the
same locations and found that
significantly more effort is required to
detect this species in areas where it was
formerly robust, such as along Eagle
Creek (AZ), the East Verde River (AZ),
the San Francisco River (NM), the Black
River (AZ), and the Blue River (AZ).
Where narrow-headed gartersnakes
are locally abundant, they can usually
be detected reliably and with
significantly less effort than populations
characterized as having low densities.
Narrow-headed gartersnakes are wellcamouflaged, secretive, and very
difficult to detect in structurally
complex, dense habitat where they
could occur at very low population
densities, which characterizes most
occupied sites. We considered factors
such as the date of the last known
records for narrow-headed gartersnakes
in an area, as well as records of one or
more native prey species, in making a
conclusion on species occupancy. We
used all records that were dated 1980 or
later because the 1980s marked the first
systematic survey efforts for narrow-
headed gartersnake species across their
range (see Rosen and Schwalbe (1988,
entire) and Fitzgerald (1986, entire)),
and the last, previous records were often
dated several decades prior and may not
accurately represent the likelihood for
current occupation. Several areas where
narrow-headed gartersnakes were
known to occur have received no, or
very little, survey effort in the past
several decades. Variability in survey
design and effort makes it difficult to
compare population sizes or trends
among sites and between sampling
periods. Thus, for each of the sites
discussed in Appendix A (available at
https://www.regulations.gov, Docket No.
FWS–R2–ES–2013–0071), we have
attempted to translate and quantify
search and capture efforts into
comparable units (i.e., person-search
hours and trap-hours) and have
cautiously interpreted those results.
Where survey data are sparse, the
presence of suitable prey species in an
area may provide evidence that narrowheaded gartersnakes may still persist at
low densities. Therefore, a record of a
native prey species was considered in
our determination of occupancy of this
species.
As of 2011, the only remaining
narrow-headed gartersnake populations
where the species could reliably be
found were located at: (1) Whitewater
Creek (NM), (2) Tularosa River (NM), (3)
Diamond Creek (NM), (4) Middle Fork
Gila River (NM), and (5) Oak Creek
Canyon (AZ). However, populations
found in Whitewater Creek and the
Middle Fork Gila River were likely
significantly affected by the large
Whitewater–Baldy Complex Fire, which
occurred in June 2012. In addition,
salvage efforts were initiated for these
two populations, which included the
removal of 25 individuals from
Whitewater Creek and 14 individuals
from the Middle Fork Gila River before
the onset of summer rains in 2012.
These 39 individuals were transported
to the Albuquerque BioPark where 22
remain in captivity. The other 17 of the
salvaged individuals were translocated
to Saliz Creek, where the resident native
prey base appears adequate, and beyond
the effects from the Whitewater-Baldy
Complex Fire. The status of those
populations in Whitewater Creek and
the Middle Fork Gila River has likely
deteriorated as a result of subsequent
declines in resident fish communities
due to heavy ash and sediment flows,
resulting fish kills, and the removal of
snakes, but subsequent survey data have
not been collected. If the Whitewater
Creek and Middle Fork Gila River
populations did decline as a result of
these factors, only three remaining
populations of this species remain
viable today across their entire
distribution. While historical records
confirm the narrow-headed gartersnake
was found on tribal lands, its current
status on tribal land is poorly known
due to limited survey access.
In Table 2 below, we summarize the
population status of the narrow-headed
gartersnake at all known localities
throughout its distribution, as supported
by museum records or reliable
observations. For a detailed discussion
that explains the rationale for site-bysite conclusions on occupancy and
status, please see Appendix A (available
at https://www.regulations.gov, Docket
No. FWS–R2–ES–2013–0071). General
rationale is provided in the introductory
paragraph to this section, ‘‘Current
Distribution and Population Status.’’
TABLE 2—CURRENT POPULATION STATUS OF THE NARROW-HEADED GARTERSNAKE
[References for this information are provided in appendix A]
tkelley on DSK3SPTVN1PROD with RULES2
Location
Last record
West Fork Gila River (NM) ...........
Middle Fork Gila River (NM) .........
East Fork Gila River (NM) ............
Gila River (AZ, NM) ......................
Snow Creek/Snow Lake (NM) ......
Gilita Creek (NM) ..........................
Iron Creek (NM) ............................
Little Creek (NM) ...........................
Turkey Creek (NM) .......................
Beaver Creek (NM) .......................
Black Canyon (NM) .......................
Taylor Creek (NM) ........................
Diamond Creek (NM) ....................
Tularosa River (NM) .....................
Whitewater Creek (NM) ................
San Francisco River (NM) ............
South Fork Negrito Creek (NM) ....
Blue River (AZ) .............................
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2011
2012
2006
2009
2012
2009
2009
2010
1985
1949
2010
1960
2011
2012
2012
2011
2011
2007
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Suitable physical
habitat present
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Native prey species
present
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
Frm 00010
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Harmful nonnative
species present
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
No ............................
Yes ..........................
Yes ..........................
Possible ...................
Yes ..........................
Possible ...................
Yes ..........................
No ............................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Possible ...................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
No ............................
No ............................
Yes ..........................
Possible ...................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Sfmt 4700
E:\FR\FM\08JYR2.SGM
08JYR2
Population status
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
not viable.
not viable.
not viable.
not viable.
not viable.
not viable.
not viable.
not viable.
not viable.
extirpated.
not viable.
extirpated.
viable.
viable.
not viable.
not viable.
not viable.
not viable.
Federal Register / Vol. 79, No. 130 / Tuesday, July 8, 2014 / Rules and Regulations
38687
TABLE 2—CURRENT POPULATION STATUS OF THE NARROW-HEADED GARTERSNAKE—Continued
[References for this information are provided in appendix A]
Location
Last record
Dry Blue Creek (AZ, NM) .............
Campbell Blue Creek (AZ, NM) ....
Saliz Creek (NM) ..........................
Eagle Creek (AZ) ..........................
Black River (AZ) ............................
East Fork Black River (AZ) ...........
Fish Creek (Tributary to East Fork
Black River; AZ).
White River (AZ) ...........................
Diamond Creek (AZ) .....................
Tonto Creek (tributary to Big
Bonita Creek, AZ).
Canyon Creek (AZ) .......................
Upper Salt River (AZ) ...................
Cibeque Creek (AZ) ......................
Carrizo Creek (AZ) ........................
Big Bonito Creek (AZ) ...................
Haigler Creek (AZ) ........................
Houston Creek (AZ) ......................
Tonto Creek (tributary to Salt
River, AZ).
Deer Creek (AZ) ...........................
Upper Verde River (AZ) ................
Oak Creek (AZ) .............................
West Fork Oak Creek (AZ) ...........
East Verde River (AZ) ..................
Suitable physical
habitat present
Native prey species
present
Harmful nonnative
species present
Population status
2010
2010
2013
2013
2013
2004
2004
Yes
Yes
Yes
Yes
Yes
Yes
Yes
..........................
..........................
..........................
..........................
..........................
..........................
..........................
Possible ...................
Possible ...................
Possible ...................
Possible ...................
Yes ..........................
Possible ...................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Possible ...................
Likely
Likely
Likely
Likely
Likely
Likely
Likely
1986
1986
1915
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Possible ...................
Possible ...................
Possible ...................
Possible ...................
Possible ...................
Likely not viable.
Likely not viable.
Likely extirpated.
1991
1985
1991
1997
1957
2008
2005
2005
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
No ............................
Yes ..........................
Possible ...................
Possible ...................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Likely
Likely
Likely
Likely
Likely
Likely
Likely
Likely
not viable.
not viable.
not viable.
not viable.
extirpated.
not viable.
not viable.
not viable.
1995
2012
2012
2012
1992
No ............................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
No ............................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
No ............................
Yes ..........................
Yes ..........................
Yes ..........................
Yes ..........................
Likely
Likely
Likely
Likely
Likely
extirpated.
not viable.
viable.
viable.
not viable.
..........................
..........................
..........................
..........................
..........................
..........................
..........................
..........................
not viable.
not viable.
not viable.
not viable.
not viable.
not viable.
viable.
Notes: ‘‘Possible’’ means there were no conclusive data found. ‘‘Likely extirpated’’ means the last record for an area pre-dated 1980, and existing threats suggest the species is likely extirpated. ‘‘Likely not viable’’ means there is a post-1980 record for the species, it is not reliably found
with minimal to moderate survey effort, and threats exist which suggest the population may be low density or could be extirpated, but there is insufficient evidence to support extirpation. ‘‘Likely viable’’ means that the species is reliably found with minimal to moderate survey effort, and the
population is generally considered to be somewhat resilient.
tkelley on DSK3SPTVN1PROD with RULES2
Table 2 lists the 41 known localities
for narrow-headed gartersnakes
throughout their range. We have
concluded that, in as many as 31 of 41
known localities (76 percent), the
narrow-headed gartersnake population
is likely not currently viable and may
exist at low population densities that
could be threatened with extirpation or
may already be extirpated, but survey
data are lacking in areas where access is
restricted. In most localities where the
species may occur at low population
densities, existing survey data are
insufficient to conclude extirpation. As
of 2014, narrow-headed gartersnake
populations are considered currently
likely viable in five localities (12
percent). The remaining five
populations (12 percent) are considered
currently likely extirpated. As displayed
in Table 2, harmful nonnative species
are a concern for all but four narrowheaded gartersnake populations. The
status of these populations is expected
to continue to decline.
Summary of Biological Status and
Threats
Section 4 of the Act (16 U.S.C. 1533),
and its implementing regulations at 50
CFR part 424, set forth the procedures
for adding species to the Federal Lists
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of Endangered and Threatened Wildlife
and Plants. Under section 4(a)(1) of the
Act, we may list a species based on any
of the following five factors: (A) The
present or threatened destruction,
modification, or curtailment of its
habitat or range; (B) overutilization for
commercial, recreational, scientific, or
educational purposes; (C) disease or
predation; (D) the inadequacy of
existing regulatory mechanisms; and (E)
other natural or manmade factors
affecting its continued existence. Listing
actions may be warranted based on any
of the above threat factors, singly or in
combination.
In the following threats analysis, we
treat both gartersnake species in a
combined discussion because of
partially overlapping ranges, similar
natural histories, similar responses to
threats, and the fact that many threats
are shared in common throughout their
ranges.
Weakened Status of Native Aquatic
Communities (Northern Mexican and
Narrow-Headed Gartersnakes) (Factors
A, C, and E)
The presence of harmful nonnative
species constitutes the most significant
threat to the two gartersnake species.
Harmful nonnative species directly prey
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upon both species of gartersnake and
compete with them for prey. Harmful
nonnative species also compete with
gartersnake prey species as well as
modify habitat for both the gartersnakes
and their prey, to the detriment of both
gartersnakes. Landscape-level effects
from the continued expansion of
harmful nonnative species have
changed the spatial orientation of these
gartersnakes’ distributions, creating
greater isolation between populations.
We expect the viability of extant
gartersnake populations to continue to
degrade into the foreseeable future as a
result of ecological interactions with
harmful nonnative species. Riparian and
aquatic communities in both the
southwestern United States and Mexico
have been significantly impacted by a
shift in species’ composition, from one
of primarily native fauna, to one
dominated by an expanding assemblage
of harmful nonnative animal species.
Harmful nonnative species have been
introduced or have spread into new
areas through a variety of mechanisms,
including intentional and accidental
releases, sport stocking, aquaculture,
aquarium releases, bait-bucket releases,
or natural dispersal (Welcomme 1984,
entire). The ecological ramifications of
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tkelley on DSK3SPTVN1PROD with RULES2
the adversarial relationships within
southwestern aquatic communities have
been discussed and described in a broad
body of literature, extending from 1985
to the present (Meffe 1985, pp. 179–185;
Propst et al. 1986, pp. 14–31, 82; 1988,
p. 64; 2009, pp. 5–17; Rosen and
Schwalbe 1988, pp. 28, 32; 1997, p. 1;
Clarkson and Rorabaugh 1989, pp. 531,
535; Douglas et al. 1994, pp. 9–19;
Rosen et al. 1995, pp. 257–258; 2001, p.
2; Degenhardt et al. 1996, p. 319;
Fernandez and Rosen 1996, pp. 8, 23–
27, 71, 96; Richter et al. 1997, pp. 1089,
1092; Inman et al. 1998, p. 17; Rinne et
al. 1998, pp. 4–6; Nowak and SantanaBendix 2002, Table 3; Propst 2002, pp.
21–25; DFT 2003, pp. 1–3, 5–6, 19;
2004, pp. 1–2, 4–5, 10, Table 1; Bonar
et al. 2004, pp. 13, 16–21; Rinne 2004,
pp. 1–2; Clarkson et al. 2005, p. 20;
Fagan et al. 2005, pp. 34, 34–41; Knapp
2005, pp. 273–275; Olden and Poff
2005, pp. 82–87; Turner 2007, p. 41;
Holycross et al. 2006, pp. 13–15;
Brennan 2007, pp. 5, 7; Caldwell 2008a,
2008b; d’Orgeix 2008; Luja and
´
Rodrıguez-Estrella 2008, pp. 17–22;
Propst et al. 2008, pp. 1242–1243;
Rorabaugh 2008a, p. 25; Brennan and
Rosen 2009, pp. 8–9; Minckley and
Marsh 2009, pp. 50–51; Pilger et al.
2010, pp. 311–312; Stefferud et al. 2009,
pp. 206–207; 2011, pp. 11–12; Young
and Boyarski 2013, pp. 159–160).
Decline of the Gartersnake Prey Base
(Northern Mexican and Narrow-Headed
Gartersnakes) (Factors A and E)
The prey base of these gartersnakes
includes native amphibians and fish
populations. Declines in their prey base
have led to subsequent declines in the
distribution and density of gartersnake
populations. In most areas across their
ranges, prey base declines are largely
attributed to the introduction and
expansion of harmful nonnative species.
Northern Mexican and narrow-headed
gartersnakes may be particularly
vulnerable to the loss of native prey
species (Rosen and Schwalbe 1988, pp.
20, 44–45). Rosen et al. (2001, pp. 10,
13, 19) theorized that the northern
Mexican gartersnake: (1) Is unlikely to
increase foraging efforts at the risk of
increased predation; and (2) needs
adequate food on a regular basis to
maintain its weight and health. If forced
to forage more often for smaller prey
items, a reduction in growth and
reproductive rates can result (Rosen et
al. 2001, pp. 10, 13). Rosen et al. (2001,
p. 22) hypothesized that the presence
and expansion of nonnative predators
(mainly bullfrogs, crayfish, and green
sunfish (Lepomis cyanellus)) are the
primary causes of decline in northern
Mexican gartersnakes and in their prey
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in southeastern Arizona. In another
´
example, Drummond and Macıas Garcia
(1989, pp. 25, 30) found that Mexican
gartersnakes fed primarily on frogs, and
when frogs became unavailable, the
species simply ceased major foraging
activities. This led the authors to
conclude that frog abundance is
probably the most important correlate,
and main determinant, of foraging
behavior in northern Mexican
gartersnakes.
With respect to narrow-headed
gartersnakes, the relationship between
harmful nonnative species, a declining
prey base, and gartersnake populations
is clearly depicted in one population
along Oak Creek. Nowak and SantanaBendix (2002, Table 3) found a strong
correlation in the distribution of fish
communities and narrow-headed
gartersnake communities in the vicinity
of Midgely Bridge. Downstream of that
point, nonnative, predatory fish species
increase in abundance, and narrowheaded gartersnakes notably decrease in
abundance. Upstream of that point,
native fish and nonnative, soft-rayed
fish species increase in abundance as do
narrow-headed gartersnakes (Nowak
and Santana-Bendix 2002, p. 23).
Fish (Northern Mexican and Narrowheaded Gartersnakes)—Fish are an
important prey item for the northern
Mexican gartersnake and are the only
prey for the narrow-headed gartersnake.
Native fish communities throughout the
range of these gartersnake have been on
the decline, both in terms of species
composition and biomass, for many
decades, and largely as a result of
predation and competition from and
with nonnative, predatory fish species.
Stocked for sport, forage, or biological
control, nonnative fishes have been
shown to become invasive where
released and do not require the natural
flow regimes that native species do
(Kolar et al. 2003, p. 9), which has
contributed to their expansion in the
Gila River basin and elsewhere.
Northern Mexican and narrow-headed
gartersnakes can successfully use
nonnative, soft-rayed fish species as
prey, such as mosquitofish, red shiner,
and introduced trout species, such as
rainbow trout (Oncorynchus mykiss),
brook trout (Salvelinus fontinalis), or
brown trout (Nowak and SantanaBendix 2002, pp. 24–25; Holycross et al.
2006, p. 23). However, predatory fish
are not generally considered prey
species for northern Mexican or narrowheaded gartersnakes and, in addition,
are known to prey on neonatal and
juvenile gartersnakes (Young and
Boyarski 2013, pp. 158–159). Nowak
and Santana-Bendix (2002, p. 24)
propose two hypotheses regarding the
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reluctance of narrow-headed
gartersnakes to prey on nonnative,
predatory fish: (1) The laterally
compressed shape and presence of
sharp, spiny dorsal spines of many
nonnative, predatory fish present a
choking hazard to gartersnakes that can
be fatal; and (2) nonnative, predatory
fish (with the exception of catfish) tend
to occupy the middle and upper zones
in the water column, while narrowheaded gartersnakes typically hunt
along the bottom (where native suckers
and minnows often occur). As a result,
nonnative, predatory fish may be less
ecologically available as prey.
Brown trout are highly predatory in
all size classes in a wide range of water
temperatures, and they adversely affect
native fish communities wherever they
are introduced (Taylor et al. 1984, pp.
343–344). Predation on gartersnakes by
adult brown trout may be a particular
problem for narrow-headed gartersnakes
due to their overlapping distributions
and habitat preferences, both in terms of
direct predation on neonatal
gartersnakes and through competitive
pressures for gartersnakes by preying on
their food source. Specifically, the
younger age classes of brown trout
present competition problems for the
narrow-headed gartersnake by eating
small fish. As brown trout mature into
the medium to larger size classes, they
may prey upon neonatal narrow-headed
gartersnakes. These issues are
confounded by the fact that young
brown trout are also eaten by narrowheaded gartersnakes and may represent
an important component of their prey
base, depending on fish species
composition and age classes represented
within the resident fish community.
However, whatever benefits fingerling
brown trout present for narrow-headed
gartersnakes are likely off-set by effects
of brown trout predation on important
native fish species, and possible effects
to recruitment of narrow-headed
gartersnakes through predation.
Harmful nonnative species invasions
can indirectly affect the health,
maintenance, and reproduction of
northern Mexican and narrow-headed
gartersnakes by altering their foraging
strategy and compromising foraging
success. Rosen et al. (2001, p. 19), in
addressing the northern Mexican
gartersnake, proposed that an increase
in energy expended in foraging, coupled
by the reduced number of small to
medium-sized prey fish available,
results in deficiencies in nutrition,
affecting growth and reproduction. This
occurs because energy is allocated to
maintenance and the increased energy
costs of intense foraging activity, rather
than to growth and reproduction. In
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contrast, a northern Mexican
gartersnake diet that includes both fish
and amphibians, such as leopard frogs,
reduces the necessity to forage at a
higher frequency, allowing metabolic
energy gained from larger prey items to
be allocated instead to growth and
reproductive development. Myer and
Kowell (1973, p. 225) experimented
with food deprivation in common
gartersnakes, and found significant
reductions in lengths and weights of
juvenile snakes that were deprived of
regular feedings versus the control
group that were fed regularly at natural
frequencies. Reduced foraging success
of both northern Mexican and narrowheaded gartersnakes means that
individuals are likely to become
vulnerable to effects from starvation,
which may increase fatality rates of
juveniles and, consequently, affect
recruitment.
Northern Mexican gartersnakes have a
more varied diet than narrow-headed
gartersnakes. We are not aware of any
studies that have addressed the direct
relationship between prey base diversity
and northern Mexican gartersnake
recruitment and survivorship. However,
Krause and Burghardt (2001, pp. 100–
123) discuss the benefits and costs that
may be associated with diet variability
in the common gartersnake
(Thamnophis sirtalis), an ecologically
similar species to the northern Mexican
gartersnake. Foraging for mixed-prey
species may impede predator learning,
as compared to specialization on a
certain prey species, but it may also
provide long-term benefits such as the
ability to capture prey throughout their
lifespan (Krause and Burghardt 2001, p.
101).
A wide variety of native fish species
(many of which are now listed as
endangered, threatened, or candidates
for listing under the Act) were
historically primary prey species for
northern Mexican and narrow-headed
gartersnakes (Rosen and Schwalbe 1988,
pp. 18, 39). Marsh and Pacey (2005, p.
60) predict that, despite the significant
physical alteration of aquatic habitat in
the southwestern United States, native
fish species could flourish in these
altered environments but for the
presence of harmful nonnative fish
species. Northern Mexican and, in
particular, narrow-headed gartersnakes
depend largely on native fish as a
principal part of their prey base,
although nonnative, soft-rayed
predatory fish have also been
documented as prey where they overlap
in distribution with these gartersnakes
(Nowak and Santana-Bendix 2002, pp.
24–25; Holycross et al. 2006, p. 23;
Emmons and Nowak 2013, p. 6).
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Nonnative, predatory fish compete with
northern Mexican and narrow-headed
gartersnakes for prey. In their extensive
surveys, Rosen and Schwalbe (1988, p.
44) only found narrow-headed
gartersnakes in abundance where native
fish species predominated but did not
find them abundant in the presence of
robust nonnative, predatory fish
populations. Minckley and Marsh (2009,
pp. 50–51) found nonnative fishes to be
the single-most significant factor in the
decline of native fish species and also
their primary obstacle to recovery. Of
the 48 conterminous States in the
United States, Arizona has the highest
proportion of nonnative fish species (66
percent) represented by approximately
68 species (Turner and List 2007, p. 13).
Collier et al. (1996, p. 16) note that
interactions between native and
nonnative fish have significantly
contributed to the decline of many
native fish species from direct predation
and, indirectly, from competition
(which has adversely affected the prey
base for northern Mexican and narrowheaded gartersnakes). Holycross et al.
(2006, pp. 52–61) documented
depressed or extirpated native fish prey
bases for northern Mexican and narrowheaded gartersnakes along the Mogollon
Rim in Arizona and New Mexico. Rosen
et al. (2001, Appendix I) documented
the decline of several native fish species
in several locations visited in
southeastern Arizona, further affecting
the prey base of northern Mexican
gartersnakes in that area.
Harmful nonnative fish species tend
to be nest-builders and actively guard
their young, which may provide them
another ecological advantage over native
species that are broadcast spawners and
provide no parental care to their
offspring (Marsh and Pacey 2005, p. 60).
In fact, nesting smallmouth bass will
attack gartersnakes (Winemiller and
Taylor 1982, p. 270). It is, therefore,
likely that recruitment and survivorship
is greater in nonnative species than
native species where they overlap,
providing nonnative species with an
ecological advantage. Table 2–1 in Kolar
et al. (2003, p. 10) provides a map
depicting the high degree of overlap in
the distribution of native and nonnative
fishes within the Gila River basin of
Arizona and New Mexico as well as
watersheds thought to be dominated by
nonnative fish species.
The widespread decline of native fish
species from the arid southwestern
United States and Mexico has resulted
largely from interactions with nonnative
species and has been noted in the listing
rules of 11 fishes under the Act, and
their historical ranges overlap with the
historical distribution of northern
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Mexican and narrow-headed
gartersnakes. Native fish species that
were likely prey species for these
gartersnakes and are now listed under
the Act, include the bonytail chub (Gila
elegans, 45 FR 27710, April 23, 1980),
Yaqui chub (Gila purpurea, 49 FR
34490, August 31, 1984), Yaqui
topminnow (Poeciliopsis occidentalis
sonoriensis, 32 FR 4001, March 11,
1967), beautiful shiner (Cyprinella
formosa, 49 FR 34490, August 31, 1984),
Gila chub (Gila intermedia, 70 FR
66663, November 2, 2005), Colorado
pikeminnow (Ptychocheilus lucius, 32
FR 4001, March 11, 1967), spikedace
(Meda fulgida, 77 FR 10810, February
23, 2012), loach minnow (Tiaroga
cobitis, 77 FR 10810, February 23,
2012), razorback sucker (Xyrauchen
texanus, 56 FR 54957, October 23,
1991), desert pupfish (Cyprinodon
macularius, 51 FR 10842, March 31,
1986), woundfin (Plagopterus
argentissiums, 35 FR 16047, October 13,
1970), and Gila topminnow
(Poeciliopsis occidentalis, 32 FR 4001,
March 11, 1967). In total within
Arizona, 19 of 31 (61 percent) native
fish species are listed under the Act.
Arizona ranks the highest of all 50
States in the percentage of native fish
species with declining trends (85.7
percent), and New Mexico ranks sixth
(48.1 percent) (Stein 2002, p. 21; Warren
and Burr 1994, p. 14).
The fastest expanding nonnative
species are red shiner (Cyprinella
lutrensis), fathead minnow (Pimephales
promelas), green sunfish, largemouth
bass (Micropterus salmoides), western
mosquitofish, and channel catfish
(Ictalurus punctatus). A nonnative
species can become invasive if
ecological advantages exist for broad
physical tolerances, feeding habits and
diet, or reproductive behavior (Taylor et
al. 1984, Table 16–1). These species are
considered to be the most invasive in
terms of their negative impacts on
native fish communities (Olden and Poff
2005, p. 75). Many nonnative fishes, in
addition to those listed immediately
above, including yellow and black
bullheads (Ameiurus sp.), flathead
catfish (Pylodictis olivaris), and
smallmouth bass, have been introduced
into formerly and currently occupied
northern Mexican or narrow-headed
gartersnake habitat and are predators on
these species (Young and Boyarski 2013,
pp. 158–159) and their prey (Bestgen
and Propst 1989, pp. 409–410; Marsh
and Minckley 1990, p. 265; Sublette et
al. 1990, pp. 112, 243, 246, 304, 313,
318; Abarca and Weedman 1993, pp. 6–
12; Stefferud and Stefferud 1994, p. 364;
Weedman and Young 1997, pp. 1,
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Appendices B, C; Rinne et al. 1998, pp.
3–6; Voeltz 2002, p. 88; Bonar et al.
2004, pp. 1–108; Fagan et al. 2005, pp.
34, 38–39, 41; Propst et al. 2008, pp.
1242–1243). Nonnative, predatory fish
species, such as flathead catfish, may be
especially dangerous to narrow-headed
gartersnake populations through
competition and direct predation
because they are primarily piscivorous
(fish-eating) (Pilger et al. 2010, pp. 311–
312), have large mouths, and have a
tendency to occur along the stream
bottom, where narrow-headed
gartersnakes principally forage.
Rosen et al. (2001, Appendix I) and
Holycross et al. (2006, pp. 15–51)
conducted large-scale surveys for
northern Mexican gartersnakes in
southeastern and central Arizona and
narrow-headed gartersnakes in central
and east-central Arizona, and
documented the presence of nonnative
fish at many locations. Holycross et al.
(2006, pp. 14–15) found nonnative fish
species in 64 percent of the sample sites
in the Agua Fria subbasin, 85 percent of
the sample sites in the Verde River
subbasin, 75 percent of the sample sites
in the Salt River subbasin, and 56
percent of the sample sites in the Gila
River subbasin. In total, nonnative fish
were observed at 41 of the 57 sites
surveyed (72 percent) across the
Mogollon Rim (Holycross et al. 2006, p.
14). Entirely native fish communities
were presumed in only 8 of 57 sites
surveyed (14 percent) (Holycross et al.
2006, p. 14). It is well documented that
nonnative fish have now infiltrated the
majority of aquatic communities in the
southwestern United States as depicted
in Tables 1 and 2, above, as well as in
Appendix A (available at https://
www.regulations.gov, Docket No. FWS–
R2–ES–2013–0071).
Several authors have identified both
the presence of nonnative fish as well as
their deleterious effects on native
species within Arizona. Many areas
have seen a shift from a predominance
of native fishes to a predominance of
nonnative fishes. On the upper Verde
River, native species dominated the
total fish community at greater than 80
percent from 1994 to 1996, before
dropping to approximately 20 percent in
1997 and 19 percent in 2001. At the
same time, three nonnative species
increased in abundance between 1994
and 2000 (Rinne et al. 2005, pp. 6–7).
In an assessment of the Verde River,
Bonar et al. (2004, p. 57) found that, in
the Verde River mainstem, nonnative
fishes were approximately 2.6 times
more dense per unit volume of river
than native fishes, and their populations
were approximately 2.8 times that of
native fishes per unit volume of river.
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Similar changes in the dominance of
nonnative fishes have occurred on the
Middle Fork Gila River, with a 65
percent decline of native fishes between
1988 and 2001 (Propst 2002, pp. 21–25).
Abarca and Weedman (1993, pp. 6–12)
found that the number of nonnative fish
species was twice the number of native
fish species in Tonto Creek in the early
1990s, with a stronger nonnative species
influence in the lower reaches, where
the northern Mexican gartersnake is
considered to still occur (Burger 2010,
p. 1, Madera-Yagla 2010, p. 6, 2011, p.
6).
Beginning in 2014, the AGFD plans to
stock 4.6 million Florida-strain
largemouth bass, 3.3 million bluegill,
and 4.5 million black crappie annually
into Roosevelt Lake in order to control
the gizzard shad (Dorosoma
cepedianum) population, which is
currently the most prevalent fish species
in the lake and is thought to be
depressing sport fish populations in the
reservoir (AGFD 2014, p. 3). Roosevelt
Lake is not, and will never be, suitable
habitat for the northern Mexican
gartersnake because of its management
as a sport fishery. However, if the goal
of this effort is achieved, we expect a
higher risk of predation of gartersnakes
in lower Tonto Creek when a suitable
hydrologic connection is made between
Tonto Creek and the lake body
(providing the opportunity for predatory
nonnative fish to move into lower Tonto
Creek). We also expect high risk of
predation of individual snakes that may
disperse downstream into the lake itself.
Fish surveys in the Salt River above
Lake Roosevelt already indicate a
decline of roundtail chub and other
native fishes, with an increase in
flathead and channel catfish numbers
(Voeltz 2002, p. 49).
In New Mexico, nonnative fish have
been identified as the main cause for
declines observed in native fish
populations (Voeltz 2002, p. 40; Propst
et al. 2008, pp. 1242–1243). Fish experts
from the U.S. Forest Service, U.S.
Bureau of Reclamation, U.S. Bureau of
Land Management (BLM), University of
Arizona, Arizona State University, The
Nature Conservancy, and others
declared the native fish fauna of the Gila
River basin to be critically imperiled,
and they cite habitat destruction and
nonnative species as the primary factors
for the declines (DFT 2003, p. 1). They
call for the control and removal of
nonnative fish as an overriding need to
prevent the decline, and possible
extinction, of native fish species within
the basin (DFT 2003, p. 1). In some
areas, nonnative fishes may not
dominate the system, but their
abundance has increased. This is the
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case for the Cliff-Gila Valley area of the
Gila River where nonnative fishes
increased from 1.1 percent to 8.5
percent, while native fishes declined
steadily over a 40-year period (Propst et
al. 1986, pp. 27–32). At the Redrock and
Virden Valleys on the Gila River, the
relative abundance in nonnative fishes
in the same time period increased from
2.4 percent to 17.9 percent (Propst et al.
1986, pp. 32–34). Four years later, the
relative abundance of nonnative fishes
increased to 54.7 percent at these sites
(Propst et al. 1986, pp. 32–36). The
percentage of nonnative fishes increased
by almost 12 percent on the Tularosa
River between 1988 and 2003, while on
the East Fork Gila River, nonnative
fishes increased to 80.5 percent relative
abundance in 2003 (Propst 2005, pp. 6–
7, 23–24).
In addition to harmful nonnative
species, various parasites may affect
native fish species that are prey for
northern Mexican and narrow-headed
gartersnakes. Parasites affecting various
species of native fishes within the range
of these gartersnakes include Asian
tapeworm (U.S. Fish and Wildlife
Service (USFWS) National Wild Fish
Health Survey 2010), Ichthyophthirius
multifiliis (Ich) (Mpoame 1982, p. 46;
Robinson et al. 1998, p. 603), anchor
worm (Lernaea cyprinacea) (Robinson et
al. 1998, pp. 599, 603–605; Hoffnagle
and Cole 1999, p. 24), yellow grub
(Clinostomum marginatum) (Amin
1969, p. 436; Mpoame and Rinne 1983,
pp. 400–401; Bryan and Robinson 2000,
p. 19; Maine Department of Inland
Fisheries and Wildlife 2002a, p. 1), and
black grub (Neascus spp.), also called
black spot (Robinson et al. 1998, p. 603;
Bryan and Robinson 2000, p. 21; Lane
and Morris 2000, pp. 2–3; Maine
Department of Inland Fisheries and
Wildlife 2002b, p. 1; Paroz 2011, pers.
comm.). However, currently, we have no
information on what effect parasite
infestation in native fish might have on
gartersnake populations.
Decline of Native Fish Communities
in Mexico (Northern Mexican
Gartersnake)—The first tabulations of
freshwater fish species at risk in Mexico
occurred in 1961, when 11 species were
identified as being at risk (ContrerasBalderas et al. 2003, p. 242). As of 2003,
of the 506 species of freshwater fish
recorded in Mexico, 185 (37 percent)
have been listed by the Mexican Federal
Government as either endangered,
facing extinction, under special
protection, or likely extinct (AlvarezTorres et al. 2003, p. 323), almost a 17fold increase in slightly over four
decades; 25 species are believed to have
gone extinct (Contreras-Balderas et al.
2003, p. 241). In the lower elevations of
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Mexico, within the distribution of the
northern Mexican gartersnake, there are
approximately 200 species of native
freshwater fish documented, with 120
native species under some form of threat
and an additional 15 that have gone
extinct (Contreras-Balderas and Lozano
1994, pp. 383–384). The Fisheries Law
in Mexico empowered the country’s
National Fisheries Institute to compile
and publish the National Fisheries Chart
in 2000, which found that Mexico’s fish
fauna has seriously deteriorated as a
result of environmental impacts
(pollution), water basin degradation
(dewatering, siltation), and the
introduction of nonnative species
(Alvarez-Torres et al. 2003, pp. 320,
323). The National Fisheries Chart is
regarded as the first time the Mexican
Government has openly revealed the
status of its freshwater fisheries and
described their management policies
(Alvarez-Torres et al. 2003, pp. 323–
324).
Industrial, municipal, and agricultural
water pollution, dewatering of aquatic
habitat, and the proliferation of
nonnative species are widely considered
to be the greatest threats to freshwater
ecosystems in Mexico (Branson et al.
1960, p. 218; Conant 1974, pp. 471,
487–489; Miller et al. 1989, pp. 25–26,
28–33; 2005, pp. 60–61; DeGregorio
1992, p. 60; Contreras Balderas and
Lozano 1994, pp. 379–381; Lyons et al.
1995, p. 572; 1998, pp. 10–12; Landa et
al. 1997, p. 316; Mercado-Silva et al.
2002, p. 180; Contreras-Balderas et al.
´
´
2003, p. 241; Domınguez-Domınguez et
al. 2007, Table 3). A shift in land use
policies in Mexico to encourage free
market principles in rural, small-scale
agriculture has been found to promote
land use practices that threaten local
biodiversity (Ortega-Huerta and Kral
2007, p. 2; Randall 1996, pp. 218–220;
Kiernan 2000, pp. 13–23).
These threats have been documented
throughout the distribution of the
northern Mexican gartersnake in Mexico
and are best represented in the scientific
literature in the context of fisheries
studies. Contreras-Balderas et al. (2003,
pp. 241, 243) named Chihuahua (46
species), Coahuila (35 species), Sonora
(19 species), and Durango (18 species)
as Mexican states that had some of the
most reports of freshwater fish species
at risk. These states are all within the
distribution of the northern Mexican
gartersnake, indicating an overlapping
trend of declining prey bases and
threatened ecosystems within the range
of the northern Mexican gartersnake in
Mexico. Contreras-Balderas et al. (2003,
Appendix 1) found various threats to be
adversely affecting the status of
freshwater fish and their habitat in
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several states in Mexico: (1) Habitat
reduction or alteration (Sonora,
Chihuahua, Durango, Coahuila, San
´
Luis Potosı, Jalisco, Guanajuato); (2)
water depletion (Chihuahua, Durango,
Coahuila, Sonora, Guanajuato, Jalisco,
´
San Luis Potosı); (3) harmful nonnative
species (Durango, Chihuahua, Coahuila,
´
San Luis Potosı, Sonora, Veracruz); and
´
(4) pollution (Mexico, Jalisco,
Chihuahua, Coahuila, Durango). Within
the states of Chihuahua, Durango,
Coahuila, Sonora, Jalisco, and
Guanajuato water depletion is
considered serious, with entire basins
having been dewatered, or conditions
have been characterized as ‘‘highly
altered’’ (Contreras-Balderas et al. 2003,
Appendix 1). All of the Mexican states
with the highest numbers of fish species
at risk are considered arid, a condition
hastened by increasing desertification
(Contreras-Balderas et al. 2003, p. 244).
Aquaculture and Nonnative Fish
Proliferation in Mexico (Northern
Mexican Gartersnake)—Nonnative fish
compete with and prey upon northern
Mexican gartersnakes and their native
prey species. The proliferation of
nonnative fish species throughout
Mexico happened mainly by natural
dispersal, intentional stockings, and
accidental breaches of artificial or
constructed barriers by nonnative fish
(Welcomme 1984, entire). Lentic water
bodies such as lakes, reservoirs, and
ponds are often used for flood control,
agricultural purposes, and most
commonly to support commercial
fisheries. The most recent estimates
indicate that Mexico has 13,936 of such
water bodies, where approximately 96
percent are between 2.47–247 acres (1–
100 hectares) and approximately half
are artificial (Sugunan 1997, Table 8.3;
Alvarez-Torres et al. 2003, pp. 318,
322). Areas where these landscape
features are most prevalent occur within
the distribution of the northern Mexican
gartersnake. For example, Jalisco and
Zacatecas are listed as two of four states
with the highest number of reservoirs,
and Chihuahua is one of two states
known for a high concentration of lakes
(Sugunan 1997, Section 8.4.2).
Based on the data presented in
Sugunan (1997, Table 8.5), a total of 422
dammed reservoirs are located within
the 16 Mexican states where the
northern Mexican gartersnake is thought
to occur. Mercado-Silva et al. (2006, p.
534) found that, within the state of
Guanajuato, ‘‘Practically all streams and
rivers in the (Laja) basin are truncated
by reservoirs or other water extraction
and storage structures.’’ On the Laja
River alone, there are two major
reservoirs and a water diversion dam; 12
more reservoirs are located on its
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tributaries (Mercado-Silva et al. 2006, p.
534). As a consequence of dam
operations, the main channel of the Laja
remains dry for extensive periods of
time (Mercado-Silva et al. 2006, p. 541).
The damming and modification of the
lower Colorado River in Mexico, where
the northern Mexican gartersnake
occurred, has facilitated the
replacement of the entire native fishery
with nonnative species (Miller et al.
2005, p. 61). Each reservoir created by
a dam is either managed as a nonnative
commercial fishery or has become a
likely source population of nonnative
species, which have naturally or
artificially colonized the reservoir,
dispersed into connected riverine
systems, and damaged native aquatic
communities.
Mexico depends in large part on
freshwater commercial fisheries as a
source of protein for both urbanized and
rural human populated areas.
Commercial and subsistence fisheries
rely heavily on introduced, nonnative
species in the largest freshwater lakes
(Soto-Galera et al. 1999, p. 133) down to
rural, small ponds (Tapia and Zambrano
2003, p. 252). At least 87 percent of the
species captured or cultivated in inland
fisheries of Mexico from 1989–1999
included tilapia (Tilapia spp.), common
carp (Cyprinus carpio), channel catfish,
trout, and black bass (Micropterus sp.),
all of which are nonnative (AlvarezTorres et al. 2003, pp. 318, 322). In fact,
the northern and central plateau region
of Mexico (which comprises most of the
distribution of the northern Mexican
gartersnake’s distribution in Mexico) is
considered ideal for the production of
harmful, predatory species such as bass
and catfish (Sugunan 1997, Section 8.3).
Largemouth bass are now produced and
stocked in reservoirs and lakes
throughout the distribution of the
northern Mexican gartersnake (Sugunan
1997, Section 8.8.1).
The Secretariat for Environment,
Natural Resources and Fisheries
(SEMARNAP), formed in 1995, is the
Mexican federal agency responsible for
management of the country’s
environment and natural resources.
SEMARNAP dictates the stocking rates
of nonnative species into the country’s
lakes and reservoirs. For example, the
permitted stocking rate for largemouth
bass in Mexico is one fish per square
meter in large reservoirs (Sugunan 1997,
Table 8.8); therefore, a 247-acre (100-ha)
reservoir could be stocked with
1,000,000 largemouth bass. The
common carp, the subject of significant
aquaculture investment since the 1960s
in Mexico, is known for altering aquatic
habitat and consuming the eggs and fry
of native fish species, and is now
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established in 95 percent of Mexico’s
freshwater systems (Tapia and
Zambrano 2003, p. 252).
Basins in northern Mexico, such as
the Rio Yaqui, have been found to be
significantly compromised by harmful
nonnative fish species. Unmack and
Fagan (2004, p. 233) compared
historical museum collections of
nonnative fish species from the Gila
River basin in Arizona and the Yaqui
River basin in Sonora, Mexico, to gain
insight into the trends in distribution,
diversity, and abundance of nonnative
fishes in each basin over time. They
found that nonnative species are slowly,
but steadily, increasing in all three
parameters in the Yaqui Basin (Unmack
and Fagan 2004, p. 233). Unmack and
Fagan (2004, p. 233) predicted that, in
the absence of aggressive management
intervention, significant extirpations or
range reductions of native fish species
are expected to occur in the Yaqui Basin
of Sonora, Mexico, which may have
extant populations of the northern
Mexican gartersnake, as did much of the
Gila Basin before the introduction of
nonnative species. Loss of native fishes
impacts prey availability for the
northern Mexican gartersnake and
threatens its persistence in these areas.
Black bullheads (Ameiurus melas) were
reported as abundant, and common carp
were detected from the Rio Yaqui in
southern Sonora, Mexico (Branson et al.
1960, p. 219). Bluegill (Lepomis
macrochirus) were also reported at this
location, representing a significant range
expansion that the authors expected was
the result of escaping nearby farm ponds
or irrigation ditches (Branson et al.
1960, p. 220). Largemouth bass, green
sunfish, and an undetermined crappie
species have also been reported from
this area (Branson et al. 1960, p. 220).
Documented problems with aquatic
habitats in Mexico include water
pollution, harmful nonnative species,
and physical habitat alteration. All of
these factors lead to declines in native
fish abundance and, therefore, a decline
in the food source for the northern
´
Mexican gartersnake. Domınguez´
Domınguez et al. (2007, p. 171) sampled
52 localities for a rare freshwater fish,
the Picotee goodeid (Zoogoneticus
quitzeoensis), along the southern
portion of the Mesa Central (Mexican
Plateau) of Mexico and found 21
localities had significant signs of
pollution. Of the 29 localities where the
target species was detected, 28 of them
also had harmful nonnative species
present, such as largemouth bass,
cichlids (Oreochromis sp.), bluegill, and
´
Patzcuaro chub (Algansea lacustris)
´
´
(Domınguez-Domınguez et al. 2007, pp.
171, Table 3). The first assessment of the
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impacts of largemouth bass on native
fishes in Mexico was in 1941 during the
examination of their effect in Lago de
´
Patzcuaro (Contreras and Escalante
1984, p. 102). Other nonnative fish
species reported are soft-rayed and
small bodied, and may be prey items for
younger age classes of gartersnakes.
Several examples of significant
aquatic habitat degradation or
destruction were also observed by
´
´
Domınguez-Domınguez et al. (2007,
Table 3) in this region of Mexico,
including the draining of natural lakes
and cienegas for conversion to
agricultural purposes, modification of
springs for recreational swimming,
diversions, and dam construction. It
should be noted that approximately 17
percent of the localities sampled by
´
´
Domınguez-Domınguez et al. (2007,
entire) are within the likely range of the
northern Mexican gartersnake; chiefly
sites located within the Rio Grande de
Santiago and Laja Basin. However,
collectively, observations made by
´
´
Domınguez-Domınguez et al. (2007,
entire) provide a regional context to
potential threats acting on northern
Mexican gartersnakes in their southernmost distribution. As of 2006, native
fish species dominated the fish
community in both species composition
and overall abundance in the Laja Basin;
however, the basin is now trending
toward a nonnative fishery compared to
historical data. For example, nonnative
species were most recently collected
from 16 of 17 sample sites in the basin,
with largemouth bass significantly
expanding their distribution within the
headwaters of the basin and bluegill
being widespread in the Laja River
(Mercado-Silva et al. 2006, pp. 537, 542,
Table 4). The decline of native fishes in
this region of Mexico is likely negatively
affecting the status of the northern
Mexican gartersnakes there.
Harmful nonnative fish species in
Mexico (Contraras and Escalante 1984,
pp. 102–125) may be posing a
significant threat to the native fish prey
base of northern Mexican gartersnakes
and to the gartersnakes themselves. The
ecological risk of nonnative, freshwater
fishes is only expected to increase with
increases in aquaculture production,
most notably in the country’s rural,
poorest regions (Tapia and Zambrano
2003, p. 252). Amendments to Mexico’s
existing fishing regulations imposed by
other government regulations have been
relaxed, and investment in commercial
fishing has expanded to promote growth
in Mexico’s aquaculture sector
(Sugunan 1997, Section 8.7.1). Several
areas within the range of the northern
Mexican gartersnake in Mexico have
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experienced adverse effects associated
with nonnative species.
Amphibian Decline (Northern
Mexican Gartersnake)—Amphibians are
a principle prey item for the northern
Mexican gartersnake, and documented
declines in amphibian population
densities and distributions have
significantly contributed to the decline
in northern Mexican gartersnakes. As an
example of these effects from another
region, Matthews et al. (2002, p. 16)
examined the relationship of
gartersnake distributions, amphibian
population declines, and nonnative fish
introductions in high-elevation aquatic
ecosystems in California. Matthews et
al. (2002, p. 16) specifically examined
the effect of nonnative trout
introductions on populations of
amphibians and mountain gartersnakes
(Thamnophis elegans elegans). Their
results indicated that the probability of
observing gartersnakes was 30 times
greater in lakes containing amphibians
than in lakes where amphibians have
been extirpated by nonnative fish. These
results supported a prediction by
Jennings et al. (1992, p. 503) that native
amphibian declines will lead directly to
gartersnake declines.
Declines in the native leopard frog
populations in Arizona have likely been
a significant, contributing factor to
declines in many northern Mexican
gartersnake populations. Native ranid
(of the family Ranidae) frog species,
such as lowland leopard frogs, northern
leopard frogs, and federally threatened
Chiricahua leopard frogs, have
experienced declines in various degrees
throughout their distribution in the
Southwest, largely due to predation and
competition with nonnative species
(Clarkson and Rorabaugh 1989, pp. 531,
535; Hayes and Jennings 1986, p. 490).
Rosen et al. (1995, pp. 257–258) found
that Chiricahua leopard frog distribution
in the Chiricahua Mountain region of
Arizona was inversely related to
nonnative species distribution. Along
the Mogollon Rim, Holycross et al.
(2006, p. 13) found that only 8 sites of
57 surveyed (15 percent) consisted of an
entirely native anuran (of the order
Anura) community and that native frog
populations in another 19 sites (33
percent) had been completely displaced
by invading bullfrogs. However, such
declines in native frog populations are
not necessarily irreversible. Ranid frog
populations have been shown to
rebound strongly when nonnative fish
are removed (Knapp et al. 2007, pp. 15–
18).
Scotia Canyon, in the Huachuca
Mountains of southeastern Arizona, is a
location where corresponding declines
of leopard frog and northern Mexican
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gartersnake populations have been
documented through repeated survey
efforts over time (Holm and Lowe 1995,
p. 33). Surveys of Scotia Canyon
occurred during the early 1980s and
again during the early 1990s. Leopard
frogs in Scotia Canyon were
infrequently observed during the early
1980s and were nearly extirpated by the
early 1990s (Holm and Lowe 1995, pp.
45–46). Northern Mexican gartersnakes
were observed in decline during the
early 1980s, with low capture rates
continuing through the early 1990s
(Holm and Lowe 1995, pp. 27–35).
Surveys documented further decline of
leopard frogs and northern Mexican
gartersnakes in 2000 (Rosen et al. 2001,
pp. 15–16).
A former large, local population of
northern Mexican gartersnakes at the
San Bernardino National Wildlife
Refuge (SBNWR) in southeastern
Arizona has also experienced a
correlative decline of leopard frogs, and
northern Mexican gartersnakes are now
thought to occur at very low population
densities or may be extirpated there
(Rosen and Schwalbe 1988, p. 28; 1995,
p. 452; 1996, pp. 1–3; 1997, p. 1; 2002b,
pp. 223–227; 2002c, pp. 31, 70; Rosen
et al. 1996b, pp. 8–9; 2001, pp. 6–10).
Survey data indicate that declines of
leopard frog populations, often
correlated with nonnative species
introductions, the spread of a chytrid
fungus (Batrachochytrium
dendrobatidis, Bd), and habitat
modification and destruction, have
occurred throughout much of the
northern Mexican gartersnake’s U.S.
distribution (Nickerson and Mays 1970,
p. 495; Vitt and Ohmart 1978, p. 44;
Ohmart et al. 1988, p. 150; Rosen and
Schwalbe 1988, Appendix I; 1995, p.
452; 1996, pp. 1–3; 1997, p. 1; 2002b,
pp. 232–238; 2002c, pp. 1, 31; Clarkson
and Rorabaugh 1989, pp. 531–538; Sredl
et al. 1995a, pp. 7–8; 1995b, pp. 8–9,
1995c, pp. 7–8; 2000, p. 10; Holm and
Lowe 1995, pp. 45–46; Rosen et al.
1996b, p. 2; 2001, pp. 2, 22; Degenhardt
et al. 1996, p. 319; Fernandez and Rosen
1996, pp. 6–20; Drost and Nowak 1997,
p. 11; Turner et al. 1999, p. 11; Nowak
and Spille 2001, p. 32; Holycross et al.
2006, pp. 13–14, 52–61). Holycross et al.
(2006, pp. 53–57, 59) documented
population declines and potential
extirpations of lowland leopard frogs
(an important prey species of the
northern Mexican gartersnake) in most
of the Agua Fria subbasin and areas of
the Salt and Verde subbasins in the
period 1986–2006. Specifically,
Holycross et al. (2006, pp. 53–57, 59)
detected no lowland leopard frogs at
several recently, historically, or
potentially occupied locations,
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including the Agua Fria River in the
vicinity of Table Mesa Road and Little
Grand Canyon Ranch, and at Rock
Springs, Dry Creek from Dugas Road to
Little Ash Creek, Little Ash Creek from
Brown Spring to Dry Creek, Sycamore
Creek (Agua Fria subbasin) in the
vicinity of the Forest Service Cabin, the
Page Springs and Bubbling Ponds fish
hatchery along Oak Creek, Sycamore
Creek (Verde River subbasin) in the
vicinity of the confluence with the
Verde River north of Clarkdale, along
several reaches of the Verde River
mainstem, Cherry Creek on the east side
of the Sierra Ancha Mountains, and
Tonto Creek from Gisela to ‘‘the Box,’’
near its confluence with Rye Creek.
Rosen et al. (2013, p. 8) suggested that
the decline of leopard frogs in the
Empire Valley of southern Arizona is
likely largely responsible for the decline
of the northern Mexican gartersnake
there.
A primary factor in the decline of
native amphibians as a food source for
northern Mexican gartersnakes in
southern Arizona is likely the result of
impacts from nonnative species, mainly
bullfrogs. Rosen et al. (1995, pp. 252–
253) sampled aquatic herpetofauna at
103 sites in the Chiricahua Mountains
region, which included the Chiricahua,
Dragoon, and Peloncillo Mountains, and
the Sulphur Springs, San Bernardino,
and San Simon valleys. They found that
43 percent of all ectothermic (coldblooded) aquatic and semi-aquatic
vertebrate species detected were
nonnative. The most commonly
encountered nonnative species was the
bullfrog (Rosen et al. 1995, p. 254).
Witte et al. (2008, p. 1) found that the
disappearance of ranid frog populations
in Arizona were 2.6 times more likely in
the presence of crayfish. Witte et al.
(2008, p. 7) emphasized the significant
influence of nonnative species on the
disappearance of ranid frogs in Arizona.
In one area, Rosen et al. (2001, p. 22)
identified the expansion of bullfrogs
into the Sonoita grasslands, which
contain occupied northern Mexican
gartersnake habitat, and the
introduction of crayfish into Lewis
Springs as being of particular concern
for the northern Mexican gartersnake in
that area.
In addition to harmful nonnative
species, disease and nonnative parasites
have been implicated in the decline of
the prey base of the northern Mexican
gartersnake. In particular, the outbreak
of chytridiomycosis or ‘‘Bd,’’ a skin
fungus, has been identified as a chief
causative agent in the significant
declines of many of the native ranid
frogs and other amphibian species. As
indicated, Bd has been implicated in
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both large-scale declines and local
extirpations of many amphibians,
chiefly anuran species, around the
world (Johnson 2006, p. 3011). Lips et
al. (2006, pp. 3166–3169) suggest that
the high virulence and large number of
potential hosts make Bd a serious threat
to amphibian diversity. In Arizona, Bd
infections have been reported in several
of the native prey species of the
northern Mexican gartersnake within
the distribution of the snake (Morell
1999, pp. 731–732; Sredl and Caldwell
2000, p. 1; Hale 2001, pp. 32–37;
Bradley et al. 2002, p. 207; USFWS
2002, pp. 40802–40804; USFWS 2007a,
pp. 26, 29–32). Declines of native prey
species of the northern Mexican
gartersnake from Bd infections have
contributed to the decline of this species
in the United States (Morell 1999, pp.
731–732; Sredl and Caldwell 2000, p. 1;
Hale 2001, pp. 32–37; Bradley et al.
2002, p. 207; USFWS 2002, pp. 40802–
40804; USFWS 2007a, pp. 26, 29–32).
Evidence of Bd-related amphibian
declines has been confirmed in portions
of southern Mexico (just outside the
range of northern Mexican
gartersnakes), and data suggest declines
are more prevalent at higher elevations
where northern Mexican gartersnakes
can occur (Lips et al. 2004, pp. 560–
562). However, much less is known
about the role of Bd in amphibian
declines across much of Mexico, in
particular the mountainous regions of
Mexico (including much of the range of
northern Mexican gartersnakes in
Mexico) as the region is significantly
understudied (Young et al. 2000, p.
1218). Because narrow-headed
gartersnakes feed on fish, Bd has not
affected their prey base. A recent study
in Panama by Kilburn et al. (2011, p.
132) found that reptiles may act as
reservoirs for Bd (at least in
environments such as Panama) based on
the presence of the fungus at nonpathological levels on lizards that occur
in areas with significant Bd outbreaks in
resident amphibians. Their study did
not conclude that Bd is a virulent reptile
pathogen, or that it causes diseaseinduced population declines in reptiles
(Kilburn et al. 2011, p. 132).
Effects of Bullfrogs on Native Aquatic
Communities (Northern Mexican and
Narrow-Headed Gartersnakes) (Factors
A, C, and E)
Direct predation by, and competition
with, bullfrogs is a serious threat to
northern Mexican gartersnakes
throughout their range (Conant 1974,
pp. 471, 487–489; Rosen and Schwalbe
1988, pp. 28–30; Rosen et al. 2001, pp.
21–22). Bullfrogs have and do threaten
some populations of narrow-headed
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gartersnakes, but differing habitat
preferences between bullfrogs and
narrow-headed gartersnakes lessen their
effect on narrow-headed gartersnake
populations. Bullfrogs adversely affect
northern Mexican and narrow-headed
gartersnake populations through direct
predation of juveniles and sub-adults.
Bullfrogs also compete with northern
Mexican gartersnakes for prey species.
Bullfrogs are not native to the
southwestern United States or Mexico,
and they first appeared in Arizona in
1926 as a result of a systematic
introduction effort by the State Game
Department (now, the AGFD) for the
purposes of sport hunting and as a food
source (Tellman 2002, p. 43). The first
bullfrog record from New Mexico is
dated 1885 (Degenhardt et al. 1996, p.
85). Bullfrogs are extremely prolific, are
strong colonizers, can reach high
densities, are persistent via cannibalism,
and may disperse distances of up to 10
mi (16 km) across uplands and likely
further within drainages (Bautista 2002,
p. 131; Rosen and Schwalbe 2002a, p. 7;
Casper and Hendricks 2005, p. 582;
Suhre 2008, pers. comm.; Rosen et al.
2013, pp. 35–36).
Bullfrogs are large-bodied, voracious,
opportunistic, even cannibalistic
predators that readily attempt to
consume any living thing smaller than
them. Bullfrogs have a highly varied
diet, which has been documented to
include vegetation, invertebrates, fish,
birds, mammals, amphibians, and
reptiles, including numerous species of
snakes (eight genera, including six
different species of gartersnakes, two
species of rattlesnakes, and Sonoran
gophersnakes (Pituophis catenifer
affinis)) (Bury and Whelan 1984, p. 5;
Clarkson and DeVos 1986, p. 45; Holm
and Lowe 1995, pp. 37–38; Carpenter et
al. 2002, p. 130; King et al. 2002; Hovey
and Bergen 2003, pp. 360–361; Casper
and Hendricks 2005, pp. 543–544;
Combs et al. 2005, p. 439; Wilcox 2005,
p. 306; DaSilva et al. 2007, p. 443; Neils
and Bugbee 2007, p. 443; Rowe and
Garcia 2012, pp. 633–634). In one study,
three different species of gartersnakes
(Thamnophis sirtalis, T. elegans, and T.
ordinoides) totaling 11 snakes were
found inside the stomachs of resident
bullfrogs from a single region
(Jancowski and Orchard 2013, p. 26).
Bullfrogs can significantly reduce or
eliminate the native amphibian
populations (Moyle 1973, pp. 18–22;
Conant 1974, pp. 471, 487–489; Hayes
and Jennings 1986, pp. 491–492; Rosen
and Schwalbe 1988, pp. 28–30; 2002b,
pp. 232–238; Rosen et al. 1995, pp. 257–
258; 2001, pp. 2, Appendix I; Wu et al.
2005, p. 668; Pearl et al. 2004, p. 18;
Kupferberg 1994, p. 95; Kupferburg
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1997, pp. 1736–1751; Lawler et al. 1999;
Bury and Whelan 1986, pp. 9–10; Hayes
and Jennings 1986, pp. 500–501; Jones
and Timmons 2010, pp. 473–474),
which are vital for northern Mexican
gartersnakes.
Different age classes of bullfrogs can
affect native ranid populations via
different mechanisms. Juvenile bullfrogs
affect native ranids through
competition; male bullfrogs affect native
ranids through predation; and female
bullfrogs affect native ranids through
both mechanisms depending on body
size and microhabitat (Wu et al. 2005,
p. 668). Pearl et al. (2004, p. 18) also
suggested that the effect of bullfrog
introductions on native ranids may be
different based on specific habitat
conditions but also suggested that an
individual ranid frog species’ physical
ability to escape influences the effect of
bullfrogs on each native ranid
community. Bullfrogs can also
negatively affect native ranid frog
populations, both locally and regionally,
as carriers or reservoir species for Bd,
depending on the strain of Bd (Gervasi
et al. 2013, p. 169).
Bullfrogs have been documented to
occur throughout Arizona. Holycross et
al. (2006, pp. 13–14, 52–61) found
bullfrogs at 55 percent of sample sites in
the Agua Fria subbasin, 62 percent of
sites in the Verde River subbasin, 25
percent of sites in the Salt River
subbasin, and 22 percent of sites in the
Gila River subbasin. In total, bullfrogs
were observed at 22 of the 57 sites
surveyed (39 percent) across the
Mogollon Rim (Holycross et al. 2006, p.
13). A number of authors have also
documented the presence of bullfrogs
throughout many subbasins in Arizona
and New Mexico adjacent to the
historical distribution of the northern
Mexican or narrow-headed gartersnake,
including northern Arizona (Sredl et al.
1995a, p. 7; 1995c, p. 7), central Arizona
and along the Mogollon Rim of Arizona
and New Mexico (Nickerson and Mays
1970, p. 495; Hulse 1973, p. 278; Sredl
et al. 1995b, p. 9; Drost and Nowak
1997, p. 11; Nowak and Spille 2001, p.
11; Holycross et al. 2006, pp. 15–51;
Wallace et al. 2008; pp. 243–244;
Hellekson 2012a, pers. comm.),
southern Arizona (Rosen and Schwalbe
1988, Appendix I; 1995, p. 452; 1996,
pp. 1–3; 1997, p. 1; 2002b, pp. 223–227;
2002c, pp. 31, 70; Holm and Lowe 1995,
pp. 27–35; Rosen et al. 1995, p. 254;
1996a, pp. 16–17; 1996b, pp. 8–9; 2001,
Appendix I; Turner et al. 1999, p. 11;
Sredl et al. 2000, p. 10; Turner 2007; p.
41), and along the Colorado River (Vitt
and Ohmart 1978, p. 44; Clarkson and
DeVos 1986, pp. 42–49; Ohmart et al.
1988, p. 143). In one of the more
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conspicuous examples, bullfrogs were
identified as the primary cause for
collapse of the northern Mexican
gartersnake and its prey base on the
SBNWR (Rosen and Schwalbe 1988, p.
28; 1995, p. 452; 1996, pp. 1–3; 1997, p.
1; 2002b, pp. 223–227; 2002c, pp. 31,
70; Rosen et al. 1996b, pp. 8–9).
Once established, bullfrogs are
persistent in an area and very difficult
to eradicate. Rosen and Schwalbe (1995,
p. 452) experimented with bullfrog
removal at various sites on the SBNWR,
in addition to a control site with no
bullfrog removal in similar habitat on
the Buenos Aires National Wildlife
Refuge (BANWR). Removal of adult
bullfrogs, without removal of eggs and
tadpoles, resulted in a substantial
increase in younger age-class bullfrogs
where removal efforts were the most
intensive (Rosen and Schwalbe 1997, p.
6). Contradictory to the goals of bullfrog
eradication, evidence from dissection
samples from young adult and subadult
bullfrogs indicated these age-classes
readily prey upon juvenile bullfrogs (up
to the average adult leopard frog size) as
well as juvenile gartersnakes, which
suggests that the selective removal of
only the large adult bullfrogs (presumed
to be the most dangerous size class to
leopard frogs and gartersnakes), favoring
the young adult and sub-adult age
classes, could indirectly lead to
increased predation of leopard frogs and
juvenile gartersnakes (Rosen and
Schwalbe 1997, p. 6). These findings
illustrate that, in addition to large
adults, sub-adult bullfrogs also
negatively impact northern Mexican
gartersnakes and their prey species. The
findings also indicate the importance of
including egg mass and tadpole removal
during efforts to control bullfrogs and
timing removal projects to ensure
reproductive bullfrogs are removed
prior to breeding. Recent success in
regional bullfrog eradication has been
found in a few cases described below in
the section entitled ‘‘Current
Conservation of Northern Mexican and
Narrow-headed Gartersnakes.’’
Bullfrogs not only compete with the
northern Mexican gartersnake for prey
items but directly prey upon juvenile
and, occasionally, sub-adult northern
Mexican and narrow-headed
gartersnakes (Rosen and Schwalbe 1988,
pp. 28–31; 1995, p. 452; 2002b, pp. 223–
227; Holm and Lowe 1995, pp. 29–29;
Rossman et al. 1996, p. 177; AGFD In
Prep., p. 12; 2001, p. 3; Rosen et al.
2001, pp. 10, 21–22; Carpenter et al.
2002, p. 130; Wallace 2002, p. 116). A
well-circulated photograph of an adult
bullfrog in the process of consuming a
northern Mexican gartersnake at Parker
Canyon Lake, Cochise County, Arizona,
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taken by John Carr of the AGFD in 1964,
provides photographic documentation
of bullfrog predation (Rosen and
Schwalbe 1988, p. 29; 1995, p. 452). The
most recent, physical evidence of
bullfrog predation of northern Mexican
gartersnakes is provided in photographs
of a dissected bullfrog at Pasture 9 Tank
in the San Rafael Valley of Arizona that
had a freshly eaten neonatal northern
Mexican gartersnake in its stomach
(Akins 2012, pers. comm.).
A common observation in northern
Mexican gartersnake populations that
co-occur with bullfrogs is a
preponderance of large, mature adult
snakes with conspicuously low numbers
of individuals in the newborn and
juvenile age size classes. This occurs
due to bullfrogs preying on young small
snakes more effectively, which leads to
reduced survival of young and
depressed recruitment within
populations (Rosen and Schwalbe 1988,
p. 18; Holm and Lowe 1995, p. 34). In
lotic (flowing water) systems, bullfrogs
prefer sites with low or limited flow,
such as backwaters, side channels, and
pool habitat. These areas are also used
frequently by northern Mexican and
narrow-headed gartersnakes, which
likely results in increased predation
rates and likely depressed recruitment
of gartersnakes. Potential recruitment
problems for northern Mexican
gartersnakes due to effects from
nonnative species are suspected at
Tonto Creek (Wallace et al. 2008, pp.
243–244). Rosen and Schwalbe (1988, p.
18) stated that the low recruitment at
the SBNWR, a typical characteristic of
gartersnake populations affected by
harmful nonnative species, is the likely
cause of that populations’ decline and
possibly for declines in populations
throughout their range in Arizona.
Specific localities within the
distribution of northern Mexican and
narrow-headed gartersnakes where
bullfrogs have been detected are
presented in Appendix A (available at
https://www.regulations.gov, Docket No.
FWS–R2–ES–2013–0071).
Effects of Crayfish on Native Aquatic
Communities (Northern Mexican and
Narrow-Headed Gartersnakes) (Factors
A and C)
Crayfish are another nonnative
species in Arizona and New Mexico that
threaten northern Mexican and narrowheaded gartersnakes through
competition by consuming prey species
of the gartersnakes and through direct
predation on juvenile gartersnakes
themselves (Fernandez and Rosen 1996,
p. 25; Voeltz 2002, pp. 87–88; USFWS
2007a, p. 22). Rogowski et al. (2013, p.
1,280) found Arizona’s aquatic
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communities to be particularly
vulnerable to crayfish because many
endemic aquatic species never evolved
in the presence of crayfish. Fernandez
and Rosen (1996, p. 3) studied the
effects of crayfish introductions on two
stream communities in Arizona, a lowelevation semi-desert stream and a high
mountain stream, and concluded that
crayfish can noticeably reduce species
diversity and destabilize food chains in
riparian and aquatic ecosystems through
their effect on vegetative structure,
stream substrate (stream bottom; i.e.,
silt, sand, cobble, boulder) composition,
and predation on eggs, larval, and adult
forms of native invertebrate and
vertebrate species. Crayfish fed on
embryos, tadpoles, newly
metamorphosed frogs, and adult leopard
frogs, but they did not feed on egg
masses (Fernandez and Rosen 1996, p.
25). However, Gamradt and Kats (1996,
p. 1155) found that crayfish readily
consumed the egg masses of California
newts (Taricha torosa). Crayfish are
known to also eat fish eggs and larva
(Inman et al. 1998, p. 17), especially
those bound to the substrate (Dorn and
Mittlebach 2004, p. 2135). Fernandez
and Rosen (1996, pp. 6–19, 52–56) and
Rosen (1987, p. 5) discussed
observations of inverse relationships
between crayfish abundance and native
reptile and amphibian populations,
including narrow-headed gartersnakes,
northern leopard frogs, and Chiricahua
leopard frogs. Crayfish may also affect
native fish populations. Carpenter
(2005, pp. 338–340) documented that
crayfish may reduce the growth rates of
native fish through competition for food
and noted that the significance of this
impact may vary between species.
Crayfish alter the abundance and
structure of aquatic vegetation by
grazing on aquatic and semiaquatic
vegetation, which reduces the cover
needed by frogs and gartersnakes, as
well as the food supply for prey species
such as tadpoles (Fernandez and Rosen
1996, pp. 10–12). Fernandez and Rosen
(1996, pp. 10–12) found that crayfish
frequently burrow into stream banks,
leading to increased bank erosion,
stream turbidity, and siltation of stream
bottoms. Creed (1994, p. 2098) found
that filamentous alga (Cladophora
glomerata) was at least 10-fold greater in
aquatic habitats that lacked crayfish.
Filamentous algae is an important
component of aquatic vegetation that
provides cover for foraging gartersnakes,
as well as microhabitat for prey species,
in situations where predation risk is
high.
Crayfish have recently been found to
also act as a host for the amphibian
disease-causing fungus, Bd (McMahon
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et al. 2013, pp. 210–213). This could
have serious implications for northern
Mexican gartersnakes because crayfish
can now be considered a source of
disease in habitat that is devoid of
amphibians but otherwise potentially
suitable habitat for immigrating
amphibians, such as leopard frogs,
which could serve as a prey base.
Because crayfish are so widespread
throughout Arizona, New Mexico, and
portions of Mexico, the scope of this
threat is significant for native
amphibian populations and, therefore,
to northern Mexican gartersnake
populations.
Inman et al. (1998, p. 3) documented
crayfish as widely distributed and
locally abundant in a broad array of
natural and artificial free-flowing and
still-water habitats throughout Arizona,
many of which overlap the historical
and current distribution of northern
Mexican and narrow-headed
gartersnakes. Hyatt (undated, p. 71)
concluded that the majority of waters in
Arizona contained at least one species
of crayfish. In surveying for northern
Mexican and narrow-headed
gartersnakes, Holycross et al. (2006, p.
14) found crayfish in 64 percent of the
sample sites in the Agua Fria subbasin;
in 85 percent of the sites in the Verde
River subbasin; in 46 percent of the sites
in the Salt River subbasin; and in 67
percent of the sites in the Gila River
subbasin. In total, crayfish were
observed at 35 (61 percent) of the 57
sites surveyed across the Mogollon Rim
(Holycross et al. 2006, p. 14), most of
which were sites historically or
currently occupied by northern Mexican
or narrow-headed gartersnakes, or sites
the investigators believed possessed
suitable habitat and may be occupied by
these gartersnakes based upon their
known historical distributions.
A number of authors have
documented the presence of crayfish
through their survey efforts throughout
Arizona and New Mexico in specific
regional areas, drainages, and lentic
wetlands within or adjacent to the
historical distribution of the northern
Mexican or narrow-headed gartersnake,
including northern Arizona (Sredl et al.
1995a, p. 7; 1995c, p. 7), central Arizona
and along the Mogollon Rim of Arizona
and New Mexico (Sredl et al. 1995b, p.
9; Fernandez and Rosen 1996, pp. 54–
55, 71; Inman et al. 1998, Appendix B;
Nowak and Spille 2001, p. 33; Holycross
et al. 2006, pp. 15–51; Brennan 2007, p.
7; Burger 2008, p. 4; Wallace et al. 2008;
pp. 243–244; Brennan and Rosen 2009,
p. 9; Karam et al. 2009; pp. 2–3;
Hellekson 2012a, pers. comm.),
southern Arizona (Rosen and Schwalbe
1988, Appendix I; Inman et al. 1998,
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Appendix B; Sredl et al. 2000, p. 10;
Rosen et al. 2001, Appendix I), and
along the Colorado River (Ohmart et al.
1988, p. 150; Inman et al. 1998,
Appendix B). Specific localities within
the distribution of northern Mexican
and narrow-headed gartersnakes where
crayfish have been detected are
presented in Appendix A (available at
https://www.regulations.gov, Docket No.
FWS–R2–ES–2013–0071). Like
bullfrogs, crayfish can be very difficult,
if not impossible, to eradicate once they
have become established in an area,
depending on the complexity of the
habitat (Rosen and Schwalbe 1996a, pp.
5–8; 2002a, p. 7; Hyatt undated, pp. 63–
71).
It is likely that crayfish populations,
where they overlap with northern
Mexican or narrow-headed gartersnakes,
could have a varied influence on
gartersnake populations. The size of
crayfish can influence their predatory
influence on gartersnakes or their prey
species; small crayfish are unlikely to
pose a significant threat to gartersnakes
themselves but may still consume fish
eggs or fry, whereas larger crayfish can
prey on neonatal gartersnakes directly.
The presence of adequate numbers of
favorable fish prey for narrow-headed
gartersnakes may counter the effects of
resident crayfish to some degree.
Crayfish densities may also be affected
by periodic flooding, which is thought
to reduce crayfish population densities
temporarily until recolonization occurs
from the dispersal of individuals from
downstream populations. More field
research is needed to fully understand
the ecological relationship between
crayfish and these gartersnakes, at least
at any particular site. However, the best
available scientific and commercial
information strongly suggests that
crayfish in larger size classes or in high
densities are a cause for concern for
gartersnakes and their prey species,
especially with other threats
simultaneously affecting gartersnake
populations.
Effects of Predation-Related Injuries to
Gartersnakes (Northern Mexican and
Narrow-Headed Gartersnakes) (Factor C)
The tails of gartersnakes are often
broken off during predation attempts by
bullfrogs, crayfish, or other predators,
and do not regenerate. The incidence of
tail breaks in gartersnakes can often be
used to assess predation pressure within
gartersnake populations. Attempted
predation occurs on both sexes and all
ages of gartersnakes within a
population, although some general
trends have been detected. For example,
female gartersnakes may be more
susceptible to predation as evidenced by
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the incidence of tail damage (Willis et
al. 1982, pp. 100–101; Rosen and
Schwalbe 1988, p. 22; Mushinsky and
Miller 1993, pp. 662–664; Fitch 2003, p.
212). This can be explained by higher
basking rates associated with pregnant
females that increase their visibility to
predators. Fitch (2003, p. 212) found
that tail injuries in the common
gartersnake occurred more frequently in
adults than in juveniles. Predation on
juvenile snakes likely results in
complete consumption of the animal,
which would limit observations of tail
injury in their age class.
Tail injuries can have negative effects
on the health, longevity, and overall
success of individual gartersnakes from
infection, slower swimming and
crawling speeds, or impeding
reproduction. Mushinsky and Miller
(1993, pp. 662–664) commented that,
while tail breakage in gartersnakes can
save the life of an individual snake, it
also leads to permanent handicapping of
the snake, resulting in slower swimming
and crawling speeds, which could leave
the snake more vulnerable to predation
or affect its foraging ability. Willis et al.
(1982, p. 98) discussed the incidence of
tail injury in three species in the genus
Thamnophis (common gartersnake,
Butler’s gartersnake (T. butleri), and the
eastern ribbon snake (T. sauritus)) and
concluded that individuals that suffered
nonfatal injuries prior to reaching a
length of 12 in (30 cm) are not likely to
survive and that physiological stress
during post-injury hibernation may play
an important role in subsequent fatality.
While northern Mexican or narrowheaded gartersnakes may survive an
individual predation attempt from a
bullfrog or crayfish with tail damage,
secondary effects from infection of the
wound may significantly contribute to
fatality of individuals. Perry-Richardson
et al. (1990, p. 77) described the
importance of tail-tip alignment in the
successful courtship and mating in
Thamnophiine snakes and found that
missing or shortened tails adversely
affected these activities and, therefore,
mating success. In researching the role
of tail length in mating success in the
red-sided gartersnake (Thamnophis
sirtalis parietalis), Shine et al. (1999, p.
2150) found that males that experienced
injuries or the partial or whole loss of
the tail experienced a three-fold
decrease in mating success.
The frequency of tail injuries can be
quite high in a given gartersnake
population; for example at the SBNWR
(Rosen and Schwalbe 1988, pp. 28–31),
78 percent of northern Mexican
gartersnakes had broken tails with a
‘‘soft and club-like’’ terminus, which
suggests repeated injury from multiple
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predation attempts by bullfrogs. While
medically examining pregnant female
northern Mexican gartersnakes, Rosen
and Schwalbe (1988, p. 28) noted
bleeding from the posterior region,
which suggested to the investigators the
snakes suffered from ‘‘squeeze-type’’
injuries inflicted by adult bullfrogs. In
another example, Holm and Lowe (1995,
pp. 33–34) observed tail injuries in 89
percent of northern Mexican
gartersnakes during the early 1990s in
Scotia Canyon in the Huachuca
Mountains, as well as a skewed age
class ratio that favored adults over subadults, which is consistent with data
collected by Willis et al. (1982, pp. 100–
101) on other gartersnake species.
Bullfrogs are largely thought to be
responsible for the significant decline of
northern Mexican gartersnake and its
prey base at this locality, although the
latter has improved through recovery
actions. In the Black River, crayfish are
very abundant and have been identified
as the likely cause for a high-frequency
of tail injuries to narrow-headed
gartersnakes (Brennan 2007, p. 7;
Brennan and Rosen 2009, p. 9). Brennan
(2007, p. 5) found that, in the Black
River, 14 of 15 narrow-headed
gartersnakes captured showed evidence
of damaged or missing tails (Brennan
2007, p. 5). In 2009, 16 of 19 narrowheaded gartersnakes captured in the
Black River showed evidence of
damaged or missing tails (Brennan and
Rosen 2009, p. 8). In the middle Verde
River region, Emmons and Nowak
(2013, p. 5) reported that 18 of 49 (37
percent) northern Mexican gartersnakes
captured had scars (n = 17) and/or
missing tails tips (n = 7).
Vegetation or other forms of
protective cover may be particularly
important for gartersnakes to reduce the
effects of harmful nonnative species on
populations. For example, the
population of northern Mexican
gartersnakes at the Page Springs and
Bubbling Ponds State Fish Hatcheries
occurs with harmful nonnative species
(Boyarski 2008b, pp. 3–4, 8). Yet, only
11 percent of northern Mexican
gartersnakes captured in 2007 were
observed as having some level of tail
damage (Boyarski 2008b, pp. 5, 8). The
relatively low occurrence of tail damage,
as compared to 78 percent of snakes
with tail damage found by Rosen and
Schwalbe (1988, pp. 28–31), may
indicate: (1) Adequate vegetation
density was used by gartersnakes to
avoid harmful nonnative species
predation attempts; (2) a relatively small
population of harmful nonnative species
may be at a comparatively lower density
than sites sampled by previous studies
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(harmful nonnative species population
density data were not collected by
Boyarski (2008b)); (3) gartersnakes may
not have needed to move significant
distances at this locality to achieve
foraging success, which might reduce
the potential for encounters with
harmful nonnative species; or (4)
gartersnakes infrequently escaped
predation attempts by harmful
nonnative species, were removed from
the population, and were consequently
not detected by surveys.
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Expansion of the American Bullfrog and
Crayfish in Mexico (Northern Mexican
Gartersnake) (Factors A, C, and E)
Bullfrogs are a significant threat to
native aquatic and riparian species
´
throughout Mexico. Luja and RodrıguezEstrella (2008, pp. 17–22) examined the
invasion of the bullfrog in Mexico. The
earliest records of bullfrogs in Mexico
were Nuevo Leon (1853), Tamaulipas
(1898), Morelos (1968), and Sinaloa
´
(1969) (Luja and Rodrıguez-Estrella
2008, p 20). By 1976, the bullfrog was
documented in seven more states:
Aguacalientes, Baja California Sur,
Chihuahua, Distrito Federal, Puebla,
San Luis Potosi, and Sonora (Luja and
´
Rodrıguez-Estrella 2008, p. 20). The
bullfrog was recently verified from the
state of Hidalgo, Mexico, at an elevation
of 8,970 feet (2,734 m), which indicates
the species continues to spread in that
country and can exist even at the
uppermost elevations inhabited by
northern Mexican gartersnakes
(Duifhuis Rivera et al. 2008, p. 479). As
´
of 2008, Luja and Rodrıguez-Estrella
(2008, p. 20) have recorded bullfrogs in
20 of the 31 Mexican States (65 percent
of the states in Mexico) and suspect that
they have invaded other States, but were
unable to find documentation.
Bullfrogs have been commercially
produced for food in Mexico in
Yucatan, Nayarit, Morelos, Estado de
´
Mexico, Michoacan, Guadalajara, San
Luis Potosi, Tamaulipas, and Sonora,
and their use for food was endorsed by
the Mexican Secretary of Aquaculture
´
Support (Luja and Rodrıguez-Estrella
2008, p. 20). However, frog legs
ultimately never gained popularity in
Mexican culinary culture (Conant 1974,
´
pp. 487–489), and Luja and RodrıguezEstrella (2008, p. 22) point out that only
10 percent of these farms remain in
´
production. Luja and Rodrıguez-Estrella
(2008, pp. 20, 22) document instances
where bullfrogs have escaped
production farms and suspect the
majority of the frogs that were produced
commercially in farms that have since
ceased operation have assimilated into
surrounding habitat.
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´
Luja and Rodrıguez-Estrella (2008, p.
20) also state that Mexican people
deliberately introduce bullfrogs for
ornamental purposes, or ‘‘for the simple
pleasure of having them in ponds.’’ The
act of deliberately releasing bullfrogs
into the wild in Mexico was cited by
´
Luja and Rodrıguez-Estrella (2008, p.
21) as being ‘‘more common than we
can imagine.’’ Bullfrogs are available for
purchase at some Mexican pet stores
´
(Luja and Rodrıguez-Estrella 2008, p.
´
22). Luja and Rodrıguez-Estrella (2008,
p. 21) state that bullfrog eradication
efforts in Mexico are often thwarted by
their popularity in rural communities
(presumably as a food source).
Currently, no regulation exists in
Mexico to address the threat of bullfrog
invasions or prevent their release into
´
the wild (Luja and Rodrıguez-Estrella
2008, p. 22). As a result, the bullfrogs’
distribution continues to increase in
Mexico, beyond what it would through
natural dispersal mechanisms.
Rosen and Melendez (2006, p. 54)
report bullfrog invasions to be prevalent
in northwestern Chihuahua and
northwestern Sonora, where the
northern Mexican gartersnake is thought
to occur. In many areas, native leopard
frogs were completely displaced where
bullfrogs were observed. Rosen and
Melendez (2006, p. 54) also
demonstrated the relationship between
fish and amphibian communities in
Sonora and western Chihuahua. Native
leopard frogs, a primary prey item for
the northern Mexican gartersnake, only
occurred in the absence of nonnative
fish, and were absent from waters
containing nonnative species, which
included several major waters. In
Sonora, Rorabaugh (2008a, p. 25) also
considers the bullfrog to be a significant
threat to the northern Mexican
gartersnake and its prey base,
substantiated by field observations
made during surveys conducted in
Chihuahua and Sonora in 2006
(Rorabaugh 2008b, p. 1).
Few data were found on the presence
or distribution of nonnative crayfish
species in Mexico. However, in a 2week gartersnake survey effort in 2006
in northern Mexico, crayfish were
observed as ‘‘widely distributed’’ in the
valleys of western Chihuahua
(Rorabaugh 2008b, p. 1). Based on the
invasive nature of crayfish ecology and
their distribution in the United States
along the Border region, it is reasonable
to assume that, at a minimum, crayfish
are likely distributed along the entire
Border region of northern Mexico,
adjacent to where they occur in the
United States, and act in a similar
fashion on affected northern Mexican
gartersnake populations.
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Risks to Gartersnakes From Fisheries
Management Activities (Northern
Mexican and Narrow-Headed
Gartersnakes) (Factors A and E)
The decline in native fish
communities from the effects of harmful
nonnative fish species has spurred
resource managers to take action to help
recover native fish species. While we
fully support activities designed to help
recover native fish, recovery actions for
native fish, in the absence of thorough
planning, can have negative effects on
resident gartersnake populations.
Piscicides—Piscicide is a term that
refers to a ‘‘fish poison.’’ The use of
piscicides, such as rotenone or
antimycin A, for the removal of harmful
nonnative fish species has widely been
considered invaluable for the
conservation and recovery of imperiled
native fish species throughout the
United States, and in particular the Gila
River basin of Arizona and New Mexico
(Dawson and Kolar 2003, entire).
Antimycin A is rarely used anymore
due to limited production and has been
largely replaced by rotenone in field
applications. Experimentation with
ammonia as a piscicide has shown
promising results and may ultimately
replace rotenone in the future as a
desired control method if legally
registered for such use (Ward et al.
2013, pp. 402–404). Currently, rotenone
is the most commonly used piscicide.
The active ingredient in rotenone is a
natural chemical compound extracted
from the stems and roots of tropical
plants in the family Leguminosae that
interrupts oxygen absorption in gillbreathing animals (Fontenot et al. 1994,
pp. 150–151). In the greater Gila River
subbasin alone, 57 streams or water
bodies have been treated with piscicide,
some on several occasions spanning
many years (Carpenter and Terrell 2005;
Table 6). However, this practice has
been the source of recent controversy
due to a perceived link between
rotenone and Parkinson’s disease in
humans, as well as potential effects to
livestock.
Speculation of the potential role of
rotenone in Parkinson’s disease was
fueled by Tanner et al. (2011, entire),
which correlated the incidence of the
disease with lifetime exposure to certain
pesticides, including rotenone. As a
result, in 2012, the Arizona State
Legislature proposed two bills that
called for the development of an
environmental impact statement prior to
the application of rotenone or antimycin
A (S.B. 1453, see State of Arizona
Senate (2012b)) and urged the U.S.
Environmental Protection Agency to
deregister rotenone from use in the
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United States (S.B. 1009, see State of
Arizona Senate (2012b)). Public safety
considerations were fully evaluated by a
multidisciplined technical team of
specialists that found no correlation
between rotenone applications
performed, according to product label
instructions, and Parkinson’s disease
(Rotenone Review Advisory Committee
2012, pp. 24–25). Nonetheless,
continued anxiety regarding the use of
piscicides for conservation and
management of fish communities leaves
an uncertain future for this important
management tool. Should circumstances
result in the discontinued practice of
using piscicides for fish recovery and
management, the likelihood of recovery
for listed or sensitive aquatic vertebrates
in Arizona, such as northern Mexican
and narrow-headed gartersnakes, would
be substantially reduced, if not
eliminated outright.
The use of piscicides is a vital and
scientifically sound tool, the only tool,
in most circumstances, for
reestablishing native fish communities
and removing threats related to
nonnative aquatic species in occupied
northern Mexican and narrow-headed
gartersnake habitat. By extension, the
use of piscicides is also invaluable in
the recovery and conservation of
northern Mexican and narrow-headed
gartersnakes. However, without proper
planning the amount of time a treated
water body remains fishless posttreatment can affect gartersnakes by
removing fish, their primary food
source. The time period between
rotenone applications and the
subsequent restocking of native fish is
contingent on two basic variables, the
time it takes for piscicide levels to reach
nontoxic levels and the level of
certainty required to ensure that
renovation goals and objectives have
been met prior to restocking.
Implementation of the latter
consideration may vary from to a year
or longer, depending on the level of
certainty required by project
proponents. Carpenter and Terrell
(2005, p. 14) reported that standard
protocols used by the AGFD for Apache
trout renovations at that time required
two applications of piscicide before
repatriating native fish to a stream,
waiting a season to see if the renovation
was successful, and then continuing to
renovate if necessary. Past protocols
have included goals for the renovated
water body to remain fishless for
extended periods, sometimes up to an
entire year before restocking (Carpenter
and Terrell 2005, p. 14). At a minimum
and according to our files, reaches of Big
Bonito Creek, the West Fork Black
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River, West Fork Gila River, Little
Creek, and O’Donnell Creek have all
been subject to fish renovations using
these or similarly accepted protocols
(Carpenter and Terrell 2005; Table 6;
Paroz and Propst 2009, p. 4; Hellekson
2012a, pers. comm.). Therefore,
northern Mexican or narrow-headed
gartersnake populations in these streams
have likely been negatively affected, due
to the eradication of a portion of, or
their entire, prey base in these systems
for varying periods of time. Big Bonito
Creek was restocked with salvaged
native fish shortly after renovation
occurred. However, we are uncertain
how long other stream reaches remained
fishless post-treatment, but it was likely
to be a minimum of weeks in each
instance, and possibly a year or longer
in some instances.
Although significant efforts are
generally made to salvage as many
native fish as possible prior to
treatment, logistics of holding fish for
several weeks prior to restocking limit
the number of individuals that can be
held safely. Therefore, not every
individual fish is salvaged, and native
fish remaining in the stream are
subsequently lost during the treatment.
The number of fish subsequently
restocked is, therefore, smaller than the
number of fish that were present prior
to the treatment. The full restoration of
native fish populations to pre-treatment
levels may take several years, depending
on the size of the treated area and the
size and maturity of the founding
populations. Restocking salvaged fish in
the fall may allow natural spawning and
recruitment to begin in the spring,
which would provide a more immediate
benefit to resident gartersnake
populations.
Several streams within the
distribution of narrow-headed
gartersnakes in New Mexico have been
identified for potential future fish
barrier construction, for which piscicide
applications are likely necessary. These
streams include Little Creek, West Fork
Gila River, Middle Fork Gila River,
Turkey Creek, Saliz Creek, Dry Blue
Creek, Iron Creek, and the San Francisco
River (Riley and Clarkson 2005, pp. 4–
5, 7, 9, 12; Clarkson and Marsh 2012, p.
8; 2013, pp. 1, 4, 6; Hellekson 2013,
pers. comm.). Of these, the Middle Fork
Gila River and Turkey Creek appear to
the most likely chosen for renovation
(Clarkson and Marsh 2013, p. 8). Mule
Creek and Cienega Creek, both occupied
by northern Mexican gartersnakes, as
well as Whitewater Creek (occupied by
narrow-headed gartersnakes), are under
consideration but ultimately may not be
chosen (Clarkson and Marsh 2013, pp.
8–9). Haigler Creek (occupied by
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narrow-headed gartersnakes) is planned
for renovation in 2015 (Burger and
Jeager 2013, p. 2) and barrier
development.
The current standard operating
procedures for piscicide application, as
adopted nationally and provided in
Finlayson et al. (2010, p. 23), provide
guidance for assuring that nontarget,
baseline environmental conditions (the
biotic community) are accounted for in
assessing whether mitigation measures
are necessary. This procedural protocol
states, ‘‘Survival and recovery of the
aquatic community may be
demonstrated by sampling plankton,
macroinvertebrates (aquatic insects,
crustacea, leeches, and mollusks), and
amphibians (frogs, tadpoles, and larval
and adult salamanders)’’ (Finlayson et
al. 2010, p. 23). This protocol, adopted
by the AGFD (see AGFD 2012a), does
not in itself consider the effects of
leaving a treated water body without a
prey base for a sensitive species much
less for a fish-specialist, such as the
narrow-headed gartersnake, for
extended periods of time. However, the
AGFDs’ internal Environmental
Assessment Checklist (EAC) addresses
considerations for nontarget aquatic
reptiles. Thus, we believe that concerns
for potential effects of piscicide
treatments on these gartersnake species
within Arizona should not be
substantial in the future.
As of 2012, a new policy was
finalized by the AGFD that includes an
early and widespread public
notification and planning process that
involves the approval of several
decision-makers within four major
stages: (1) Piscicide project internal
review and approval; (2) preliminary
planning and public involvement; (3)
intermediate planning and public
involvement; and (4) project
implementation and evaluation (AGFD
2012a, p. 3). Within the Internal Review
and Approval stage of the process,
sensitive, endemic, and listed species
potentially impacted by the project must
be identified (AGFD 2012a, p. 13), such
as northern Mexican or narrow-headed
gartersnakes. This change ensures that
an analysis of potential effects to
nontarget wildlife by fisheries
management activities occurs within the
same planning document, versus a
separate process. In addition, the
AGFD’s Conservation and Mitigation
Program has specifically committed to
quickly restocking renovated streams
that are occupied by either northern
Mexican or narrow-headed gartersnakes
(USFWS 2011, Appendix C).
Piscicide application protocols used
by the New Mexico Department of Game
and Fish are provided in Pierce (2014,
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entire) and specify that effects to
amphibian species are reviewed prior to
application; however, the protocol does
not provide for an assessment of
potential gartersnake effects from
treatment. No specific timeframe, posttreatment, was recommended by the
protocol for when native fish are
recommended for stocking into treated
waters (Pierce 2014, pers. comm.). We
intend to coordinate with the New
Mexico Department of Game and Fish as
active partners in wildlife conservation
to ensure potential effects, from
piscicide treatments, to either
gartersnake are avoided or minimized.
However, if proper protocols are not
incorporated into future fish restoration
projects, these activities will continue to
threaten local gartersnake populations.
Mechanical Methods—In addition to
chemical renovation techniques,
mechanical methods using
electroshocking equipment are often
used in fisheries management, both for
nonnative aquatic species removal and
fisheries survey and monitoring
activities that often occur in conjunction
with piscicide treatments. Northern
Mexican and narrow-headed
gartersnakes often flee into the water as
a first line of defense when startled. In
occupied habitat, gartersnakes present
in the water and within the affected
radius of electroshockers are often
temporarily paralyzed from electrical
impulses intended for fish, and are,
therefore, readily detected by surveyors
(Hellekson 2012a, pers. comm.). We are
not aware of any research that has
investigated potential short- or longterm consequences to gartersnakes from
these events, and so we do not consider
electroshock surveys as a substantial
threat to either gartersnake.
Trapping methods are also used in
fisheries surveys, for other applications
in aquatic species management, and for
the collection of live baitfish in
recreational fishing. One such common
method to study aquatic or semi-aquatic
wildlife (including populations of
aquatic snakes such as gartersnakes) is
through the use of wire minnow traps.
When used to monitor gartersnake
populations, wire minnow traps are
anchored to vegetation, logs, etc., along
the shoreline (in most applications) and
positioned so that half to one-third of
the trap, along its lateral line, is above
the water surface to allow snakes to
surface for air. These traps often attract
prey species, such as small fishes and
amphibian larvae (when present), and,
therefore, become self-baiting. They are
then checked according to a
predetermined schedule. Because the
wire, twine, etc., used to anchor these
traps is fixed in length, these traps may
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become fully submerged if there is a
sudden, unanticipated rise in water
levels (e.g., storm event). During the
monsoon in Arizona and New Mexico,
these types of storm events are common,
and river hydrographs respond
accordingly with rapid and dynamic
increases in flow.
We are aware of examples where
northern Mexican gartersnakes,
intentionally captured in minnow traps,
have drowned as a direct result of a
rapid, unexpected rise in water levels.
Some examples include an adult female
northern Mexican gartersnake along
lower Tonto Creek in 2004, an adult and
two neonates at the Bubbling Ponds
State Fish Hatchery in 2009 and 2010,
respectively, and an individual of
undisclosed age in the upper Santa Cruz
River (Holycross et al. 2006, p. 41,
Boyarski 2011, pp. 2–3; Lashway 2012,
p. 5). In another example, involving an
underwater funnel trap used to survey
for lowland leopard frogs (but which are
not used for fishery surveys), a large
adult female northern Mexican
gartersnake was discovered deceased in
the trap (Jones 2012a, pers. comm.).
Death of that individual was likely due
to drowning or predation by numerous
crayfish that were also confined in the
funnel trap with the gartersnake (Jones
2012a, pers. comm.). Depending on the
mesh size of traps, neonatal gartersnakes
can become stuck in the mesh of traps
(Lashway 2012, p. 5), which could
result in injury or death of the
individual. There are likely additional
cases where northern Mexican or
narrow-headed gartersnake fatality from
trapping has not been reported,
particularly where trapping has
occurred in occupied habitat prone to
flash flooding.
Minnow traps are often deployed for
monitoring fully aquatic species, such
as fish, and are, therefore, intentionally
positioned in the water column where
they are fully under water. Traps used
for this purpose may be checked less
frequently, because risks to gillbreathing aquatic species are less if held
in the trap for longer periods of time. As
fish collectively become trapped, the
trap becomes incidentally self-baited for
gartersnakes and, if deployed in habitat
occupied by either northern Mexican or
narrow-headed gartersnakes, these traps
may accidentally attract, capture, and
drown gartersnakes that are actively
foraging under water and are lured to
the traps because of captured prey
species. Neonatal northern Mexican and
narrow-headed gartersnakes can also
wriggle through the mesh of some wire
minnow traps and become lodged
halfway through, depending on the pore
size of the wire mesh (Jaeger 2012, pers.
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comm.). If not found in time, this
situation would likely result in their
death from drowning, predation, or
exposure.
The use of minnow traps is also
allowed in recreational fishing in
Arizona and New Mexico (AGFD 2013a,
p. 57; New Mexico Department of Game
and Fish (NMDGF) 2013, p. 17). In
Arizona and New Mexico, it is lawful to
set minnow traps for the collection of
live baitfish (AGFD 2013a, pp. 56–57;
NMDGF 2013, p. 17). In Arizona,
minnow traps used for collecting live
baitfish must be checked once daily and
the trapping activity must occur where
captured bait will be used (AGFD 2013a,
pp. 56–57); in New Mexico, there is no
stipulation on time intervals in the
regulations to check minnow traps
(NMDGF 2013, p. 17). In either scenario
in either state, these minnow traps are
likely to be fully submerged when in
use and pose a drowning hazard to
resident gartersnakes while foraging
underwater, as they can be lured into
the traps by fish already caught.
We do not have adequate information
to assess the frequency and geographical
extent to which accidental drownings of
gartersnakes in minnow traps may be
occurring. This is mainly because it
happens incidentally as a result of
trapping efforts for other species, and so
it historically did not get reported by
researchers. Without additional
information, we cannot conclude at this
time that deaths from accidental
minnow trapping are likely having
population-level effects on either
gartersnake. However, if even a few
adult females are lost from populations
that already have low densities and low
rates of recruitment, these losses would
contribute to population extirpations
and the continued decline in the status
of the gartersnakes. Working with
researchers in the future to minimize
the chances of snake drownings and to
report any incidental collections of
gartersnakes will be important for future
conservation of both species.
Intentional Dewatering—Lastly,
dewatering or water fluctuation
techniques are sometimes considered
for eliminating undesirable fish species
from water bodies (Finlayson et al.
2010, p. 4). Dewatering of occupied
northern Mexican or narrow-headed
gartersnake habitat would have
deleterious effects to affected
populations by removing a primary
habitat feature and eliminating the prey
base. Because northern Mexican
gartersnakes often occupy lentic water
bodies or intermittently watered canyon
bottoms, where this practice is most
feasible, effects of dewatering activities
may disproportionately affect that
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species. This technique is being
considered by the AGFD for pools
within Redrock Canyon where northern
Mexican gartersnakes could be
adversely affected. We have been made
aware that northern Mexican
gartersnakes are being considered by the
AGFD in their implementation planning
process. Depending on the availability
of suitable habitat regionally and the
length of time water is absent, these
activities may ultimately cause local
extirpations of gartersnake populations.
Summary
In our review of the scientific and
commercial literature, we have found
that over time, native aquatic
communities, specifically the native
prey bases for northern Mexican and
narrow-headed gartersnakes, have been
substantially weakened as a result of the
cumulative effects of disease and
harmful nonnative species. Harmful
nonnative species have been
intentionally introduced or have
naturally dispersed into virtually every
subbasin throughout the distribution of
northern Mexican and narrow-headed
gartersnakes in the United States and
Mexico. According to Geographic
Information System (GIS) analyses,
nonnative, predatory fish are known to
occur in 90 percent of the historical
distribution of the northern Mexican
gartersnake and 85 percent of the
historical distribution of the narrowheaded gartersnake in the United States.
Bullfrogs are known to occur in 85
percent of the historical distribution of
the northern Mexican gartersnake and
53 percent of the historical distribution
of the narrow-headed gartersnake in the
United States. Crayfish are known to
occur in 77 percent of the historical
distribution of the northern Mexican
gartersnake and 75 percent of the
historical distribution of the narrowheaded gartersnake in the United States.
Nonnative, predatory fish, bullfrogs, and
crayfish are known to occur
simultaneously in 65 percent of the
historical distribution of the northern
Mexican gartersnake and 44 percent of
the historical distribution of the narrowheaded gartersnake in the United States.
Native fish are important prey for
northern Mexican gartersnakes but
much more so for narrow-headed
gartersnakes. Predation by and
competition with primarily nonnative,
predatory fish species, and secondarily
with brown trout and crayfish, are
widely considered to be the primary
reason for major declines in native fish
communities throughout the range of
both gartersnakes. In Arizona, 19 of 31
(61 percent) of all native fish species are
listed under the Act. Consequently,
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Arizona ranks the highest of all 50
States in the percentage of native fish
species with declining trends (85.7
percent). Similar trends in the loss of
native fish biodiversity have been
described in New Mexico and Mexico.
Native amphibians such as the
Chiricahua leopard frog, an important
component of the northern Mexican
gartersnake prey base, have declined
significantly and may face future
declines as a result of Bd and harmful
nonnative species. Historical native frog
populations have been wholly replaced
by harmful nonnative species, both on
local and regional scales. These declines
have directly contributed to subsequent
northern Mexican gartersnake
population declines or extirpations in
these areas. An adequate native prey
base is essential to the conservation and
recovery of northern Mexican
gartersnakes, and this native ranid frog
prey base faces an uncertain future if
harmful nonnative species continue to
persist and expand their distributions in
occupied habitat.
The best available commercial and
scientific information confirms that
harmful nonnative species are the most
important threat to northern Mexican
and narrow-headed gartersnakes and
their prey bases, and they have had a
profound role in their decline. A large
body of literature documents that
northern Mexican and narrow-headed
gartersnakes are uniquely susceptible to
the influence of harmful nonnative
species in their biotic communities.
This sensitivity is largely the result of
complex ecological interactions that
result in direct predation on
gartersnakes; shifts in biotic community
structure from largely native to largely
nonnative; and competition for a
diminished prey base that can
ultimately result in the injury,
starvation, or death of northern Mexican
or narrow-headed gartersnakes followed
by reduced recruitment, population
declines, and extirpations.
Lastly, fisheries management
activities can have negative effects on
gartersnake populations when
gartersnakes are not considered in
project planning and implementation.
The use of rotenone and other fisheries
management techniques are important
in the conservation and recovery of
native fish. However, significant threats
can occur if streams are left without an
intact fish community for extended
periods of time. New policies and
mitigation measures have been
developed in Arizona that will reduce
the likelihood of these activities having
negative effects on either northern
Mexican or narrow-headed gartersnake
populations in the future. However,
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some level of effect is still expected
based on logistical complications and
complexities of restoring fish
populations to pre-treatment levels. We
expect to coordinate with resource
managers in New Mexico as we do in
Arizona, to ensure gartersnake
populations are not significantly
affected by these activities. However, if
proper protocols are not incorporated
into future fish restoration projects,
these activities will continue to threaten
local gartersnake populations. Other
mechanisms or activities used in
fisheries management, such as
electroshocking, trapping, or
dewatering, can result in the injury or
death of northern Mexican or narrowheaded gartersnakes, where these
activities coincide with extant
populations, and if they have not been
considered in the planning or
implementation processes. The
significance of these losses depends on
the status of the gartersnake population
affected and whether or not either
gartersnake, as appropriate, was
considered in project planning. If
similar fisheries management
techniques are used in Mexico, we
conclude that the northern Mexican
gartersnake populations in Mexico are
threatened by the same mechanisms
described above.
The presence of harmful nonnative
species ultimately affects where
northern Mexican and narrow-headed
gartersnakes can live as viable
populations. Collectively, the
ubiquitous presence of harmful
nonnative species across the landscape
has appreciably reduced the quantity of
suitable gartersnake habitat and changed
its spatial orientation on the landscape.
Most northern Mexican and narrowheaded gartersnake populations, even
some considered viable today, live in
the presence of harmful nonnative
species. While they continue to persist,
they do so under constant threat from
unnatural levels of predation and
competition associated with harmful
nonnative species. This weakens their
resistance to other threats, including
those that affect the physical suitability
of their habitat (discussed below). This
ultimately renders populations much
less resilient to stochastic, natural, or
anthropogenic stressors that could
otherwise be withstood. Over time and
space, subsequent population declines
have threatened the genetic
representation of each species because
many populations have become
disconnected and isolated from
neighboring populations. Expanding
distances between extant populations
coupled with increasing populations of
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harmful nonnative species prevents
normal colonizing mechanisms that
would otherwise reestablish
populations where they have become
extirpated. This subsequently leads to a
reduction in species redundancy when
isolated, small populations are at
increased vulnerability to the effects of
stochastic events, without a means for
natural recolonization. Ultimately, the
effect of scattered, small, and disjunct
populations, without the means to
naturally recolonize, is weakened
species resiliency as a whole, which
ultimately enhances the risk of either or
both species becoming endangered.
Therefore, based on the best available
scientific and commercial information,
we conclude that harmful nonnative
species are the most significant threat to
both the northern Mexican and narrowheaded gartersnake, rangewide. We
expect the impacts from harmful
nonnative species to only increase in
the foreseeable future. The effects of
these threats on both gartersnakes have
resulted in the extirpation of a few
populations already and the decline in
abundance in the vast majority of
populations, so we expect the results of
continuing decline of the gartersnakes,
in terms of additional population losses
and increased risk of extinction in the
foreseeable future, which we consider as
the next several decades.
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Main Factors That Destroy or Modify the
Physical Habitat of Northern Mexican
and Narrow-Headed Gartersnakes
(Factor A)
Relationship Between Harmful
Nonnative Species and Adverse Effects
to Physical Habitat (Northern Mexican
and Narrow-headed Gartersnakes)
The presence or absence of harmful
nonnative species in occupied
gartersnake habitat affects the tolerance,
or sensitivity, of gartersnake
populations to factors or activities that
threaten to modify or destroy
components of their physical habitat.
When we use the term ‘‘physical
habitat,’’ we refer to the structural
integrity of aquatic and terrestrial
components to habitat, such as plant
species richness and density, available
water, stream banks and substrates, and
any habitat feature that does not pertain
to the animal community, which we
also define as a habitat component. The
animal community (the prey and
predator species that co-occur within
habitat) is not considered in our usage
of ‘‘physical habitat,’’ for reasons
described immediately below. In the
presence of harmful nonnative species,
gartersnake populations are more
sensitive to alterations in their physical
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habitat. In the absence of harmful
nonnative species, gartersnake
populations have shown resiliency, or
tolerance, to changes in their physical
habitat.
As discussed above, we found
harmful nonnative species to be a
significant and widespread factor that
continues to drive further declines in
and extirpations of gartersnake
populations. Furthermore, we found
various activities have affected, and
continue to affect, primary components
of the physical habitat required by
northern Mexican and narrow-headed
gartersnakes, even when the potential
impact of harmful nonnatives is absent.
These activities, such as dams, water
diversions, groundwater pumping, and
residential and commercial
development, result in the loss of stream
flow. The period from 1850 to 1940
marked the greatest loss and
degradation of riparian and aquatic
communities in Arizona, many of which
were caused by anthropogenic (humancaused) land uses (Stromberg et al.
1996, p. 114; Webb and Leake 2005, pp.
305–310). An estimated one-third of
Arizona’s wetlands has dried or is no
longer suitable (Yuhas 1996, entire).
However, not all aquatic and riparian
habitats in the United States that
support northern Mexican or narrowheaded gartersnakes have been degraded
or lost. Despite the loss or modification
of aquatic and riparian habitat, large
reaches of the Verde, Salt, San Pedro,
and Gila Rivers, as well as several of
their tributaries, remain functionally
suitable as physical habitat for either
gartersnake species.
Our treatment of how the loss or
modification of physical habitat may
affect the northern Mexican or narrowheaded gartersnake is based, in part, on
recent observations made in Mexico that
illustrate the relationship of
gartersnakes’ physical habitat suitability
to the presence of native prey species
and the lack of harmful nonnative
species, and the presence, or lack
thereof, of attributes associated with
these gartersnakes’ physical habitat. In
2007, two groups consisting of agency
biologists (including U.S. Fish and
Wildlife Service staff), species experts,
and field technicians conducted
numerous gartersnake surveys in
Durango and Chihuahua, Mexico
(Burger 2007, p. 1; Burger et al. 2010,
entire).
While considerable gartersnake
habitat in Mexico is affected by the
presence of harmful nonnative species
(Conant 1974, pp. 471, 487–489;
Contreras Balderas and Lozano 1994,
pp. 383–384; Unmack and Fagan 2004,
p. 233; Miller et al. 2005, pp. 60–61;
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Rosen and Melendez 2006, p. 54; Luja
´
and Rodrıguez-Estrella 2008, pp. 17–22),
Burger (2007, pp. 1–72) surveyed
several sites in remote areas that
appeared to be free of nonnative species.
In some sites, the physical habitat for
northern Mexican gartersnakes and
similar species of gartersnakes appeared
to be in largely good condition, but few
or no gartersnakes were detected. At
other sites, the physical habitat was
drastically affected by overgrazing, rural
development, or road crossings;
however, gartersnakes were relatively
easily detected, indicating seemingly
adequate population densities, but we
do not have the necessary data to
calculate population trends at sampled
localities. Inversely, gartersnake habitat
in Arizona and New Mexico is in
relatively better physical condition
compared to observations of these
habitats made in Durango and
Chihuahua, Mexico. However, harmful
nonnative species are essentially
ubiquitous in the southwestern United
States, based on our literature review
and GIS modeling. Several sites visited
by Burger (2007, pp. 1–72) in Durango
and Chihuahua, Mexico, had physical
habitat in poor to very poor condition,
but were largely free of nonnative
species. These situations are rarely
encountered in Arizona and New
Mexico and, therefore, provided Burger
(2007, entire) a unique opportunity to
examine differences in gartersnake
population densities based on condition
of the physical habitat, without the
confounding effect of harmful nonnative
species on resident gartersnake
populations.
Our observations of gartersnake
populations in Mexico provide evidence
for the relative importance of native
prey species and the lack of nonnative
species in comparison to the physical
attributes of gartersnake habitat. For
example, Burger (2007, pp. 6, 12, 36, 41,
58, 63) detected moderate to high
densities of gartersnakes at six sites
where their physical habitat was
moderately to highly impacted by land
uses but were largely free of nonnatives.
Burger (2007, pp. 18, 26, 32, 61, 64, 66,
67, 69, 72) also detected either low
densities or no gartersnakes at nine sites
where the physical habitat was in
moderate to good condition but where
nonnative species were detected. Eight
streams surveyed by Burger (2007, pp.
15, 22, 46, 49, 51–52, 54, 62) had little
to no surface flow, were without fish
detections and had few to no
gartersnake observations. As a result, we
have formulated three general
hypotheses: (1) Northern Mexican and
narrow-headed gartersnakes may be
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more resilient to adverse effects to
physical habitat in the absence of
harmful nonnative species and,
therefore, more sensitive to negative
effects to physical habitat in the
presence of harmful nonnative species;
(2) the presence of an adequate prey
base is important for persistence of
gartersnake populations regardless of
whether or not harmful nonnative
species are present; and (3) detections
and effects from harmful nonnative
species appear to decrease from north to
south in the Mexican states of
Chihuahua and Durango (from the
United States–Mexico International
Border), as discussed in Unmack and
Fagan (2004, pp. 233–243).
Based on field data collected by
Burger (2007, entire), Burger et al.
(2010, entire), and on the above
hypotheses, we evaluated effects to
physical habitat in the context of the
presence or absence of nonnative
species. Effects to the physical habitat of
gartersnakes can have varying effects on
the gartersnakes themselves depending
on the composition of their biotic
community. In the presence of harmful
nonnative species, effects to physical
habitat, especially those that diminish
or weaken the gartersnake prey base, are
believed to be comparatively more
significant than those that do not. As
previously discussed, harmful
nonnative species are essentially
ubiquitous in Arizona and New Mexico
where the northern Mexican and
narrow-headed gartersnakes occur and,
therefore, exacerbate the effects from
activities or factors that modify or
destroy their physical habitat.
Altering or Dewatering Aquatic Habitat
(Northern Mexican and Narrow-headed
Gartersnakes)
Dams and Diversions (Northern
Mexican and Narrow-headed
Gartersnakes)—The presence of water is
critical for northern Mexican and
narrow-headed gartersnakes, as well as
their prey base. Activities that reduce
flows or dewater habitat, such as dams,
diversions, flood-control projects, and
groundwater pumping, seriously
threaten the physical habitat of the
gartersnakes, because both fish and
amphibians must have water to survive
and reproduce and without this prey
base, gartersnakes cannot persist. Such
activities are widespread in Arizona.
For example, municipal water use in
central Arizona increased by 39 percent
from 1998 to 2006 (American Rivers
2006), and at least 35 percent of
Arizona’s perennial rivers have been
dewatered, assisted by approximately 95
dams that are in operation in Arizona
today (Turner and List 2007, pp. 3, 9).
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Larger dams may prevent movement of
fish between populations (which affects
prey availability for northern Mexican
and narrow-headed gartersnakes) and
dramatically alter the flow regime of
streams through the impoundment of
water (Ligon et al. 1995, pp. 184–189).
These diversions also require periodic
maintenance and reconstruction,
resulting in potential habitat damages
and inputs of sediment into the active
stream.
Flow regimes within stream systems
are a primary factor that shape fish
community assemblages. The timing,
duration, intensity, and frequency of
flood events has been altered to varying
degrees by the presence of dams, which
has an effect on fish communities
(Rinne et al. 1998, pp. 8–10; 2005, p. 2).
Specifically, Haney et al. (2008, p. 61)
suggested that flood pulses may help to
reduce populations of nonnative
species, and efforts to increase the
baseflows may assist in sustaining
native prey species for northern
Mexican and narrow-headed
gartersnakes. However, the investigators
in this study also suggest that, because
the northern Mexican gartersnake preys
on both fish and frogs, it may be less
affected by reductions in baseflow of
streams (Haney et al. 2008, pp. 82, 93).
The effect of regulated flow regimes on
the fish community in the Bill Williams
River was studied by Pool and Olden
(2014 In press, p. 5), who found the
presence of Alamo Dam having a
negative effect on native fish, while
benefitting harmful nonnative species,
which now account for the majority of
the fish fauna, in terms of species
composition and relative biomass, in the
Bill Williams River.
Other streams that are not dammed in
the same watershed still reflect a largely
native fish community due to the
presence of a natural flow regime (Pool
and Olden 2014 In press, pp. 5–6).
Collier et al. (1996, p. 16) mentions that
water development projects are one of
two main causes for the decline of
native fish in the Salt and Gila rivers of
Arizona. Unregulated flows with
elevated discharge events favor native
species, and regulated flows, absent
significant discharge events, favor
nonnative species (Propst et al. 2008, p.
1246). Interactions among native fish,
nonnative fish, and flow regimes were
observed in the upper reaches of the
East Fork of the Gila River. Prior to the
1983 and 1984 floods in the Gila River
system, native fish occurrence was
limited, while nonnative fish were
moderately common. Following the
1983 flood event, adult nonnative
predators were generally absent, and
native fish were subsequently collected
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in moderate numbers in 1985 (Propst et
al. 1986, p. 83). These relationships are
most readily observed in canyon-bound
streams, where shelter sought by
nonnative species during large-scale
floods is minimal (Propst et al. 2008, p.
1249). Propst et al. (2008, p. 1246) also
suggested the effect of nonnative fish
species on native fish communities may
be most significant during periods of
natural drought (simulated by artificial
dewatering).
Effects from flood control projects
threaten riparian and aquatic habitat, as
well as threaten the northern Mexican
gartersnake directly in lower Tonto
Creek. Kimmell (2008, pers. comm.),
Gila County Board of Supervisors (2008,
pers. comm.), Trammell (2008, pers.
comm.), and Sanchez (2008, pers.
comm.) all discuss a growing concern of
residents that live within or adjacent to
the floodplain of Tonto Creek in Gila
County, Arizona, both upstream and
downstream of the town of Gisela,
Arizona. Specifically, there is growing
concern to address threats to private
property and associated infrastructure
posed by flooding of Tonto Creek
(Sanchez 2008, pers. comm.). An
important remaining population of
northern Mexican gartersnakes within
the Salt River subbasin occurs on Tonto
Creek. In Resolution No. 08–06–02, the
Gila County Board of Supervisors
proactively declared a state of
emergency within Gila County as a
result of the expectation for heavy rain
and snowfall causing repetitive flooding
conditions (Gila County Board of
Supervisors 2008, pers. comm.). In
response, the Arizona Division of
Emergency Management called meetings
and initiated discussions among
stakeholders in an attempt to mitigate
these flooding concerns (Kimmell 2008,
pers. comm., Trammell 2008, pers.
comm.).
Mitigation measures that have been
discussed include removal of riparian
vegetation, removal of debris piles,
potential channelization of Tonto Creek,
improvements to existing flood control
structures or addition of new structures,
and the construction of new bridges.
Adverse effects from these types of
activities to aquatic and riparian habitat,
and to the northern Mexican gartersnake
or its prey species, will result from the
physical alteration or destruction of
habitat, significant increases to flow
velocity, and removal of key foraging
habitat and areas to hibernate, such as
debris jams. Specifically, flood control
projects permanently alter stream flow
characteristics and have the potential to
make the stream unsuitable as habitat
for the northern Mexican gartersnake by
reducing or eliminating stream sinuosity
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and associated pool and backwater
habitats that are critical to northern
Mexican gartersnakes and their prey
species. Threats presented by these
flood control planning efforts are
considered imminent within the next
decade because high flows associated
with the monsoon are expected to
increase in both intensity and frequency
according to climate change predictions,
as discussed below in the section
‘‘Climate Change and Drought.’’
Many streams in New Mexico,
currently or formerly occupied by
northern Mexican or narrow-headed
gartersnakes, have been or could be
affected by water withdrawals.
Approximately 9.5 river mi (15.3 km) of
the Gila River mainstem in New Mexico,
from Little Creek to the Gila Bird Area,
are in private ownership and have been
channelized, and the water is largely
used for agricultural purposes
(Hellekson 2012a, pers. comm.). Below
the Highway 180 crossing of the
mainstem Gila River, several water
diversions have reduced stream flow
(Hellekson 2012a, pers. comm.).
Channelization has also affected a
privately owned reach of Whitewater
Creek from the Catwalk downstream to
Glenwood, New Mexico (Hellekson
2012a, pers. comm.). The Gila River
downstream of the town of Cliff, New
Mexico, flows through a broad valley
where irrigated agriculture and livestock
grazing are the predominant uses.
Human settlement has increased since
1988 (Propst et al. 2008, pp. 1237–
1238). Agricultural practices have led to
dewatering of the river in the Cliff-Gila
valley at times during the dry season
(Soles 2003, p. 71). For those portions
of the Gila River downstream of the
Arizona–New Mexico border,
agricultural diversions and groundwater
pumping have caused declines in the
water table, and surface flows in the
central portion of the river basin are
diverted for agriculture (Leopold 1997,
pp. 63–64; Tellman et al. 1997, pp. 101–
104).
The San Francisco River in New
Mexico has undergone sedimentation,
riparian habitat degradation, and
extensive water diversion, and at
present has an undependable water
supply throughout portions of its length
(Hellekson 2012a, pers. comm.; 2013,
pers. comm.). The San Francisco River
is seasonally dry in the Alma Valley,
and two diversion structures fragment
habitat in the upper Alma Valley and at
Pleasanton (NMDGF 2006, p. 302). An
approximate 2-stream-mi (3.2-km) reach
of the lower San Francisco River
between the Glenwood Diversion and
Alma Bridge, which would otherwise be
good narrow-headed gartersnake habitat,
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has been completely dewatered by
upstream diversions (Hellekson 2012a,
pers. comm.).
Additional withdrawals of water from
the Gila and San Francisco Rivers may
occur in the next several decades as the
effects of drought and human
population levels increase.
Implementation of Title II of the
Arizona Water Settlements Act (AWSA)
(Public Law 108–451) would facilitate
the exchange of Central Arizona Project
water within and between southwestern
river basins in Arizona and New
Mexico, and may result in the
construction of new water development
projects. Section 212 of the AWSA
pertains to the New Mexico Unit of the
Central Arizona Project. The AWSA
provides for New Mexico water users to
deplete 14,000 acre-feet of additional
water from the Gila Basin in any 10-year
period. The settlement also provides the
ability to divert that water without
complaint from downstream pre-1968
water rights in Arizona. New Mexico
will receive $66 million to $128 million
in non-reimbursable Federal funding.
The Interstate Stream Commission (ISC)
funds may be used to cover costs of an
actual water supply project, planning,
environmental mitigation, or restoration
activities associated with or necessary
for the project, and may be used on one
or more of 15 alternative projects
ranging from Gila National Forest San
Francisco River Diversion/Ditch
improvements to a regional water
supply project (the Deming Diversion
Project). Currently, 3 of the 15 projects
under consideration include elements of
diversion or storage. At this time, it is
not known how the funds will be spent
or which potential alternatives may be
chosen. While multiple potential project
proposals have been accepted by the
New Mexico Office of the State Engineer
(NMOSE) (NMOSE 2011a, p. 1),
implementation of the AWSA is still in
the planning stages on these streams,
and final notice is expected by the end
of 2014. Should water be diverted from
the Gila or San Francisco Rivers, flows
would be diminished and direct and
indirect losses and degradation of
habitat for the narrow-headed
gartersnake and its prey species would
result.
In addition to affecting the natural
behavior of streams and rivers through
changes in timing, intensity, and
duration of flood events, dams create
reservoirs that alter resident fish
communities (Paradzick et al. 2006,
entire). Water level fluctuation can
affect the degree of benefit to harmful
nonnative fish species. Reservoirs that
experience limited or slow fluctuations
in water levels are especially beneficial
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to harmful nonnative species whereas
reservoirs that experience greater
fluctuations in water levels provide less
benefit for harmful nonnative species
(Paradzick et al. 2006, entire). The
timing of fluctuating water levels
contributes to their effect; a precipitous
drop in water levels during harmful
nonnative fish reproduction is most
deleterious to their recruitment
(Paradzick et al. 2006, entire). A drop in
water levels outside of the reproductive
season of harmful nonnative species has
less effect on overall population
dynamics (Paradzick et al. 2006, entire).
Large dams can also act as fish barriers,
which prevent upstream migration of
harmful nonnative fish that occur
downstream of these structures.
The cross-sectional profile of any
given reservoir also contributes to its
benefit for harmful nonnative fish
species (Paradzick et al. 2006, entire).
Shallow reservoir profiles generally
provide maximum space and elevated
water temperatures favorable to
reproduction of harmful nonnative
species, while deep reservoir profiles,
with limited shallow areas, provide
commensurately less benefit (Paradzick
et al. 2006, entire). Examples of
reservoirs that benefit harmful
nonnative species, and therefore
adversely affect northern Mexican and
narrow-headed gartersnakes (presently
or historically), include Horseshoe and
Bartlett Reservoirs on the Verde River,
and Roosevelt, Saguaro, Canyon, and
Apache Lakes on the Salt River. The
Salt River Project (SRP) operates the
previously mentioned reservoirs on the
Verde and Salt Rivers and, in the case
of Horseshoe and Bartlett Reservoirs,
received section 10(a)(1)(B) take
authorization under the Act for adverse
effects to several avian and aquatic
species (including northern Mexican
and narrow-headed gartersnakes)
through a comprehensive threat
minimization and mitigation program
found in SRP’s habitat conservation
plan (SRP 2008, entire). There is no
such minimization and mitigation
program developed for the operation of
Lake Roosevelt, where comparatively
limited fluctuation in reservoir levels
benefit harmful nonnative species and
negatively affect northern Mexican or
narrow-headed gartersnakes and their
prey bases in Tonto Creek. A detailed
analysis of the effects of reservoir
operations on aquatic communities is
provided in our intra-Service biological
and conference opinion provided in
USFWS (2008, pp. 112–131).
The Effect of Human Population
Growth and Development on Water
Demands and Gartersnake Habitat
(Northern Mexican and Narrow-headed
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Gartersnakes)—Arizona’s population is
expected to double from 5 million to 10
million people by the year 2030, which
will put increasing pressure on water
demands (Overpeck 2008, entire).
Arizona increased its population by 474
percent from 1960 to 2006 (Gammage
2008, p. 15) and is second only to
Nevada as the fastest growing State in
terms of human population (Social
Science Data Analysis Network
(SSDAR) (2000, p. 1). Over
approximately the same time period,
population growth rates in Arizona
counties where northern Mexican or
narrow-headed gartersnake habitat
exists have varied by county but are no
less remarkable, and all are increasing:
Maricopa (463 percent); Pima (318
percent); Santa Cruz (355 percent);
Cochise (214 percent); Yavapai (579
percent); Gila (199 percent); Graham
(238 percent); Apache (228 percent);
Navajo (257 percent); Yuma (346
percent); LaPaz (142 percent); and
Mohave (2,004 percent) (SSDAR 2000,
entire). From 1960 to 2006, the Phoenix
metropolitan area alone grew by 608
percent, and the Tucson metropolitan
area grew by 356 percent (Gammage
2008, p. 15). Population growth in
Arizona is expected to be focused along
wide swaths of land from the
international border in Nogales, through
Tucson, Phoenix, and north into
Yavapai County (called the Sun
Corridor ‘‘Megapolitan’’) and is
predicted to have 8 million people by
2030, an 82.5 percent increase from
2000 (Gammage et al. 2008, pp. 15, 22–
23). If build-out occurs as expected, it
could indirectly affect (through
increased recreation pressure and
demand for water) currently occupied
habitat for the northern Mexican or
narrow-headed gartersnake, particularly
regional populations in lower Cienega
Creek near Vail, Arizona, and the Verde
Valley, and, to a lesser extent, Red Rock
Canyon in extreme south-central
Arizona.
The effect of the increased water
withdrawals may be exacerbated by the
current, long-term drought facing the
arid southwestern United States, which
is predicted to continue. The effect of
long-term drought has already been
observed in the Southwest. Philips and
Thomas (2005, pp. 1–4) provided stream
flow records that indicate that the
drought Arizona experienced between
1999 and 2004 was the worst drought
since the early 1940s and possibly
earlier. The Arizona Drought
Preparedness Plan Monitoring
Technical Committee (ADPPMTC)
(2012) determined the drought status
within the Arizona distributions of
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northern Mexican and narrow-headed
gartersnakes, through June 2012, to be in
‘‘severe drought.’’ Ongoing drought
conditions have depleted recharge of
aquifers and decreased base flows in the
region. While drought periods have
been relatively numerous in the arid
Southwest from the mid-1800s to the
present, the effects of human-caused
impacts on riparian and aquatic
communities have compromised the
ability of these communities to function
under the additional stress of prolonged
drought conditions. Below we further
discuss the effect of climate changeinduced drought in the future.
The Arizona Department of Water
Resources (ADWR) manages water
supplies in Arizona and has established
five Active Management Areas (AMAs)
across the State (ADWR 2006, entire).
An AMA is established by ADWR when
an area’s water demand has exceeded
the groundwater supply and an
overdraft has occurred. In these areas,
groundwater use has exceeded the rate
where precipitation can recharge the
aquifer, and these areas are subject to
regulation pursuant to Arizona’s
Groundwater Code with a goal of
balancing groundwater use with
recharge (reaching safe yield) by the
year 2025. Geographically, these five
AMAs overlap the historical
distribution of the northern Mexican or
narrow-headed gartersnake, or both, in
Arizona. The establishment of these
AMAs further illustrates the condition
of limited water availability for riparian
habitat in these areas both currently and
into the future, and they indicate a
cause of concern for the long-term
maintenance of northern Mexican and
narrow-headed gartersnake habitat.
These areas are already vulnerable to
declines in surface and groundwater
availability, and surface water may not
be sustainable to support the
gartersnakes’ prey base. An overdraft of
groundwater withdrawal creates what is
referred to as a cone of depression
within the groundwater. Reduced or
eliminated surface flow can result in
areas where these cones of depression
intersect with stream alluvium (deposits
in a valley a stream flows through).
The presence of surface water is a
primary habitat component for northern
Mexican and narrow-headed
gartersnakes. Existing water laws in
Arizona and New Mexico may not be
fully adequate to protect gartersnake
habitat from the dewatering effects of
groundwater withdrawals. New Mexico
water law now includes provisions for
instream water rights to protect fish and
wildlife and their habitats. Arizona
water law also recognizes such
provisions; however, because this
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change is relatively recent, instream
water rights have low priority, and are
often never fulfilled because more
senior diversion rights have priority.
Existing water laws are considered
outdated and reflect a legislative
interpretation of water resources that is
not consistent with current scientific
understanding of the hydrologic
connection between groundwater and
surface water (Gelt 2008, pp. 1–12).
Water for development and
urbanization is often supplied by
groundwater pumping and surface water
diversions from sources that include
reservoirs and Central Arizona Project’s
allocations from the Colorado River. As
stated previously, groundwater
pumping creates a cone of depression
within the affected aquifer that slowly
radiates outward from the well site.
When the cone of depression intersects
the hyporheic zone of a stream (the
active transition zone between two
adjacent ecological communities under
or beside a stream channel or floodplain
between the surface water and
groundwater that contributes water to
the stream itself), the surface water flow
may decrease, and the subsequent
drying of riparian and wetland
vegetative communities can follow.
Continued groundwater pumping at
such levels draws down the aquifer
sufficiently to create a water-level
gradient away from the stream and
floodplain (Webb and Leake 2005, p.
309). Complete disconnection of the
aquifer and the stream results in strong
negative effects to riparian vegetation
(Webb and Leake 2005, p. 309) that
result in a reduction or loss in surface
water and riparian vegetation that can
reduce or eliminate the local prey base
that gartersnakes depend on for
survival.
The arid southwestern United States
is characterized by limited annual
precipitation, which means limited
annual recharge of groundwater
aquifers; even modest changes in
groundwater levels from groundwater
pumping can affect above-ground
stream flow as evidenced by depleted
flows in the Santa Cruz, Verde, San
Pedro, Blue, and lower Gila rivers as a
result of regional groundwater demands
(Stromberg et al. 1996, pp. 113, 124–
128; Rinne et al. 1998, p. 9; Voeltz 2002,
pp. 45–47, 69–71; Haney et al. 2009 p.
1). Groundwater demands are expected
to reduce surface water flow in Arivaca
Creek, Babocomari River, lower Cienega
Creek, San Pedro River, upper Verde
River, and Agua Fria River over the next
several decades (Haney et al. 2009 p. 3,
Table 2), which historically or currently
support northern Mexican or narrowheaded gartersnake populations. If
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surface flow is lost entirely from
additional stress caused by drought
induced by projected climate change in
the Southwest, local or regional
extirpations of both gartersnake species
are likely to occur.
Water depletion is a concern for the
Verde River (Garner et al. 2013, entire).
For example, the City of Prescott,
Arizona, experienced a 22 percent
increase in population between 2000
and 2005 (U.S. Census Bureau 2010, p.
1), averaging around 4 percent growth
per year (City of Prescott 2010, p. 1). In
addition, the towns of Prescott Valley
and Chino Valley experienced growth
rates of 66 and 67 percent, respectively
(Arizona Department of Commerce
2009a, p. 1; 2009b, p. 1). This growth is
facilitated by groundwater pumping in
the Verde River basin. In 2004, the cities
of Prescott and Prescott Valley
purchased a ranch in the Big Chino
basin in the headwaters of the Verde
River, with the intent of drilling new
wells to supply up to approximately 5
million cubic meters (4,000 acre-feet
(AF)) of groundwater per year. Barnett
and Hawkins (2002, Table 4) reported
population census data from 1970, as
well as projections for 2030, for
communities situated along the middle
Verde River or within the Verde River
subbasin as a whole, such as Clarkdale,
Cottonwood, Jerome, and Sedona. From
1970–2000, population growth was
recorded as Clarkdale (384 percent),
Cottonwood (352 percent), Jerome (113
percent), and Sedona (504 percent)
(Barnett and Hawkins 2002, Table 4).
Projected growth in these same
communities from 1970–2030 was
tabulated at Clarkdale (620 percent),
Cottonwood (730 percent), Jerome (292
percent), and Sedona (818 percent)
(Barnett and Hawkins 2002, Table 4).
Garner et al. (2013, p. 5) found that
the Verde Valley population grew 13
percent in 10 years from 63,000 in 2000
to 71,000 in 2010. These examples of
documented and projected population
growth within the Verde River subbasin
indicate ever-increasing water demands
that have impacted base flow in the
Verde River and are expected to
continue. The middle and lower Verde
River has limited or no flow during
portions of the year due to agricultural
diversion and upstream impoundments,
and it has several impoundments in its
middle reaches, which could expand
the area of impacted northern Mexican
and narrow-headed gartersnake habitat.
Blasch et al. (2006, p. 2) suggests that
groundwater storage in the Verde River
subbasin has already declined due to
groundwater pumping and reductions in
natural channel recharge resulting from
stream flow diversions.
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Scientific studies have shown a link
between the Big Chino aquifer and
spring flows that form the headwaters of
the Verde River. It is estimated that 80
to 86 percent of baseflow in the upper
Verde River comes from the Big Chino
aquifer (Wirt 2005, p. G8). An in-depth
discussion of the potential effects to the
Verde River from pumping of the Big
Chino Aquifer is available in Marder
(2009, pp. 183–189). However, while
these withdrawals could potentially
dewater the upper 26 mi (42 km) of the
Verde River (Wirt and Hjalmarson 2000,
p. 4; Marder 2009, pp. 188–189), it is
uncertain that this project will occur
given the cost and administrative
challenges it faces. An agreement in
principle was signed among the Salt
River Project, the City of Prescott, and
Town of Prescott Valley to work toward
resolution of water rights in the Verde
watershed, and, in 2012,
Comprehensive Agreement No. 1, which
established monitoring and modeling
plans, was entered into. Within the
Verde River subbasin, and particularly
within the Verde Valley, where the
northern Mexican and narrow-headed
gartersnakes could occur, several other
activities continue to threaten surface
flows (Rinne et al. 1998, p. 9; Paradzick
et al. 2006, pp. 104–110).
Portions of the Verde River or its
tributaries are permanently or
seasonally dewatered by water
diversions for agriculture (Paradzick et
al. 2006, pp. 104–110). The demands for
surface water allocations from rapidly
growing communities and agricultural
and mining interests have altered flows
or dewatered significant reaches during
the spring and summer months in some
of the Verde River’s larger, formerly
perennial tributaries such as Wet Beaver
Creek, West Clear Creek, and the East
Verde River (Girmendonk and Young
1993, pp. 45–47; Sullivan and
Richardson 1993, pp. 38–39; Paradzick
et al. 2006, pp. 104–110), which may
have supported either the northern
Mexican or narrow-headed gartersnake,
or both. Groundwater pumping in the
Tonto Creek drainage regularly
eliminates surface flows during parts of
the year (Abarca and Weedman 1993, p.
2).
Further south in Arizona, portions of
the once-perennial San Pedro River are
now ephemeral, and water withdrawals
are a concern for the San Pedro River
(USGS 2013, p. 3). The Cananea Mine in
Sonora, Mexico, owns the land
surrounding the headwaters of the San
Pedro. There is disagreement on the
exact amount of water withdrawn by the
mine, Mexicana de Cananea, which is
one of the largest open-pit copper mines
in the world. However, there is
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38705
agreement that it is the largest water
user in the basin (Harris et al. 2001, p.
213; Varady et al. 2000, p. 232). Along
the upper San Pedro River, Stromberg et
al. (1996, pp. 124–127) found that
wetland herbaceous species, important
as cover for northern Mexican
gartersnakes, are the most sensitive to
the effects of a declining groundwater
level. Webb and Leake (2005, pp. 302,
318–320) described a correlative trend
regarding vegetation along southwestern
streams from historically being
dominated by marshy grasslands
preferable to northern Mexican
gartersnakes, to currently being
dominated by woody species that are
more tolerant of declining water tables
due to their deeper rooting depths. The
cone of depression associated with
regional groundwater pumping is
expected to continue expanding its
influence on surface flow in the San
Pedro River over the next several
decades, which is expected to further
reduce surface flow in the river and
negatively affect riparian vegetation
(Stromberg et al. 1996, pp. 124–128).
Another primary groundwater user in
the San Pedro subbasin is Fort
Huachuca. Fort Huachuca is a U.S.
Army installation located near Sierra
Vista, Arizona. Initially established in
1877 as a camp for the military, the Fort
has some of the earliest priority dates
for water rights in the state (Varady et
al. 2000, p. 230). Fort Huachuca has
pursued a rigorous water use reduction
plan, working over the past decade to
reduce groundwater consumption in the
Sierra Vista subbasin. Their efforts have
focused primarily on reductions in
groundwater demand both on-post and
off-post and increased artificial and
enhanced recharge of the groundwater
system. Annual pumping from Fort
Huachuca production wells has
decreased from a high of approximately
3,200 AF in 1989, to a low of
approximately 1,400 AF in 2005. In
addition, Fort Huachuca and the City of
Sierra Vista have increased the amount
of water recharged to the regional
aquifer through construction of effluent
recharge facilities and detention basins
that not only increase stormwater
recharge but mitigate the negative
effects of increased runoff from
urbanization. The amount of effluent
that was recharged by Fort Huachuca
and the City of Sierra Vista in 2005 was
426 AF and 1,868 AF, respectively.
During this same year, enhanced
stormwater recharge at detention basins
was estimated to be 129 AF. The total
net effect of all the combined efforts
initiated by Fort Huachuca has been to
reduce the net groundwater
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consumption by approximately 2,272
AF (71 percent) since 1989 (USFWS
2007b, pp. 41–42). Additional water
conservation and recharge efforts have
since been implemented by Fort
Huachuca and have reduced the Fort’s
effect on baseflow in the upper San
Pedro River to near zero, as analyzed in
a recent section 7 consultation (see
https://www.fws.gov/southwest/es/
arizona/Documents/Biol_Opin/120173_
Fort%20HuachucaFINALBO_
3.31.2014.pdf).
Groundwater withdrawal in Eagle
Creek, primarily for water supplying the
large open-pit copper mine at Morenci,
Arizona, dries portions of the stream
(Sublette et al. 1990, p. 19; USFWS
2005; Propst et al. 1986, p. 7) that
otherwise supports habitat for narrowheaded gartersnakes. Mining is the
largest industrial water user in
southeastern Arizona (ADWR Undated
(accessed 2014), p. 62). The Morenci
mine on Chase Creek is North America’s
largest producer of copper, covering
approximately 24,281 hectares (ha)
(60,000 acres (ac)). Water for the
Morenci mine is pumped from the Black
River as an inter-basin transfer via
pipeline and open channel to Willow
Creek, an east-flowing tributary to Eagle
Creek, then downstream more than 30
stream miles (50 km) to a facility where
water is withdrawn and pumped uphill
to the mine in the adjacent Chase Creek
drainage (Arizona Department of Water
Resources 2009, p. 1; Marsh 2013, pers.
comm.). We are not aware of plans for
the closure of the Morenci Mine over
the next several years, and as the price
for copper increases, the demand for
copper mining will increase into the
future.
The Rosemont Copper Mine proposed
to be constructed in the northeastern
area of the Santa Rita Mountains in
Santa Cruz County, Arizona, will
include a mine pit that will be
excavated to a depth greater than that of
the regional aquifer. Water will thus
drain from storage in the aquifer into the
pit. The need to dewater the pit during
mining operations will thus result in
ongoing removal of aquifer water
storage. Upon cessation of mining, a pit
lake will form, and evaporation from
this water body will continue to remove
water from storage in the regional
aquifer. This aquifer also supplies
baseflow to Cienega Creek, immediately
east of the proposed project site. Several
groundwater models have been
developed to analyze potential effects of
expected groundwater withdrawals. The
latest independent models indicate that
a potentially significant reduction to
baseflows in Cienega Creek and Emprire
Gulch are expected within 50 years
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post-closure of the Rosemont Copper
Mine, should it be permitted for
development (see https://
www.rosemonteis.us/final-eis).
The best available scientific and
commercial information indicates that
any reduction in the presence or
availability of water is a significant
threat to northern Mexican and narrowheaded gartersnakes, their prey base,
and their habitat. This is because water
is a fundamental need that supports the
necessary aquatic and riparian habitats
and prey species needed by both species
of gartersnake. Through GIS analyses,
we found that approximately 32 percent
of formerly perennial streams have been
dewatered within the historical
distribution of the northern Mexican
gartersnake. Within the historical
distribution of the narrow-headed
gartersnake, approximately 13 percent
of formerly perennial streams have been
dewatered. With continued human
population growth and corresponding
water use throughout the range of both
gartersnakes, we expect the loss of
habitat due to reduction in stream flows
to increase in the foreseeable future and
result in additional declines and
extirpations of gartersnake populations.
Climate Change and Drought
(Northern Mexican and Narrow-headed
gartersnake)—Our analyses under the
Act include consideration of ongoing
and projected changes in climate. The
terms ‘‘climate’’ and ‘‘climate change’’
are defined by the Intergovernmental
Panel on Climate Change (IPCC).
‘‘Climate’’ refers to the mean and
variability of different types of weather
conditions over time, with 30 years
being a typical period for such
measurements, although shorter or
longer periods also may be used (IPCC
2007, p. 78). The term ‘‘climate change’’
thus refers to a change in the mean or
variability of one or more measures of
climate (e.g., temperature or
precipitation) that persists for an
extended period, typically decades or
longer, whether the change is due to
natural variability, human activity, or
both (IPCC 2007, p. 78). Various types
of changes in climate can have direct or
indirect effects on species. These effects
may be positive, neutral, or negative and
they may change over time, depending
on the species and other relevant
considerations, such as the effects of
interactions of climate with other
variables (e.g., habitat fragmentation)
(IPCC 2007, pp. 8–14, 18–19). In our
analyses, we use our expert judgment to
weigh relevant information, including
uncertainty, in our consideration of
various aspects of climate change and
their predicted effects on northern
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Mexican and narrow-headed
gartersnakes.
The ecology and natural histories of
northern Mexican and narrow-headed
gartersnakes are strongly linked to
water. As discussed above, the northern
Mexican gartersnake is a highly aquatic
species and relies largely upon other
aquatic species, such as ranid frogs and
native and nonnative, soft-rayed fish as
prey. The narrow-headed gartersnake is
the most aquatic of the southwestern
gartersnakes and is a specialized
predator on native and nonnative, softrayed fish found primarily in clear,
rocky, higher elevation streams. Because
of their aquatic nature, they may be
uniquely susceptible to environmental
change, especially factors associated
with climate change (Wood et al. 2011,
p. 3). Together, these factors are likely
to make northern Mexican and narrowheaded gartersnakes vulnerable to
effects of climate change and drought
discussed below.
Several climate-related trends have
been detected since the 1970s in the
southwestern United States, including
increases in surface temperatures,
rainfall intensity, drought, heat waves,
extreme high temperatures, and average
low temperatures (Overpeck 2008,
entire). Annual precipitation amounts in
the southwestern United States may
decrease by 10 percent by the year 2100
(Overpeck 2008, entire). Seager et al.
(2007, pp. 1181–1184) analyzed 19
different computer models of differing
variables to estimate the future
climatology of the southwestern United
States and northern Mexico in response
to predictions of changing climatic
patterns. All but 1 of the 19 models
predicted a drying trend within the
Southwest; one predicted a trend
toward a wetter climate (Seager et al.
2007, p. 1181). A total of 49 projections
were created using the 19 models, and
all but 3 predicted a shift to increasing
aridity (dryness) in the Southwest as
early as 2021–2040 (Seager et al. 2007,
p. 1181). Northern Mexican and
particularly narrow-headed
gartersnakes, and their prey bases,
depend on permanent or nearly
permanent water for survival. A large
percentage of habitats within the current
distribution of northern Mexican and
narrow-headed gartersnakes are
predicted to be at risk of becoming more
arid with reductions in snow pack
levels by 2021–2040 (Seager et al. 2007,
pp. 1183–1184). This has severe
implications for the integrity of aquatic
and riparian ecosystems and the water
that supports them.
In assessing potential effects of
predicted climate change to river
systems in New Mexico, Molles (2007,
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entire) found that: (1) Variation in
stream flow will likely be higher than
variation in precipitation; (2) predicted
effects such as warming and drying are
expected to result in higher variability
in stream flows; and (3) high-elevation
fish and non-flying invertebrates (which
are prey for gartersnake prey species)
are at greatest risk from effects of
predicted climate change. Enquist and
Gori (2008, p. iii) found that most of
New Mexico’s mid- to high-elevation
forests and woodlands have experienced
either consistently warmer and drier
conditions or greater variability in
temperature and precipitation from
1991 to 2005. However, Enquist et al.
(2008, p. v) found the upper Gila and
San Francisco subbasins, which support
narrow-headed gartersnake populations,
have experienced very little change in
moisture stress during the same period.
Cavazos and Arriaga (2010, entire)
found that average temperatures along
the Mexican Plateau in Mexico could
rise in the range of 1.8 °F (1 °C) to 9 °F
(5 °C) in the next 20 years, according to
their models. Cavazos and Arriaga
(2010, entire) also found that
precipitation may decrease up to 12
percent over the next 20 years in the
same region, with pronounced decreases
in winter and spring precipitation.
Potential drought associated with
changing climatic patterns may
adversely affect the amphibian prey
base for the northern Mexican
gartersnake. Amphibians may be among
the first vertebrates to exhibit broadscale changes in response to changes in
global climatic patterns due to their
sensitivity to changes in moisture and
temperature (Reaser and Blaustein 2005,
p. 61). Changes in temperature and
moisture, combined with the ongoing
threat to amphibians from the
persistence of disease-causing bacteria
such as Batrachochytrium dendrobatidis
(Bd) may cause prey species to
experience increased physiological
stress and decreased immune system
function, possibly leading to disease
outbreaks (Carey and Alexander 2003,
pp. 111–121; Pounds et al. 2006, pp.
161–167). Of the 30 different vertebrate
species in the Sky Island region of
southeastern Arizona, the northern
Mexican gartersnake was found to be
the fifth most vulnerable (total
combined score) to predicted climate
change; one of its primary prey species,
the Chiricahua leopard frog, was
determined to be the fourth most
vulnerable (Coe et al. 2012, p. 16). Both
the northern Mexican gartersnake and
the Chiricahua leopard frog ranked the
highest of all species assessed for
vulnerability of their habitat to
predicted climate change, and the
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Chiricahua leopard frog was also found
to be the most vulnerable in terms of its
physiology (Coe et al. 2012, p. 18).
Relative uncertainty for the
vulnerability assessment provided by
Coe et al. (2012, Table 2.2) ranged from
0 to 8 (higher score means greater
uncertainty), and the northern Mexican
gartersnake score was 3, meaning that
the vulnerability assessment was more
certain than not. Coe et al. (2012, entire)
focused their assessment of species
vulnerability to climate change on those
occurring on the Coronado National
Forest in southeastern Arizona.
However, it is not unreasonable to
hypothesize that results might be
applicable in a larger, regional context
as applied in most climate models.
The bullfrog, also assessed by Coe et
al. (2012, pp. 16, 18, Table 2.2), was
shown to be significantly less
vulnerable to predicted climate change
than either northern Mexican
gartersnakes or Chiricahua leopard frogs
with an uncertainty score of 1 (very
certain). We suspect bullfrogs were
found to be less vulnerable by Coe et al.
(2012) to predicted climate change in
southeastern Arizona due to their
dispersal and colonization capabilities,
capacity for self-sustaining cannibalistic
populations, and ecological dominance
where they occur. Based upon climate
change models, nonnative species
biology, and ecological observations,
Rahel et al. (2008, p. 551) concluded
that climate change could foster the
expansion of nonnative aquatic species
into new areas, magnify the effects of
existing aquatic nonnative species
where they currently occur, increase
nonnative predation rates, and heighten
the virulence of disease outbreaks in
North America.
Rahel and Olden (2008, p. 526) expect
that increases in water temperatures in
drier climates such as the southwestern
United States will result in periods of
prolonged low flows and stream drying.
These effects from changing climatic
conditions may have profound effects
on the amount, permanency, and quality
of habitat for northern Mexican and
narrow-headed gartersnakes as well as
their prey base. Changes in amount or
type of winter precipitation may affect
snowpack levels as well as the timing of
their discharge into high-elevation
streams. Low or no snowpack levels
would jeopardize the amount and
reliability of stream flow during the arid
spring and early summer months, which
would increase water temperatures to
unsuitable levels or eliminate flow
altogether. Harmful nonnative species
such as largemouth bass are expected to
benefit from prolonged periods of low
flow (Rahel and Olden 2008, p. 527).
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These nonnative predatory species
evolved in river systems with
hydrographs that were largely stable,
not punctuated by flood pulses in which
native species evolved and benefit from.
Propst et al. (2008, p. 1246) also
suggested that nonnative fish species
may benefit from drought.
Changes to climatic patterns may
warm water temperatures, alter stream
flow events, and increase demand for
water storage and conveyance systems
(Rahel and Olden 2008, pp. 521–522).
Warmer water temperatures across
temperate regions are predicted to
expand the distribution of existing
harmful nonnative species, which
evolved in warmer water temperatures,
by providing 31 percent more suitable
habitat. This conclusion is based upon
studies that compared the thermal
tolerances of 57 fish species with
predictions made from climate change
temperature models (Mohseni et al.
2003, p. 389). Eaton and Scheller (1996,
p. 1,111) reported that, while several
cold-water fish species (such as trout, a
prey species for narrow-headed
gartersnakes) in North America are
expected to have reductions in their
distribution from effects of climate
change, several harmful nonnative
species are expected to increase their
distribution. In the southwestern United
States, this situation may occur where
the quantity of water is sufficient to
sustain effects of potential prolonged
drought conditions but where water
temperature may warm to a level found
suitable to harmful nonnative species
that were previously physiologically
precluded from occupation of these
areas. Species that are particularly
harmful to northern Mexican and
narrow-headed gartersnake populations,
such as the green sunfish, channel
catfish, largemouth bass, and bluegill,
are expected to increase their
distribution by 7.4 percent, 25.2
percent, 30.4 percent, and 33.3 percent,
respectively (Eaton and Scheller 1996,
p. 1,111).
Vanishing Cienegas (Northern
Mexican Gartersnake)—Cienegas are
particularly important habitat for the
northern Mexican gartersnake because
these areas present ideal habitat
characteristics for the species and its
prey base and have been shown to
support robust populations of both
(Rosen and Schwalbe 1988, p. 14).
Hendrickson and Minckley (1984, p.
131) defined cienegas as ‘‘mid-elevation
(3,281–6,562 ft (1,000–2000 m))
wetlands characterized by permanently
saturated, highly organic, reducing
(lowering of oxygen level) soils.’’ Many
of these unique communities of the
southwestern United States, Arizona in
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particular, and Mexico have been lost in
the past century to streambed
modification, intensive livestock
grazing, woodcutting, artificial drainage
structures, stream flow stabilization by
upstream dams, channelization, and
stream flow reduction from groundwater
pumping and water diversions
(Hendrickson and Minckley 1984, p.
161). Stromberg et al. (1996, p. 114)
state that cienegas were formerly
extensive along streams of the
Southwest; however, most were
destroyed during the late 1800s, when
groundwater tables declined several
meters and stream channels became
incised. Drying trends are expected to
continue into the next several decades
and likely beyond.
Development and Recreation Within
Riparian Corridors (Northern Mexican
and Narrow-headed Gartersnake)—
Development within and adjacent to
riparian areas has proven to be a
significant threat to riparian biological
communities and their suitability for
native species (Medina 1990, p. 351;
Nowak and Santana-Bendix 2002, p.
37). Riparian communities are sensitive
to even low levels (less than 10 percent)
of urban development within a subbasin
(Wheeler et al. 2005, p. 142).
Development along or within proximity
to riparian zones can alter the nature of
stream flow dramatically, changing
once-perennial streams into ephemeral
streams, which has direct consequences
on the riparian community (Medina
1990, pp. 358–359). Medina (1990, pp.
358–359) correlated tree density and age
class representation to stream flow in a
high-elevation system with a narrow
alluvium basin, finding that decreased
flow reduced tree densities and
generally resulted in few to no smalldiameter trees. Small-diameter trees
assist northern Mexican and narrowheaded gartersnakes by providing
additional habitat complexity,
thermoregulatory opportunities, and
cover needed to reduce predation risk
and enhance the usefulness of areas for
maintaining optimal body temperature.
Development along lower elevation
streams with broad alluvial basins may
have different effects on stream flow
and riparian vegetation, as compared to
high-elevation streams. The presence of
small shrubs and trees may be
particularly important for the narrowheaded gartersnake (Deganhardt et al.
1996, p. 327). Development within
occupied riparian habitat also likely
increases the number of humangartersnake encounters and, therefore,
the frequency of adverse human
interaction, described below.
Obvious examples of the influence of
urbanization and development can be
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observed within the areas of greater
Tucson and Phoenix, Arizona, where
impacts have modified riparian
vegetation, structurally altered stream
channels, facilitated nonnative species
introductions, and dewatered large
reaches of formerly perennial rivers
where the northern Mexican gartersnake
historically occurred (Santa Cruz, lower
Gila, and lower Salt Rivers,
respectively). Urbanization and
development of these areas, along with
the introduction of nonnative species,
are largely responsible for the likely
extirpation of the northern Mexican
gartersnake from these regions.
Development near riparian areas
usually leads to increased recreation.
Riparian areas located near urban areas
are vulnerable to the effects of increased
recreation. An example of such an area
within the existing distribution of both
the northern Mexican and narrowheaded gartersnake is the Verde Valley.
The reach of the Verde River that winds
through the Verde Valley receives a high
amount of recreational use from people
living in central Arizona (Paradzick et
al. 2006, pp. 107–108). Increased human
use results in the trampling of nearshore vegetation, which reduces cover
for gartersnakes, especially newborns.
Increased human visitation in occupied
habitat also increases the potential for
adverse human interactions with
gartersnakes, which frequently leads to
the capture, injury, or death of the snake
(Rosen and Schwalbe 1988, p. 43; Ernst
and Zug 1996, p. 75; Green 1997, pp.
285–286; Nowak and Santana-Bendix
2002, pp. 37–39).
Oak Creek Canyon, which represents
an important source population for
narrow-headed gartersnakes, is also a
well-known example of an area with
very high recreation levels (Nowak and
Santana-Bendix 2002, p. 37). In 1995,
1.3 million people visited the Red Rock
Ranger District, which includes Oak
Creek Canyon and the Sedona, Arizona
area; that figure climbed to six million
visitors by 1999 (Nowak and SantanaBendix 2002, p. 37). Recreational
activities in the Southwest are often
heavily tied to water bodies and riparian
areas, due to the general lack of surface
water on the landscape. Increased
recreational impacts on the quantity and
quality of water, as well as the adjacent
vegetation, negatively affect northern
Mexican and narrow-headed
gartersnakes. The impacts to riparian
habitat from recreation can include
movement of people or livestock, such
as horses or mules, along stream banks,
trampling, loss of vegetation, and
increased danger of fire starts (Northern
Arizona University 2005, p. 136; Monz
et al. 2010, pp. 553–554).
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High stream-side recreation levels can
result in increased siltation of streams,
which can result in lower recruitment
rates of native fish and, therefore,
negatively affect the prey base for
narrow-headed gartersnakes (Nowak
and Santana-Bendix 2002, pp. 37–38).
In the arid Gila River Basin, recreational
impacts are disproportionately
distributed along streams as a primary
focus for recreation (Briggs 1996, p. 36).
Within the range of the northern
Mexican and narrow-headed
gartersnakes in the United States, the
majority of the occupied areas occur on
Federal lands, which are managed for
recreation and other purposes. On the
Gila National Forest, and associated
private, state, or non-Forest Service
inholdings in the area, heavy recreation
use can affect gartersnakes within
occupied narrow-headed gartersnake
habitat along the Middle Fork Gila
River, the West Fork Gila River between
Cliff Dwellings and Little Creek, and
Whitewater Creek from the Catwalk to
Glenwood (Hellekson 2012a, pers.
comm.). Much of the recreation use in
these areas is related to hiking and
backpacking, which are not a threat to
gartersnakes except when increased
human visitation leads to more
gartersnake encounters and potentially
more killing of gartersnakes where the
foot trail is near the canyon bottom (see
‘‘Adverse Human Interactions with
Gartersnakes’’ below).
Urbanization on smaller scales can
also impact habitat suitability and the
prey base for the northern Mexican or
narrow-headed gartersnakes, such as
along Tonto Creek, within the Verde
Valley, and the vicinity of Rock Springs
along the Agua Fria River (Girmendonk
and Young 1997, pp. 45–52; Voeltz
2002, pp. 58–59, 69–71; Holycross et al.
2006, pp. 53, 56; Paradzick et al. 2006,
pp. 89–90). One of the more stable
populations of the northern Mexican
gartersnake in the United States, at the
Page Springs and Bubbling Ponds fish
hatcheries along Oak Creek, is likely to
be affected by future small-scale
development over the next decade. As
mitigation for effects to species covered
under their habitat conservation plan for
the operation of Horseshoe and Bartlett
Reservoirs on the Verde River, the Salt
River Project will be funding
development improvements and
capacity expansion at these State-owned
and operated hatcheries for the purpose
of creating a native fish hatchery.
Construction is likely to include the
replacement of earthen ponds currently
used by the gartersnakes, with
modernized non-earthen units.
However, the AGFD is committed to
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maintaining the healthy population of
northern Mexican gartersnakes at these
hatcheries, and is investigating land use
options to improve gartersnake habitat.
A variety of activities associated with
ongoing and future operation of the
hatchery is likely to contribute to some
level of fatality in resident gartersnakes,
but that level might be offset by a
mitigation strategy when adopted.
Diminishing Water Quantity and
Quality in Mexico (Northern Mexican
Gartersnake)—While effects to riparian
and aquatic communities affect both the
northern Mexican gartersnake and the
narrow-headed gartersnake in the
United States, Mexico provides habitat
only for the northern Mexican
gartersnake. Threats to northern
Mexican gartersnake habitat in Mexico
include intensive livestock grazing,
urbanization and development, water
diversions and groundwater pumping,
loss of vegetation cover and
deforestation, and erosion, as well as
impoundments and dams that have
modified or destroyed riparian and
aquatic communities in areas of Mexico
where the species occurred historically.
Rorabaugh (2008, pp. 25–26) noted
threats to northern Mexican
gartersnakes and their native amphibian
prey base in Sonora, which included
disease, pollution, intensive livestock
grazing, conversion of land for
agriculture, nonnative plant invasions,
and logging.
Illegal or under-regulated logging in
the Sierra Madre of Mexico, and
particularly within Chihuahua (Sierra
Tarahumara), has been identified as a
significant environmental concern
(Gingrich 1993, entire). Gingrich (1993,
p. 6) described the risk to streams from
excessive logging in the Sierra Madre as
including increased flooding, increased
sedimentation, and lower baseflows. In
an attempt to reverse disturbing trends
in logging practices, the World Wildlife
Fund-Mexico (2004, entire) has begun
implementing a conservation plan for
the Sierra Tarahumara region. Ramirez
Bautista and Arizmendi (2004, p. 3)
stated that the principal threats to
northern Mexican gartersnake habitat in
Mexico include the drying of temporary
ponds, livestock grazing, deforestation,
wildfires, and human settlements. In
addition, nonnative species, such as
bullfrogs and nonnative, predatory fish,
have been introduced throughout
Mexico and continue to disperse
naturally, broadening their distributions
(Conant 1974, pp. 487–489; Miller et al.
´
2005, pp. 60–61; Luja and RodrıguezEstrella 2008, pp. 17–22).
Mexico’s water needs for urban and
agricultural development, as well as
impacts to aquatic habitat from these
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uses, are linked to significant human
population growth over the past century
in Mexico. Mexico’s human population
grew 700 percent from 1910 to 2000
(Miller et al. 2005, p. 60). Mexico’s
population increased by 245 percent
from 1950 to 2002 and is projected to
grow by another 28 percent by 2025
(EarthTrends 2005, p. 1). Growth is
concentrated in Mexico’s northern states
(Stoleson et al. 2005, Table 3.1) and is
now skewed towards urban areas (Miller
et al. 2005, p. 60). The human
population of Sonora, Mexico, doubled
in size from 1970 (1.1 million) to 2000
(2.2 million) (Stoleson et al. 2005, p.
54). The population of Sonora is
expected to increase by 23 percent, to
2.7 million people, in 2020 (Stoleson et
al. 2005, p. 54). Increasing trends in
Mexico’s human population will
continue to place additional stress on
the country’s freshwater resources and
continue to be the catalyst for the
elimination of northern Mexican
gartersnake habitat and prey species.
Much knowledge of the status of
aquatic ecosystems in Mexico has come
from fisheries research, which is
particularly applicable to assessing the
status of northern Mexican gartersnakes
because of the gartersnakes’ ecology and
relationship to other aquatic and
riparian vertebrates. Fisheries research
is particularly applicable because of the
role fishes serve as indicators of the
status of the aquatic community as a
whole. Miller et al. (2005) reported
information on threats to freshwater
fishes and riparian and aquatic
communities in specific water bodies
from several regions throughout Mexico
within the range of the northern
Mexican gartersnake: headwaters of the
´
Rıo Lerma (extirpation of freshwater fish
species, nonnative species, pollution,
dewatering, pp. 60, 105, 197); mediumsized streams throughout the Sierra
Madre Occidental (localized
extirpations, logging, dewatering, pp.
´
109, 177, 247); the Rıo Conchos
(extirpations of freshwater fish species,
´
p. 112); the rıos Casas Grandes, Santa
´
Marıa, del Carmen, and Laguna
Bustillos (water diversions, groundwater
pumping, channelization, flood control
practices, pollution, and introduction of
´
nonnative species, pp. 124, 197); the Rıo
´
Santa Cruz (extirpations, p. 140); the Rıo
Yaqui (dewatering, nonnative species, p.
´
148, Plate 61, p. 247); the Rıo Colorado
´
(nonnative species, p. 153); the rıos
´
Fuerte and Culiacan (logging, p. 177);
canals, ponds, lakes in the Valle de
´
Mexico (nonnative species, extirpations,
´
pollution, pp. 197, 281); the Rıo Verde
Basin (dewatering, nonnative species,
´
extirpations, Plate 88); the Rıo Mayo
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(dewatering, nonnative species, p. 247);
´
the Rıo Papaloapan (pollution, p. 252);
´
´
and the Rıo Panuco Basin (nonnative
species, p. 295). These examples should
not be construed as to suggest that all
native fishes are threatened and all
aquatic habitat or ecosystems are in
peril. Rather, these examples suggest
that threats may be localized in some
examples and wider-ranging in others,
but collectively several types of threats
are acting in various degrees across
numerous drainages in Mexico,
throughout the range of the northern
Mexican gartersnake. This provides
some level of insight into the status of
native aquatic ecosystems within its
range.
Excessive sedimentation also appears
to be a significant problem for aquatic
habitat in Mexico. Recent estimates
indicate that 80 percent of Mexico is
affected by soil erosion caused by
vegetation removal related to grazing,
fires, agriculture, deforestation, etc. The
most serious erosion is occurring in the
states of Guanajuato (43 percent of the
state’s land area), Jalisco (25 percent of
´
the state’s land area), and Mexico (25
percent of the state’s land area) (Landa
et al. 1997, p. 317), all of which occur
within the distribution of the northern
Mexican gartersnake. Miller et al. (2005,
p. 60) stated that ‘‘During the time we
have collectively studied fishes in
´
Mexico and southwestern United States,
the entire biotas of long reaches of major
´
streams such as the Rıo Grande de
Santiago below Guadalajara (Jalisco) and
´
Rıo Colorado (lower Colorado River in
Mexico) downstream of Hoover
(Boulder) Dam (in the United States),
have simply been destroyed by
pollution and river alteration.’’ These
streams are within the distribution of
the northern Mexican gartersnake. The
geographic extent of threats reported by
Miller et al. (2005) across the
distribution of the northern Mexican
gartersnake in Mexico is evidence that
they are widespread through the
country, and encompass a large
proportion of the distribution of the
northern Mexican gartersnake in
Mexico.
In northern Mexico, effects of
development, which is expected to
continue at similar rates, if not increase,
over the next several decades, such as
agriculture and irrigation practices on
streams and rivers in Sonora have been
documented at least as far back as the
1960s. Branson et al. (1960, p. 218)
found that the perennial rivers that
drain the ‘‘mountains’’ (Sierra Madre)
are ‘‘silt-laden and extremely turbid,
mainly because of irrigation practices.’’
Specific rivers were not identified
where Branson et al. (1960, p. 218)
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describes the effects of irrigation
practices, but the Sierra Madre in
Sonora is within the known distribution
of the northern Mexican gartersnake in
Mexico and, therefore, suggests that at
least some portion of occupied habitat
has been adversely impacted by these
practices. Smaller mountain streams,
such as the Rio Nacozari in Sonora were
found to be ‘‘biological deserts’’ from
the effects of numerous local mining
practices (Branson et al. 1960, p. 218).
The perennial rivers and their mountain
tributaries that may have been
historically occupied by northern
Mexican gartersnakes (as well as their
prey species) have since been adversely
affected, which likely contributed to
declines in these areas.
Minckley et al. (2002, pp. 687–705)
provided a summary of threats (p. 696)
to two newly described (at the time)
species of pupfish and their habitat in
Chihuahua, Mexico, which occur with
the northern Mexican gartersnake and
comprise part of its prey base. Initial
settlement and agricultural development
of the area resulted in significant
channel cutting through soil layers
protecting the alluvial plain above them,
which resulted in reductions in the base
level of each basin in succession
(Minckley et al. 2002, p. 696). Related
to these activities, the building of dams
and diversion structures dried entire
reaches of some regional streams and
altered flow patterns of others
(Minckley et al. 2002, p. 696). This was
followed by groundwater pumping
(enhanced by the invention of the
electric pump), which lowered
groundwater levels and dried up springs
and small channels and reduced the
reliability of baseflow in ‘‘essentially all
systems’’ (Minckley et al. 2002, p. 696).
Subsequently, the introduction and
expansion of nonnative species in the
area successfully displaced or extirpated
many native species (Minckley et al.
2002, p. 696). Conant (1974, pp. 486–
489) described significant threats to
northern Mexican gartersnake habitat
within its distribution in western
Chihuahua, Mexico, and within the Rio
Concho system where it occurs. These
threats included impoundments, water
diversions, and purposeful
introductions of largemouth bass,
common carp, and bullfrogs.
In the central portions of the northern
Mexican gartersnakes’ range in Mexico,
such as in Durango, Mexico, population
growth since the 1960s has led to
regional effects such as reduced stream
flow, increased water pollution, and
largemouth bass introductions, which
‘‘have seriously affected native biota’’
(Miller et al. 1989, p. 26). McCranie and
Wilson (1987, p. 2) discuss threats to the
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pine–oak communities of higher
elevation habitats (within the
distribution of the northern Mexican
gartersnake) in the Sierra Madre
Occidental in Mexico, specifically
noting that ‘‘. . . the relative pristine
character of the pine–oak woodlands is
threatened . . . every time a new road
is bulldozed up the slopes in search of
new madera or pasturage. Once the road
is built, further development follows;
pueblos begin to pop up along its
length. . . .’’ Several drainages that
possess suitable habitat for the northern
Mexican gartersnake occur in the area
referenced above by McCranie and
Wilson (1987, p. 2), including the Rio de
la Cuidad, Rio Quebrada El Salto, Rio
Chico, Rio Las Bayas, Rio El Cigarrero,
Rio Galindo, Rio Santa Barbara, and the
Rio Chavaria.
In the southern portion of the
northern Mexican gartersnake’s range in
Mexico, growth and development
around Mexico City resulted in
agricultural practices and groundwater
demands that dewatered aquatic habitat
and led to declines, and in some cases,
extinctions of local native fish species
(Miller et al. 1989, p. 25). Considerable
research has been focused in the central
and west-central regions of Mexico,
within the southern portion of the
northern Mexican gartersnake’s range,
where native fish endemism (unique,
narrowly distributed suite of species) is
high, as are threats to their populations
and habitat. Since the 1970s in central
Mexico, significant human population
growth has resulted in the
overexploitation of local fisheries and
water pollution; these factors have
accelerated the degradation of stream
and riverine habitats and led to fish
communities becoming reduced or
undergoing significant changes in
structure and composition (MercadoSilva et al. 2002, p. 180).
These shifts in fish community
composition, population density, and
shrinking distributions have adversely
affected the northern Mexican
gartersnake prey base in the southern
portion of its range in Mexico. The
Lerma River basin is the largest in westcentral Mexico and is within the
distribution of the northern Mexican
gartersnake in the states of Jalisco,
´
Guanajuato, and Queretaro in the
southern portion of its range. Lyons et
al. (1995, p. 572) reported that many
fish communities in large perennial
rivers, isolated spring-fed streams, or
spring sources themselves of this region
have been ‘‘radically restructured’’ and
are now dominated by a few nonnative,
generalist species. Lowland streams and
rivers in this region are used heavily for
irrigation and are polluted by industrial,
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municipal, and agricultural discharges
(Lyons and Navarro-Perez 1990, p. 37;
Lyons et al. 1995, p. 572).
Native fish communities of westcentral Mexico have been found to be in
serious decline as a result of habitat
degradation at an ‘‘unprecedented’’ rate
due to water withdrawals (diversions for
irrigation), as well as untreated
municipal, industrial, and agricultural
discharges (Lyons et al. 1998, pp. 10–
11). Numerous dams have been built
along the Lerma River and along its
major tributaries to support one of
Mexico’s most densely populated
regions during the annual dry period;
the water is used for irrigation, industry,
and human consumption (Lyons et al.
1998, p. 11). From 1985 to 1993, Lyons
et al. (1998, p. 12) found that 29 of 116
(25 percent) fish sampling locations
visited within the Lerma River
watershed were completely dry and
another 30 were too polluted to support
a fish community. These figures
indicate that over half of the localities
visited by Lyons et al. (1998, p. 12) that
maintained fish populations prior to
1985 no longer support fish, which has
likely adversely affected local northern
Mexican gartersnake populations, and
perhaps led to population declines or
extirpations.
Soto-Galera et al. (1999, p. 137)
reported fish and water quality
sampling results from within the Rio
Grande de Morelia-Lago de Cuitzeo
´
Basin of Michoacan and Guanajuato,
Mexico. The easternmost portion of this
basin occurs at the periphery of the
known northern Mexican gartersnake
range in Mexico. Soto-Galera et al.
(1999, p. 137) found that over the past
several decades, diminishing water
quantity and worsening water quality
have resulted in the elimination of 26
percent of native fish species from the
basin, the extinction of two species of
native fish, and declining distributions
of the remaining 14 species. These
figures suggest significant concern for
aquatic ecosystems of this region. Some
conservation value, however, is realized
when headwaters, springs, and small
streams are protected as parks or
municipal water supplies (Lyons et al.
1998, p. 15), but these efforts do little
to protect larger perennial rivers that
represent valuable habitat for northern
Mexican gartersnakes.
Mercado-Silva et al. (2002, Appendix
2) reported results from fish community
sampling and habitat assessments along
63 sites across central Mexico; the
easternmost of these sites include most
of the northern Mexican gartersnake’s
southern range. Specifically, sampling
locations in the Balsas, Lerma, Morelia,
´
´
Panuco Moctezuma, and Panuco
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´
Tampaon basins each occurred within
the range of the northern Mexican
gartersnake in the states of Guanajuato,
Queretaro, Mexico, and Puebla;
approximately 30 locations in total. The
purpose of this sampling effort was to
score each site in terms of its index of
biotic integrity (IBI) and environmental
quality (EQ), with a score of 100
representing the optimum score for each
category. The IBI scoring method has
been verified as a valid means to
quantitatively assess ecosystem integrity
at each site (Lyons et al. 1995, pp. 576–
581; Mercado-Silva et al. 2002, p. 184).
The range in IBI scores in these
sampling locations was 85 to 35, and the
range in EQ scores was 90 to 50
(Mercado-Silva et al. 2002, Appendix 2).
The average IBI score was 57, and the
average EQ score was 74, across all 30
sites and all 4 basins (Mercado-Silva et
al. 2002, Appendix 2). According to the
qualitative equivalencies assigned to
scores (Mercado-Silva et al. 2002, p.
184), these values indicate that the
environmental quality score averaged
across all 30 sites was ‘‘good’’ and the
biotic integrity scores were ‘‘fair.’’ It
should be noted that 14 of the 30 sites
sampled had IBI scores equal to or less
than 50, and 5 of those ranked as
‘‘poor.’’ Of all the basins throughout
central Mexico that were scored in this
´
exercise, the two Panuco basins
represented 20 of the 30 sites sampled
and scored the worst of all basins
(Mercado-Silva et al. 2002, p. 186). This
indicates that threats to the northern
Mexican gartersnake, its prey base, and
its habitat pose the greatest risk in this
portion of its range in Mexico.
´
Near Torreon, Coahuila, where the
northern Mexican gartersnake occurs,
groundwater pumping has resulted in
flow reversal, which has dried up many
local springs, drawn arsenic-laden water
to the surface, and resulted in adverse
human health effects in that area (Miller
et al. 2005, p. 61). Severe water
pollution from untreated domestic
waste is evident downstream of large
Mexican cities, such as Mexico City,
and inorganic pollution from nearby
industrialized areas and agricultural
irrigation return flow has dramatically
affected aquatic communities through
contamination (Miller et al. 2005, p. 60).
Miller et al. (2005, p. 61) provide an
excerpt from Soto Galera et al. (1999)
´
addressing the threats to the Rıo Lerma,
Mexico’s longest river, which is
occupied by the northern Mexican
gartersnake: ‘‘The basin has experienced
a staggering amount of degradation
during the 20th Century. By 1985–1993,
over half of our study sites had
disappeared or become so polluted that
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they could no longer support fishes.
Only 15 percent of the sites were still
capable of supporting sensitive species.
Forty percent (17 different species) of
the native fishes of the basin had
suffered major declines in distribution,
and three species may be extinct. The
extent and magnitude of degradation in
´
the Rıo Lerma basin matches or exceeds
the worst cases reported for comparably
sized basins elsewhere in the world.’’
In the Transvolcanic Belt Region of
the states of Jalisco, Mexico, and
Veracruz in southern Mexico, Conant
(2003, p. 4) noted that water diversions,
pollution (e.g., discharge of raw
sewage), sedimentation of aquatic
habitats, and increased dissolved
nutrients were resulting in decreased
dissolved oxygen in suitable northern
Mexican gartersnake habitat. Conant
(2003, p. 4) stated that many of these
threats were evident during his field
work in the 1960s, and that they are
‘‘continuing with increased velocity.’’
High-Intensity Wildfires and
Sedimentation of Aquatic Habitat
(Narrow-Headed Gartersnake)
High-intensity wildfires lead to
excessive sedimentation and ash flows
in streams, which can, in turn, result in
sharp declines, and even complete
elimination, in fish communities
downstream. According to the ApacheSitgreaves National Forest forested
vegetation types, historic fire-return
intervals varied from frequent, lowintensity surface fires in ponderosa pine
types (every 2–17 years), to mixedseverity fires in wet mixed-conifer
forests (every 35–50 years), to highseverity, stand-replacement fires of the
spruce-fir ecosystems (every 150–400
years) (U.S. Forest Service (USFS)
2013). Low-intensity fire has been a
common, natural disturbance factor in
forested landscapes for centuries prior
to European settlement (Rinne and
Neary 1996, pp. 135–136). Rinne and
Neary (1996, p. 143) concluded that
existing wildfire suppression policies
intended to protect the expanding
number of human structures on forested
public lands have altered the fuel loads
in these ecosystems and increased the
probability of high-intensity wildfires.
Climate change-driven drought cycles
are also likely contributing to a
changing fire regime in the west
(Westerling et al. (2006, pp. 941–943).
Westerling et al. (2006, p. 940) showed
that ‘‘large wildfire activity (in the
western United States) increased
suddenly and markedly in the mid1980s, with higher large-wildfire
frequency, longer wildfire durations,
and longer wildfire seasons.’’ The
effects of these high-intensity wildfires
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include the removal of vegetation, the
degradation of subbasin condition,
altered stream behavior, and increased
sedimentation of streams. These effects
can harm fish communities, as observed
in the 1990 Dude Fire, when
corresponding ash flows resulted in fish
kills in Dude Creek and the East Verde
River (Voeltz 2002, p. 77). Fish kills,
also discussed below, can drastically
affect the suitability of habitat for
northern Mexican and narrow-headed
gartersnakes due to the removal of a
portion or the entire prey base. The
Chiricahua leopard frog recovery plan
cites altered fire regimes as a serious
threat to Chiricahua leopard frogs, a
prey species for northern Mexican
gartersnakes (USFWS 2007a, pp. 38–39).
The nature and occurrence of
wildfires in the Southwest is expected
to also be affected by climate change
and ongoing and predicted future
drought. Current predictions of drought
and/or higher winter low temperatures
may stress ponderosa pine forests in
which the narrow-headed gartersnake
principally occurs, and may increase the
frequency and magnitude of wildfire.
Ganey and Vojta (2010, entire) studied
tree mortality in mixed-conifer and
ponderosa pine forests in Arizona from
1997–2007, a period of extreme drought.
They found the mortality of trees to be
severe; the number of trees dying over
a 5-year period increased by more than
200 percent in mixed-conifer forest and
by 74 percent in ponderosa pine forest
during this timeframe. Ganey and Vojta
(2010) attributed drought and
subsequent insect (bark beetle)
infestation to the die-offs in trees.
Drought stress and a subsequent high
degree of tree mortality from bark
beetles make high-elevation forests more
susceptible to high-intensity wildfires.
Climate is a top-down factor that
synchronizes with fuel loads, a bottomup factor. Combined with a predicted
reduction in snowpack and an earlier
snowmelt, these factors suggest
wildfires will be larger, more frequent,
and more severe in the southwestern
´
United States (Fule 2010, entire).
Wildfires are expected to reduce
vegetative cover and result in greater
soil erosion, subsequently resulting in
increased sediment flows in streams
´
(Fule 2010, entire). Increased
sedimentation in streams reduces the
visibility of gartersnakes in the water
column, hampering their hunting ability
as well as resulting in fish kills (which
is also caused by the disruption in the
nitrogen cycle post-wildfire), which
reduce the amount of prey available to
gartersnake populations. Additionally,
unnaturally high amounts of sediment
fill in pools in intermittent streams,
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which reduces the amount and
availability of habitat for fish and
amphibian prey.
In 2011 and 2012, both Arizona (2011
Wallow Fire) and New Mexico (2012
Whitewater-Baldy Complex Fire)
experienced the largest wildfires in their
respective State histories; indicative of
the last decade that has been punctuated
by wildfires of massive proportion. The
2011 Wallow Fire affected (to various
degrees) approximately 540,000 acres
(218,530 ha) of Apache-Sitgreaves
National Forest, White Mountain
Apache Indian Tribe, and San Carlos
Apache Indian Reservation lands in
Apache, Navajo, Graham, and Greenlee
counties in Arizona as well as Catron
County, New Mexico (InciWeb 2011).
The 2011 Wallow Fire impacted 97
percent of perennial streams in the
Black River subbasin, 70 percent of
perennial streams in the Gila River
subbasin, and 78 percent of the San
Francisco River subbasin and resulted
in confirmed fish kills in each subbasin
(Meyer 2011, p. 3, Table 1); each of
these streams is known to support
populations of either northern Mexican
or narrow-headed gartersnakes.
Although the Black River drainage
received no moderate or high-severity
burns as a result of the 2011 Wallow
Fire, the Fish and Snake Creek
subbasins (tributaries to the Black River)
were severely burned (Coleman 2011, p.
2). Post-fire fisheries surveys above
Wildcat Point in the Black River found
no fish in a reach extending up to the
confluence with the West Fork of the
Black River. This was likely due to
subsequent ash and sediment flows that
had occurred there (Coleman 2011, p.
2). Fisheries surveys of the Black River
in 2012 also reflected a largely absent
prey base for narrow-headed
gartersnakes (narrow-headed
gartersnakes observed appeared to be in
starving condition), but young-of-theyear native fish were detected, which
may signal the beginning of fish
recruitment (Lopez et al. 2012, entire).
Post-fire fisheries surveys at ‘‘the Box,’’
in the Blue River, detected only a single
native fish. This was also likely due to
ash and sediment flows and the
associated subsequent fish kills that had
occurred there, extending down to the
Gila River Box in Safford, Arizona
(Coleman 2011, pp. 2–3). The East Fork
Black River subbasin experienced
moderate to high-severity burns in 23
percent of its total acreage that resulted
in declines in Apache trout and native
sucker populations, but speckled dace
and brown trout remained prevalent as
of 2011 (Coleman 2011, p. 3). These fire
data suggest that the persistence of the
prey base for northern Mexican and
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narrow-headed gartersnakes in the Black
River, and narrow-headed gartersnakes
in the lower Blue River, will be
precarious into the near- to mid-term
future, as will likely be the stability of
gartersnake populations there.
Immediate post-fire fish sampling in
Eagle Creek confirmed that fish
populations had been severely depleted,
but that some level of population
rebound had occurred by 2 years postfire (Marsh 2013, pers. comm.).
Several large wildfires have occurred
historically on the Gila National Forest.
These fires have resulted in excessive
sedimentation of streams and affected
resident fish populations that serve as
prey for narrow-headed gartersnakes.
From 1989–2004, numerous wildfires
cumulatively burned much of the
uplands within the Gila National Forest,
which resulted in most perennial
streams in the area experiencing ash
flows and elevated sedimentation (Paroz
et al. 2006, p. 55). More recently, the
2012 Whitewater-Baldy Complex Fire in
the Gila National Forest in New Mexico
is the largest wildfire in that State’s
history. This wildfire was active for
more than 5 weeks and consumed
approximately 300,000 acres (121,406
ha) of ponderosa, mixed-conifer,
pinyon-juniper, and grassland habitat
(InciWeb 2012). Over 25 percent of the
burn area experienced high-moderate
burn severity (InciWeb 2012) and
included several subbasins occupied by
narrow-headed gartersnakes such as the
Middle Fork Gila River, West Fork Gila
River, Iron Creek, the San Francisco
River, Whitewater Creek, Turkey Creek,
and Mineral Creek (Brooks 2012, Table
1; Hellekson 2013, pers. comm.). Other
extant populations of the narrowheaded gartersnake in Gilita and South
Fork Negrito Creeks are also expected to
be impacted from the 2012 WhitewaterBaldy Complex Fire. Narrow-headed
gartersnake populations in the Middle
Fork Gila River and Whitewater Creek
formerly represented two of the four
most robust populations known from
New Mexico, and two of the five known
rangewide, and are expected to have
been severely jeopardized by post-fire
effects to their prey base. Thus, we now
consider them currently as likely not
viable, at least until the watershed
stabilizes and again supports a fish
community, or perhaps the next 5–10
years. In reference to Gila trout
populations, Brooks (2012, p. 3) stated
that fish populations are expected to be
severely impacted in the West Fork Gila
River and Whitewater Creek. The loss of
fish communities in affected streams is
likely to lead to associated declines, or
potential extirpations, in affected
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narrow-headed gartersnake populations
as a result of the collapse in their prey
base.
Since 2000, several wildfires have
affected occupied narrow-headed
gartersnake habitat on the Gila National
Forest. The West Fork Gila subbasin was
affected by the 2002 Cub Fire, the 2003
Dry Lakes Fire, and the 2011 Miller Fire;
each resulted in post-fire ash and
sediment flows, which adversely
affected fish populations used by
narrow-headed gartersnakes (Hellekson
2012a, pers. comm.). In 2011, the Miller
Fire significantly affected the Little
Creek subbasin and has resulted in
substantive declines in abundance of
the fish community (Hellekson 2012a,
pers. comm.). Dry Blue and Campbell
Blue creeks were affected by the 2011
Wallow Fire (Hellekson 2012a, pers.
comm.). Saliz Creek was highly affected
by the 2006 Martinez Fire (Hellekson
2012a, pers. comm.). Turkey Creek was
heavily impacted by the Dry Lakes Fire
in 2003, which resulted in an extensive
fish kill, but the fish community has
since rebounded (Hellekson 2012a, pers.
comm.). It is not certain how long the
fish community was depleted or absent
from Turkey Creek, but it is suspected
that the narrow-headed gartersnake
population there may have suffered
declines from the loss of their prey base,
as evidenced by the current low
population numbers. Black Canyon was
affected by large ash and debris flows
from the 2013 Silver Fire (USFS 2013,
entire). Prior to the 2002 Dry Lakes Fire,
Turkey Creek was largely populated by
nonnative, predatory fish species, in its
lower reaches. Upper reaches were
largely dominated by native fish
species, which have since rebounded in
numbers (Hellekson 2012a, pers.
comm.), and may provide high-quality
habitat for narrow-headed gartersnakes,
once the subbasin has adequately
stabilized.
Effects to northern Mexican and
narrow-headed gartersnake habitat from
wildfire should be considered in light of
effects to the structural habitat and
effects to the prey base. Post-fire effects
vary with burn severity, percent of area
burned within each severity category,
and the intensity and duration of
precipitation events that follow
(Coleman 2011, p. 4). Low-severity
burns within riparian habitat can
actually have a rejuvenating effect by
removing decadent ground cover and
providing nutrients to remaining
vegetation. As a result, riparian
vegetative communities may be more
resilient to wildfire, given that water is
present (Coleman 2011, p. 4). Willows,
an important component to narrowheaded gartersnake habitat, can be
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positively affected by low-severity
burns, as long as the root crowns are not
damaged (Coleman 2011, p. 4). Highseverity burns that occur within the
floodplain of occupied habitat are
expected to have some level of shorter
term effect on resident gartersnake
populations through effects to the
vegetative structure and abundance,
which may include a reduction of
basking sites and a loss of cover, which
could increase the risk of predation.
These potential effects need further
study. Post-fire ash flows, flooding, and
impacts to native prey populations are
longer term effects and can occur for
many years after a large wildfire
(Coleman 2011, p. 2).
Post-fire flooding with significant ash
and sediment loads can result in
significant declines, or even the
collapse, of resident fish communities,
which poses significant concern for the
persistence of resident gartersnake
populations in affected areas.
Sedimentation can adversely affect fish
populations used as prey by northern
Mexican or narrow-headed gartersnakes
by: (1) Interfering with respiration; (2)
reducing the effectiveness of fish’s
visually based hunting behaviors; and
(3) filling in interstitial spaces (spaces
between cobbles, etc., on the stream
floor) of the substrate, which reduces
reproduction and foraging success of
fish (Wheeler et al. 2005, p. 145).
Excessive sediment also fills in
intermittent pools required for
amphibian prey reproduction and
foraging. Siltation of the rocky
interstitial spaces along stream bottoms
decreases the dissolved oxygen content
where fish lay their eggs, resulting in
depressed recruitment of fish and a
subsequent reduction in prey
abundance for northern Mexican and
narrow-headed gartersnakes through the
loss of prey microhabitat (Nowak and
Santana-Bendix 2002, pp. 37–38). As
stated above, sediment can lead to
several effects in resident fish species
used by northern Mexican or narrowheaded gartersnakes as prey, which can
ultimately cause increased direct
fatalities, reduced reproductive success,
lower overall abundance, and
reductions in prey species composition
as documented by Wheeler et al. (2005,
p. 145). The underwater foraging ability
of narrow-headed gartersnakes (de
Queiroz 2003, p. 381) and likely
northern Mexican gartersnakes is largely
based on vision and is also directly
compromised by excessive turbidity
caused by sedimentation of water
bodies. Suspended sediment in the
water column may reduce the narrowheaded gartersnake’s visual hunting
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efficiency from effects to water clarity,
based on research conducted by de
Queiroz (2003, p. 381) that concluded
the species relied heavily on visual cues
during underwater striking behaviors.
The presence of adequate interstitial
spaces along stream floors may be
particularly important for narrowheaded gartersnakes. Hibbitts et al.
(2009, p. 464) reported the precipitous
decline of narrow-headed gartersnakes
in a formerly robust population in the
San Francisco River at San Francisco
Hot Springs from 1996 to 2004. The
exact cause for this decline is uncertain,
but the investigators suspected that a
reduction in interstitial spaces along the
stream floor from an apparent
conglomerate, cementation process may
have affected the narrow-headed
gartersnake’s ability to successfully
anchor themselves to the stream bottom
when seeking refuge or foraging for fish
(Hibbitts et al. 2009, p. 464). These
circumstances would likely result in
low predation success and eventually
starvation. Other areas where
sedimentation has affected either
northern Mexican or narrow-headed
gartersnake habitat are Cibecue Creek in
Arizona, and the San Francisco River
and South Fork Negrito Creek in New
Mexico (Rosen and Schwalbe 1988, p.
46; Arizona Department of Water
Resources 2011, p. 1; Hellekson 2012a,
pers. comm.). The San Francisco River
in Arizona was classified as impaired
due to excessive sediment from its
headwaters downstream to the Arizona–
New Mexico border (Arizona
Department of Water Resources 2011, p.
1). South Fork Negrito Creek is also
listed as impaired due to excessive
turbidity (Hellekson 2012a, pers.
comm.).
Potential mechanisms exist that can
ameliorate the effects of wildfires, such
as prescribed fire, use of wildland fire,
fuels management, and timber harvest,
and can sustain desired conditions for
fire-adapted ecosystems and provide
habitat for threatened and endangered
species, but will only be effective at a
landscape scale. The Guidance for
Implementation of Federal Wildland
Fire Management Policy is the
Department of Agriculture’s single
cohesive Federal fire policy, and it was
updated in February 2009. The intent of
this policy is to solidify that the full
range of strategic and tactical options
are available and considered in the
response to every wildland fire (USFS
2013, entire). Benefits are considered to
include the movement of vegetation
toward desired conditions, a greater
contribution to landscape restoration,
control of invasive species, a reduction
in uncharacteristic wildfire across the
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broader landscape, and the resiliency of
potential natural vegetation types to
adapt to climate change (USFS 2013,
entire). We are uncertain whether such
projects can be completed with the
scope and urgency required to reverse
the current trend of massive, highintensity wildfires in the southwest but
intend to facilitate their implementation
as project cooperators. We conclude that
effects of high-intensity wildfires are
threatening narrow-headed gartersnakes
with increasing likelihood of future
impacts as a result of climate change.
Summary
The presence of water is critical to
both northern Mexican and narrowheaded gartersnakes and their primary
prey species because their ecology and
natural histories are strongly linked to
water. Several factors, both natural and
manmade, contribute to the continued
degradation and dewatering of aquatic
habitat throughout the range of northern
Mexican and narrow-headed
gartersnakes. Increasing human
population growth is driving higher and
higher demands for water in both the
United States and Mexico. Water is
subsequently secured through dams,
diversions, flood-control projects, and
groundwater pumping, which affects
gartersnake habitat through reductions
in flow and complete dewatering of
stream reaches. Entire reaches of the
Gila, Salt, Santa Cruz, and San
Francisco Rivers, as well as numerous
other rivers throughout the Mexican
Plateau in Mexico that were historically
occupied by either or both northern
Mexican or narrow-headed gartersnakes,
are now completely dry due to
diversions, dams, and groundwater
pumping. Several groundwater basins
within the range of northern Mexican
and narrow-headed gartersnakes in the
United States are considered active
management areas where pumping
exceeds recharge, which is a constant
threat to surface flow in streams and
rivers connected to these aquifers.
Reduced flows concentrate northern
Mexican and narrow-headed
gartersnakes and their prey with
harmful nonnative species, which
accelerate and amplify adverse effects of
native–nonnative community
interactions. Where surface water
persists, increasing land development
and recreation use adjacent to and
within riparian habitat has led to further
reductions in stream flow, removal or
alteration of vegetation, and increased
frequency of adverse human
interactions with gartersnakes.
Exacerbating the effects of increasing
human populations and higher water
demands, climate change predictions
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include increased aridity, lower annual
precipitation totals, lower snow pack
levels, higher variability in flows (lower
low-flows and higher high-flows), and
enhanced stress on ponderosa pine
communities in the southwestern
United States and northern Mexico.
Increased stress to ponderosa pine
forests places them at higher risk of
high-intensity wildfires, the effects of
which are discussed below. Climate
change has also been predicted to
enhance the abundance and distribution
of harmful nonnative species, which
adversely affect northern Mexican and
narrow-headed gartersnakes.
Cienegas, a unique and important
habitat for northern Mexican
gartersnakes, have been adversely
affected or eliminated by a variety of
historical and current land uses in the
United States and Mexico, including
streambed modification, intensive
livestock grazing, woodcutting, artificial
drainage structures, stream flow
stabilization by upstream dams,
channelization, and stream flow
reduction from groundwater pumping
and water diversions. The historical loss
of the cienega habitat of the northern
Mexican gartersnake has resulted in
local population declines or
extirpations, negatively affecting its
status and contributing to its decline
rangewide.
Wildfire has historically been a
natural and important disturbance factor
within the range of northern Mexican
and narrow-headed gartersnakes.
However, in recent decades, forest
management policies in the United
States have favored fire suppression, the
result of which has led to wildfires of
unusual proportions, particularly along
the Mogollon Rim of Arizona and New
Mexico. These policies are generally not
in place in Mexico, and consequently,
wildfire is not viewed as a significant
threat to the northern Mexican
gartersnake in Mexico. However, in the
last 2 years, both Arizona (2011 Wallow
Fire) and New Mexico (2012
Whitewater-Baldy Complex Fire) have
experienced the largest wildfires in their
respective State histories, which is
indicative of the last decade having
been punctuated by wildfires of
significant magnitude. High-intensity
wildfire has been shown to result in
significant ash and sediment flows into
habitat occupied by northern Mexican
or narrow-headed gartersnakes,
resulting in significant reductions of
their fish prey base and, in some
instances, total fish kills. The interstitial
spaces between rocks located along the
stream floor are important habitat for
the narrow-headed gartersnake because
of its specialized foraging strategy and
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specialized diet. These spaces are also
important spawning and egg deposition
habitat for native fish species used as
prey by narrow-headed gartersnakes.
When these spaces fill in with sediment,
the narrow-headed gartersnake may be
unable to forage successfully and may
succumb to stress created by a
depressed prey base.
A significant reduction or absence of
a prey base results in stress of resident
gartersnake populations and can result
in local population extirpations. Also,
narrow-headed gartersnakes are
believed to rely heavily on visual cues
while foraging underwater; increased
turbidity from suspended fine sediment
in the water column is likely to impede
their ability to use visual cues at some
level. Factors that result in depressed
foraging ability from excessive
sedimentation are likely to be enhanced
when effects from harmful nonnative
species are also acting on resident
northern Mexican and narrow-headed
gartersnake populations. We consider
the narrow-headed gartersnake to be
particularly threatened by the effects of
wildfires as described because they
occur throughout its range, the species
is a fish-eating specialist that is
unusually vulnerable to localized fish
kills, and wildfire has already
significantly affected two of the last
remaining five populations that were
formerly considered viable, pre-fire. We
have demonstrated that high-intensity
wildfires have the potential to eliminate
gartersnake populations through a
reduction or loss of their prey base.
Since 1970, wildfires have adversely
impacted the native fish prey base in 6
percent of the historical distribution of
northern Mexican gartersnakes in the
United States and 21 percent of that for
narrow-headed gartersnakes rangewide,
according to GIS analysis. These
percentages represent only stream miles
within fire perimeters, not downstream
effects of ash flows within drainages,
which would undoubtedly increase the
percentage of habitat impacted, at least
for narrow-headed gartersnakes, whose
distribution overlaps more concisely
with more and larger wildfires over
recent decades.
All of these conditions affect the
primary drivers of gartersnake habitat
suitability (the presence of water and
prey) and exist in various degrees
throughout the range of both gartersnake
species. Collectively, they reduce the
amount and arrangement of physically
suitable habitat for northern Mexican
and narrow-headed gartersnakes over
their regional landscapes. The genetic
representation of each species is
threatened when populations become
disconnected and isolated from
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neighboring populations because the
length or area of dewatered zones is too
great for dispersing individuals to
overcome. Therefore, normal colonizing
mechanisms that would otherwise
reestablish populations where they have
become extirpated are no longer viable.
This subsequently leads to a reduction
in species redundancy when isolated,
small populations are at increased
vulnerability to the effects of stochastic
events, without a means for natural
recolonization. Ultimately, the effects of
scattered, small, and disjunct
populations, without the means to
naturally recolonize, is weakened
species resiliency as a whole, which
ultimately enhances the risk of either or
both species becoming endangered or
going extinct. Therefore, based on the
best available scientific and commercial
information, we conclude that land uses
or conditions described above that alter
or dewater northern Mexican and
narrow-headed gartersnake habitat are
threats rangewide, now and in the
foreseeable future.
Other Cumulative and Synergistic Effect
of Threats on Low-Density Populations
(Northern Mexican and Narrow-Headed
Gartersnakes)
In most locations where northern
Mexican or narrow-headed gartersnakes
historically occurred or still occur
currently, two or more threats are likely
acting in combination with regard to
their influence on the suitability of
those habitats or on the species
themselves. Many threats could be
considered minor in isolation, but when
they affect gartersnake populations in
combination with other threats, become
more serious. We have concluded that
in as many as 24 of 29 known localities
in the United States (83 percent), the
northern Mexican gartersnake
population is likely not viable and may
exist at low population densities that
could be threatened with extirpation or
may already be extirpated. We also
determined that in as many as 29 of 38
known localities (76 percent), the
narrow-headed gartersnake population
is likely not viable and may exist at low
population densities that could be
threatened with extirpation or may
already be extirpated, but survey data
are lacking in areas where access is
restricted. We have also discussed how
harmful nonnative species have affected
recruitment of gartersnakes across their
range. In viable populations,
gartersnakes are resilient to the loss of
individuals through ongoing
recruitment into the reproductive age
class. However, when northern Mexican
or narrow-headed gartersnakes occur at
low population densities in the absence
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of appropriate recruitment, the loss of
even a few adults could substantially
increase the risk of extirpation of local
populations. Below, we discuss threats
that, when considered in combination,
can appreciably threaten low-density
populations of these species with
extirpation.
Historical and Unmanaged Livestock
Grazing and Agricultural Land Uses
(Northern Mexican and Narrow-Headed
Gartersnake) (Factor A)
Currently in the United States,
livestock grazing is a largely managed
activity, but in Mexico, livestock grazing
is much less managed or unmanaged
altogether. Several examples of extant
gartersnake populations (in some cases,
apparently robust populations) in
Mexico were found in habitat that was
heavily grazed with no riparian
vegetation development; these sites
were coincidently free or largely free of
harmful nonnative species (Burger 2007,
entire). Historical livestock grazing has
damaged approximately 80 percent of
stream, cienega, and riparian
ecosystems in the western United States
(Kauffman and Krueger 1984, pp. 433–
435; Weltz and Wood 1986, pp. 367–
368; Cheney et al. 1990, pp. 5, 10;
Waters 1995, pp. 22–24; Pearce et al.
1998, p. 307; Belsky et al. 1999, p. 1).
Fleischner (1994, p. 629) found that
‘‘Because livestock congregate in
riparian ecosystems, which are among
the most biologically rich habitats in
arid and semiarid regions, the ecological
costs of grazing are magnified at these
sites.’’ Stromberg and Chew (2002, p.
198) and Trimble and Mendel (1995, p.
243) also discussed the propensity for
cattle to remain within or adjacent to
riparian communities. Expectedly, this
behavior is more pronounced in more
arid regions (Trimble and Mendel 1995,
p. 243). Effects from historical or
unmanaged grazing include: (1)
Declines in the structural richness of the
vegetative community; (2) losses or
reductions of the prey base; (3)
increased aridity of habitat; (4) loss of
thermal cover and protection from
predators; (5) a rise in water
temperatures to levels lethal to larval
stages of amphibian and fish
development; and (6) desertification
(Szaro et al. 1985, p. 362; Schulz and
Leininger 1990, p. 295; Schlesinger et
al. 1990, p. 1043; Belsky et al. 1999, pp.
8–11; Zwartjes et al. 2008, pp. 21–23).
In one rangeland study, it was
concluded that 81 percent of the
vegetation that was consumed,
trampled, or otherwise removed was
from a riparian area, which amounted to
only 2 percent of the total grazing space,
and that these actions were 5 to 30 times
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higher in riparian areas than on the
uplands (Trimble and Mendel 1995, pp.
243–244). However, according to one
study along the Agua Fria River,
herbaceous ground cover can recover
quickly from heavy grazing pressure
(Szaro and Pase 1983, p. 384).
Additional information on the effects of
historical livestock grazing can be found
in Sartz and Tolsted (1974, p. 354);
Rosen and Schwalbe (1988, pp. 32–33,
47); Clary and Webster (1989, p. 1);
Clary and Medin (1990, p. 1); Orodho et
al. (1990, p. 9); and Krueper et al. (2003,
pp. 607, 613–614).
Szaro et al. (1985, p. 360) assessed the
effects of historical livestock
management on a related taxon and
found that western (terrestrial)
gartersnake (Thamnophis elegans
vagrans) populations were significantly
higher (versus controls) in terms of
abundance and biomass in areas that
were excluded from grazing, where the
streamside vegetation remained lush,
than where uncontrolled access to
grazing was permitted. This effect was
complemented by higher amounts of
cover from organic debris from ungrazed
shrubs that accumulate as the debris
moves downstream during flood events.
Specifically, results indicated that snake
abundance and biomass were
significantly higher in ungrazed habitat,
with a five-fold difference in number of
snakes captured, despite the difficulty
of making observations in areas of
increased habitat complexity (Szaro et
al. 1985, p. 360). Szaro et al. (1985, p.
362) also noted the importance of
riparian vegetation for the maintenance
of an adequate prey base and as cover
in thermoregulation and predation
avoidance behaviors, as well as for
foraging success. Direct fatalities of
amphibian species, in all life stages,
from being trampled by livestock has
been documented (Bartelt 1998, p. 96;
Ross et al. 1999, p. 163). Gartersnakes
may, on occasion, be trampled by
livestock. A black-necked gartersnake
(Thamnophis cyrtopsis cyrtopsis) had
apparently been killed by livestock
trampling along the shore of a stock tank
in the Apache–Sitgreaves National
Forest, within an actively grazed
allotment (Chapman 2005).
Subbasins where historical grazing
has been documented as a suspected
contributing factor for either northern
Mexican or narrow-headed gartersnake
declines include the Verde, Salt, Agua
Fria, San Pedro, Gila, and Santa Cruz
(Hendrickson and Minckley 1984, pp.
140, 152, 160–162; Rosen and Schwalbe
1988, pp. 32–33; Girmendonk and
Young 1997, p. 47; Hale 2001, pp. 32–
34, 50, 56; Voeltz 2002, pp. 45–81;
Krueper et al. 2003, pp. 607, 613–614;
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Forest Guardians 2004, pp. 8–10;
Holycross et al. 2006, pp. 52–61;
Paradzick et al. 2006, pp. 90–92; USFS
2008). Livestock grazing still occurs in
these subbasins but is a largely managed
land use and is not likely to pose
significant threats to either northern
Mexican or narrow-headed gartersnakes
where closely managed. In cases where
poor livestock management results in
fence lines in persistent disrepair,
providing unmanaged livestock access
to occupied habitat, adverse effects from
loss of vegetative cover may result, most
likely in the presence of harmful
nonnative species. As we described
above, however, we strongly suspect
that northern Mexican and narrowheaded gartersnakes are somewhat
resilient to physical habitat disturbance
where harmful nonnative species are
absent.
The creation and maintenance of
stock tanks is an important component
to livestock grazing in the southwestern
United States. Stock tanks associated
with livestock grazing may facilitate the
spread of harmful nonnative species
when they are intentionally or
unintentionally stocked by anglers and
private landowners (Rosen et al. 2001,
p. 24). The management of stock tanks
is an important consideration for
northern Mexican gartersnakes in
particular. Stock tanks associated with
livestock grazing can be intermediary
‘‘stepping stones’’ in the dispersal of
nonnative species from larger source
populations to new areas (Rosen et al.
2001, p. 24). The effects of livestock
grazing at stock tanks on northern
Mexican gartersnakes depend on how
they are managed. Dense bank and
aquatic vegetation is an important
habitat characteristic for the northern
Mexican gartersnake in the presence of
harmful nonnative species. This
vegetation can be affected if the
impoundment is poorly managed. When
harmful nonnative species are absent,
the presence of bank line vegetation is
less important. Well-managed stock
tanks provide important habitat for
northern Mexican gartersnakes and their
prey base, especially when the tank: (1)
Remains devoid of harmful nonnative
species while supporting native prey
species; (2) provides adequate
vegetation cover; and (3) provides
reliable water sources in periods of
prolonged drought. Given these benefits
of well-managed stock tanks, we believe
well-managed stock tanks are an
important, even vital at this time,
component to northern Mexican
gartersnake conservation and recovery.
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Road Construction, Use, and
Maintenance (Northern Mexican and
Narrow-Headed Gartersnake) (Factor A)
Roads can pose unique threats to
herpetofauna, and specifically to species
like the northern Mexican gartersnake,
its prey base, and the habitat where it
occurs. The narrow-headed gartersnake,
alternatively, is probably less affected
by roads due to its more aquatic nature.
Roads fragment occupied habitat and
can result in diminished genetic
variability in populations from
increased fatality from vehicle strikes
and adverse human encounters as
supported by current research on
eastern indigo snakes (Breininger et al.
2012, pp. 364–366). Roads often track
along streams and present a fatality risk
to gartersnakes seeking more upland,
terrestrial habitat for brumation and
gestation. Roads may cumulatively
impact both species through the
following mechanisms: (1)
Fragmentation, modification, and
destruction of habitat; (2) increase in
genetic isolation; (3) alteration of
movement patterns and behaviors; (4)
facilitation of the spread of nonnative
species via human vectors; (5) an
increase in recreational access and the
likelihood of subsequent, decentralized
urbanization; (6) interference with or
inhibition of reproduction; (7)
contributions of pollutants to riparian
and aquatic communities; (8) reduction
of prey communities; and (9) acting as
population sinks (when population
death rates from vehicle strikes exceed
birth rates in a given area) (Rosen and
Lowe 1994, pp. 146–148; Waters 1995,
p. 42; Foreman and Alexander 1998, p.
220; Trombulak and Frissell 2000, pp.
19–26; Carr and Fahrig 2001, pp. 1074–
1076; Hels and Buchwald 2001, p. 331;
Smith and Dodd 2003, pp. 134–138;
Angermeier et al. 2004, pp. 19–24;
Shine et al. 2004, pp. 9, 17–19; Andrews
and Gibbons 2005, pp. 777–781;
Wheeler et al. 2005, pp. 145, 148–149;
Roe et al. 2006, p. 161; Sacco 2007, pers.
comm.; Ouren et al. 2007, pp. 6–7, 11,
16, 20–21; Jones et al. 2011, pp. 65–66;
Hellekson 2012a, pers. comm.).
Perhaps the most common factor in
road fatality of snakes is the propensity
for drivers to unintentionally and
intentionally run them over, both
because people often dislike snakes
(Rosen and Schwalbe 1988, p. 43; Ernst
and Zug 1996, p. 75; Green 1997, pp.
285–286; Nowak and Santana-Bendix
2002, p. 39) and because they can be
difficult to avoid when crossing roads at
perpendicular angles (Klauber 1956, p.
1026; Langley et al. 1989, p. 47; Shine
et al. 2004, p. 11). Fatality data for
northern Mexican gartersnakes have
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been collected at the Bubbling Ponds
Hatchery since 2006. Of the 15 dead
specimens, 8 were struck by vehicles on
roads within or adjacent to the hatchery
ponds, perhaps while crossing between
ponds to forage (Boyarski 2011, pp. 1–
3). Van Devender and Lowe (1977, p.
47), however, observed several northern
Mexican gartersnakes crossing the road
at night after the commencement of the
summer monsoon (rainy season), which
highlights the seasonal variability in
surface activity of this snake. Wallace et
al. (2008, pp. 243–244) documented a
vehicle-related fatality of a northern
Mexican gartersnake on Arizona State
Route 188 near Tonto Creek that
occurred in 1995.
Adverse Human Interactions With
Gartersnakes (Northern Mexican and
Narrow-Headed Gartersnake) (Factor E)
A fear of snakes is generally and
universally embedded in modern
culture and is prevalent in the United
States (Rosen and Schwalbe 1988, p. 43;
Ernst and Zug 1996, p. 75; Green 1997,
pp. 285–286; Nowak and SantanaBendix 2002, p. 39). We use the phrase
‘‘adverse human interaction’’ to refer to
the act of humans directly injuring or
killing snakes out of a sense of fear or
anxiety (ophidiophobia), or for no
apparent purpose. One reason the
narrow-headed gartersnake is vulnerable
to adverse human interactions is
because of its appearance. The narrowheaded gartersnake is often confused for
a venomous water moccasin
(cottonmouth, Agkistrodon piscivorus),
because of its triangular-shaped head
and propensity to be found in or near
water (Nowak and Santana-Bendix
2002, p. 38). Although the nearest water
moccasin populations are located over
700 miles (1,127 km) to the east in
central Texas, these misidentifications
prove fatal for narrow-headed
gartersnakes (Nowak and SantanaBendix 2002, p. 38).
Adverse human interaction may be
largely responsible for highly localized
extirpations in narrow-headed
gartersnakes based on the collection
history of the species at Slide Rock State
Park along Oak Creek, where high
recreation use is strongly suspected to
result in direct fatality of snakes by
humans (Nowak and Santana-Bendix
2002, pp. 21, 38). Declines in narrowheaded gartersnake populations in the
North and East Forks of the White River
have also been attributed to humans
killing snakes (Rosen and Schwalbe
1988, pp. 43–44). Locations in New
Mexico where this unnatural form of
fatality has been observed include Wall
Lake (Fleharty 1967, p. 219) and
Whitewater Creek (Hellekson 2012a,
pers. comm.). Areas with high visitation
and recreation levels, where this type of
fatality is most likely to be more
common, include the Middle Fork and
mainstem of the Gila River within 1
mile of Cliff Dwellings to Little Creek,
from the confluence with the East Fork
to Little Creek and the reach from
Turkey Creek to the Gila Bird Area
south of Highway 180 (Hellekson 2013,
pers. comm.), in Whitewater Creek from
the Catwalk to Glenwood (Hellekson
2012a, pers. comm.), near San Francisco
Hot Springs along the San Francisco
River (Hibbitts and Fitzgerald 2009, p.
466), the San Francisco River ‘‘Box’’,
Black Canyon near the FR150 crossing,
and the south Fork Negrito Creek
(Hellekson 2013, pers. comm.).
Environmental Contaminants (Northern
Mexican and Narrow-Headed
Gartersnake) (Factor A)
Environmental contaminants, such as
heavy metals, may be common at low
background levels in soils and, as a
result, concentrations are known to
bioaccumulate in food chains. A
bioaccumulative substance increases in
concentration in an organism or in the
food chain over time. A mid- to higherorder predator, such as a gartersnake,
may, therefore, accumulate these types
of contaminants over time in their fatty
tissues, which may lead to adverse
health effects (Wylie et al. 2009, p. 583,
Table 5). Campbell et al. (2005, pp. 241–
243) found that metal concentrations
accumulated in the northern watersnake
(Nerodia sipedon) at levels six times
that of their primary prey item, the
central stoneroller (a fish, Campostoma
anomalum). Metals, in trace amounts,
can be sequestered in the skin of snakes
(Burger 1992, p. 212), interfere with
metabolic rates of snakes (Hopkins et al.
1999, p. 1261), affect the structure and
function of their liver and kidneys, and
may also act as neurotoxins, affecting
nervous system function (Rainwater et
al. 2005, p. 670). Burger (1992, p. 209)
found higher concentrations of mercury,
lead, and chromium in the skin of
snakes, as opposed to whole body
tissue, ‘‘suggesting that frequent
shedding of skin can act as a method of
toxic excretion by snakes.’’ Drewett et
al. (2013, entire) studied mercury
accumulation in 4 species of snakes
(including the common gartersnake)
ranging from mostly aquatic to mostly
terrestrial in an attempt to ascertain if a
snake’s ecology affected the risk of
exposure and tissue accumulation
levels. They found that the more aquatic
the species’ ecology and prey base, the
higher risk for exposure and
accumulation of mercury (Drewett et al.
2013, pp. 7–8).
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Based on data collected in 2002–2010,
mercury appears to be bioaccumulating
in fish found in the lower reaches of
Tonto Creek, where northern Mexican
gartersnakes also occur (Rector 2010,
pers. comm.; Arizona Department of
Environmental Quality (ADEQ) 2011,
Table 1). In fact, the State record for the
highest mercury concentrations in fish
tissue was reported in Tonto Creek from
this investigation by Rector (2010, pers.
comm.). Mean mercury levels in fish
were found to range from 0.2–1.5 mg/kg.
The mean mercury concentration for all
fish was 1.1 mg/kg (ADEQ 2011, p. 3).
Due to the risks of adverse human
health effects, ADEQ (2011, p. 8)
recommends that smallmouth bass,
green sunfish, and black bullheads
caught from Tonto Creek not be
consumed, and common carp be
consumed sparingly. Because
gartersnakes eat fish, mercury may be
bioaccumulating in resident
populations, although no testing of
gartersnakes has occurred.
Specific land uses such as mining and
smelting, as well as road construction
and use, can be significant sources of
contaminants in air, water, or soil
through point-source and non-point
source mechanisms. Copper mining has
occurred in Arizona and adjacent
Mexico for centuries, and many of these
sites have smelters (now
decommissioned), which are former
sources of airborne contaminants.
Industrial mine sites occur in several
counties in Arizona (Greenlee, Pima,
Pinal, Yavapai, and Gila), as well as in
Grant County, New Mexico. The current
price of copper is high and is expected
to continue to increase into the next
several decades, fueled by international
development and economic growth.
Overall, 18 mines are either in
production or in the pre-production
phases of development in Arizona and
New Mexico. The mining industry in
Mexico is largely concentrated in the
northern tier of that country, with the
State of Sonora being the leading
producer of copper, gold, graphite,
molybdenum, and wollastonite, as well
as the leader among Mexican States
with regard to the amount of surface
area dedicated to mining (Stoleson et al.
2005, p. 56). The three largest mines in
Mexico (all copper) are found in Sonora
(Stoleson et al. 2005, p. 57). One of
these, the Cananea Copper Mine
adjacent to the Upper San Pedro River
in northern Sonora, was responsible for
a massive spill event. For two
consecutive years (1977–1978), two
leaching ponds overflowed into the San
Pedro River resulting in very acidic
water conditions and high levels of
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heavy metals such as copper, zinc, and
manganese (Eberhardt 1981, pp. 1, 16).
These releases caused the death of all
aquatic organisms in the San Pedro
River for a 60-mile (97-km) reach
downstream of the mine (Eberhardt
1981, pp. 1, 16).
The sizes of mines in Sonora vary
considerably, as do the known
environmental effects from miningrelated activities (from exploration to
long after closure), which include
contamination and drawdown of
groundwater aquifers, erosion, acid
mine drainage, fugitive dust, pollution
from smelter emissions, and landscape
clearing (Stoleson et al. 2005, p. 57). We
are aware of no specific research on
potential effects of mining or
environmental contaminants acting on
northern Mexican gartersnakes, but
conclude, based on the best available
scientific and commercial information,
that where this land use is prevalent,
contaminants may be a concern for
resident gartersnakes or their prey.
Northern Mexican Gartersnake
Competition With Marcy’s Checkered
Gartersnake (Northern Mexican
Gartersnake) (Factor E)
Preliminary research suggests that
Marcy’s checkered gartersnake
(Thamnophis marcianus marcianus)
may impact the future conservation of
the northern Mexican gartersnake in
southern Arizona. Rosen and Schwalbe
(1988, p. 31) hypothesized that bullfrogs
are more likely to eliminate northern
Mexican gartersnakes when Marcy’s
checkered gartersnakes are also present.
Marcy’s checkered gartersnake is a semiterrestrial species that is able to co-exist
to some degree with harmful nonnative
predators. This might be due to its
apparent ability to forage in more
terrestrial habitats, specifically during
the vulnerable juvenile size classes
(Rosen and Schwalbe 1988, p. 31; Rosen
et al. 2001, pp. 9–10). In every age class,
the northern Mexican gartersnake
forages in aquatic habitats where
nonnative predatory fish, bullfrogs, and
crayfish are present, which increases
not only the encounter rate between
predator and prey, but also the juvenile
fatality rate of the northern Mexican
gartersnake, which negatively affects
recruitment. As northern Mexican
gartersnake numbers decline within a
population, space becomes available for
occupation by Marcy’s checkered
gartersnakes. If competitive pressure
between these two species has existed
over time, it is reasonable to conclude
that northern Mexican gartersnakes
were successfully out-competing
Marcy’s checkered gartersnake prior to
the invasion of harmful nonnative
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species. Therefore, Marcy’s checkered
gartersnake may simply be filling the
ecological void left by the decline of the
northern Mexican gartersnake. At a
minimum, more research is needed to
determine the relationship between
these two gartersnake species.
Fatality From Entanglement Hazards
(Northern Mexican and Narrow-Headed
Gartersnake) (Factor E)
In addressing the effects of soil
erosion associated with road
construction projects or post-fire
remedial subbasin management, erosion
control materials placed on the ground
surface are often used. Examples of
products used in erosion or sediment
control include mulch control netting,
erosion control blankets, fiber rolls
(wattles), and reinforced silt fences
(California Coastal Commission 2012, p.
1). Erosion control is considered a best
management practice for most soildisturbing activities, and is broadly
required as mitigation across the United
States, in particular to avoid excess
sedimentation of streams and rivers.
Rolled erosion control products, such as
temporary erosion control blankets and
permanent turf reinforcement mats, are
two methods commonly used for these
purposes (Barton and Kinkead 2005, p.
34). These products use stitching or netlike mesh products to hold absorbent
media together. At a restoration site in
South Carolina, 19 snakes (15 dead)
representing 5 different species were
found entangled in the netting and had
received severe lacerations in the
process of attempting to escape their
entanglement (Barton and Kinkead
2005, p. 34). Stuart et al. (2001, pp. 162–
164) also reported the threats of net-like
debris to snake species. Kapfer and
Paloski (2011, p. 4) reported at least 31
instances involving 6 different species
of snake (including the common
gartersnake) in Wisconsin that had
become entangled in the netting used
for either erosion control or as a wildlife
exclusion product. In their review,
Kapfer and Paloski (2011, p. 6) noted
that 0.5-in.-by-0.5-in. mesh has the
greatest likelihood of entangling snakes.
Similar snake fatalities have not been
documented in Arizona or New Mexico,
according to our files. However, given
the broad usage of these materials across
the distribution of the northern Mexican
and narrow-headed gartersnakes, it is
not unlikely that fatalities occur, but go
unreported. The likelihood of either
gartersnake species becoming entangled
depends on the distance these erosion
control materials are used from water in
occupied habitat and the density of
potentially affected populations.
Because erosion control products are
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usually used to prevent sedimentation
of streams, there is a higher likelihood
for gartersnakes to become entangled.
We encourage those who use these
materials in or near gartersnake habitat
to take necessary precautions and
monitor their use as gartersnake
fatalities could occur.
Discarded fishing nets have also been
documented as a source of fatalities for
northern Mexican gartersnakes in the
area of Lake Chapala, Jalisco, Mexico
´
´
(Barragan-Ramırez and AscencioArrayga 2013, p. 159). Netting or seining
is not an authorized form of recreational
fishing for sport fish in Arizona or New
Mexico, but the practice is allowed in
either state for the collection of live
baitfish (AGFD 2013a, p. 57; NMDGF
2013, p. 17). Arizona fishing regulations
authorize seining for baitfish only where
the baitfish will be used and specify that
seining is not allowed in Coconino,
Apache, Pima, and Cochise Counties. In
other areas, it is suspected that most
seinng activity occurs at sites dominated
by warmwater sportfish, where these
gartersnakes are less likely to occur. We
are not certain of the frequency at which
these techniques are used for such
purposes in either state, but we do not
suspect that discarded nets or seines are
commonly left on-site where they could
ensnarl resident gartersnakes. However,
this practice is used in Mexico as a
primary means of obtaining freshwater
fish as a food source and may be more
of a threat to local northern Mexican
gartersnake populations where this
practice occurs.
Disease and Parasites (Northern
Mexican and Narrow-Headed
Gartersnake) (Factor C)
Our review of the scientific literature
did not find evidence that disease is a
current factor contributing to the
decline in northern Mexican or narrowheaded gartersnakes. However, a recent
wildlife health bulletin announced the
emergence of snake fungal disease (SFD)
within the eastern and midwestern
portions of the United States (Sleemen
2013, p. 1). SFD has now been
diagnosed in several terrestrial and
aquatic snake genera including Nerodia,
Coluber, Pantherophis, Crotalus,
Sistrurus, and Lampropeltis. Clinical
signs of SFD include scabs or crusty
scales, subcutaneous nodules, abnormal
molting, white opaque cloudiness of the
eyes, localized thickening or crusting of
the skin, skin ulcers, swelling of the
face, or nodules in the deeper tissues
(Sleemen 2013, p. 1). While fatalities
have been documented as a result of
SFD, population-level impacts have not,
due to the cryptic and solitary nature of
snakes and the lack of long-term
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monitoring data (Sleemen 2013, p. 1).
So far, no evidence of SFD has been
found in the genus Thamnophis, but the
documented occurrence of SFD in
ecologically similar, aquatic colubrids
such as Nerodia is cause for concern.
Parasites, such as the common
plerocercoid larvae of a
pseudophyllidean tapeworm (possibly
Spirometra spp.), have been observed in
northern Mexican gartersnakes
(Boyarski (2008b, pp. 5–6), which may
not be detrimental to the snake’s health
(Boyarski 2008b, p. 8). However,
´
Guzman (2008, p. 102) first documented
a Mexican gartersnake fatality from a
larval Eustrongylides sp. (endoparasitic
nematode), which ‘‘raises the possibility
that infection of Mexican gartersnakes
by Eustrongylides sp. larvae might cause
fatality in some wild populations,’’
especially if those populations are
under stress as a result of the presence
of other threats. Nowak et al. (2014, pp.
148–149) reported the first observation
of what appears as maternal
transmission of endoparasites,
specifically of the genus (Macdonaldius
sp.). We found no substantive evidence
that parasites represent a significant
threat to either gartersnake species.
Summary
We found numerous effects of
livestock grazing that have resulted in
the historical degradation of riparian
and aquatic communities that have
likely affected northern Mexican and
narrow-headed gartersnakes.
Mismanaged or unmanaged grazing can
have disproportionate effects to riparian
communities in arid ecosystems due to
the attraction of livestock to water,
forage, and shade. We found current
livestock grazing activities to be more of
a concern in Mexico, at least when it
occurs in areas that also support
harmful nonnative species. The most
profound impacts from livestock grazing
in the southwestern United States
occurred nearly 100 years ago, were
significant, and may still be affecting
some areas that have yet to fully
recover. Unmanaged or poorly managed
livestock operations likely have more
pronounced effects in areas impacted by
harmful nonnative species through a
reduction in cover. However, land
managers in Arizona and New Mexico
currently emphasize the protection of
riparian and aquatic habitat in allotment
management planning, usually through
fencing, rotation, monitoring, and range
improvements such as developing
remote water sources. Collectively,
these measures have reduced the
likelihood of significant adverse impacts
on northern Mexican or narrow-headed
gartersnakes, their habitat, and their
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prey base. We also recognize that, while
the presence of stock tanks on the
landscape can benefit nonnative
species, well-managed stock tanks are
currently an invaluable tool in the
conservation and recovery of northern
Mexican gartersnakes and their prey.
Other activities, factors, or conditions
that act in combination, such as road
construction, use, and management,
adverse human interactions,
environmental contaminants,
entanglement hazards, and competitive
pressures from sympatric species, occur
within the distribution of these
gartersnakes and have the propensity to
contribute to further population
declines or extirpations where
gartersnakes occur at low population
densities. An emerging skin disease,
SFD, has not yet been documented in
gartersnakes but has affected snakes of
many genera within the United States,
including ecologically similar species,
and may pose a future threat to northern
Mexican and narrow-headed
gartersnakes. Where low-density
populations are affected by these types
of threats described above, even the loss
of a few reproductive adults, especially
females, from a population can have
significant population-level effects,
most notably in the presence of harmful
nonnative species. Continued
population declines and extirpations
threaten the genetic representation of
each species because many populations
have become disconnected and isolated
from neighboring populations. This
subsequently leads to a reduction in
species redundancy and resiliency
when isolated, small populations are at
increased vulnerability to the effects of
stochastic events, without a means for
natural recolonization. Based on the
best available scientific and commercial
information, we conclude that these
threats have the tendency to act
synergistically and disproportionately
on low-density gartersnake populations
rangewide, now and in the foreseeable
future.
Adequacy and Effectiveness at Reducing
Identified Threats of Existing Regulatory
Mechanisms (Northern Mexican and
Narrow-Headed Gartersnake) (Factors D
and E)
Below, we examine whether existing
regulatory mechanisms are adequate to
address the threats to the northern
Mexican and narrow-headed
gartersnakes discussed under other
factors and whether these regulations
are acting to alleviate the threats
identified to the species. Section
4(b)(1)(A) of the Endangered Species
Act requires the Service to take into
account ‘‘those efforts, if any, being
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made by any State or foreign nation, or
any political subdivision of a State or
foreign nation, to protect such species.’’
We interpret this language to require us
to consider relevant Federal, State, and
Tribal laws, regulations, and other such
mechanisms that may minimize any of
the threats we describe in the threats
analysis under the other four factors, or
otherwise influence conservation of the
species. We give strongest weight to
statutes and their implementing
regulations, and management direction
that stems from those laws and
regulations. They are nondiscretionary
and enforceable, and are considered a
regulatory mechanism under this
analysis. Having evaluated the
significance of the threat as mitigated by
any such conservation efforts, we
analyze under Factor D the extent to
which existing regulatory mechanisms
are inadequate to address the specific
threats to the species. Regulatory
mechanisms, if they exist, may reduce
or eliminate the impacts from one or
more identified threats. In this section,
we review existing State and Federal
regulatory mechanisms to determine
whether they effectively reduce or
remove threats to the species.
A number of Federal statutes
potentially afford protection to northern
Mexican and narrow-headed
gartersnakes or their prey species. These
include section 404 of the Clean Water
Act (33 U.S.C. 1251 et seq.), Federal
Land Policy and Management Act (43
U.S.C. 1701 et seq.), National Forest
Management Act (16 U.S.C. 1600 et
seq.), National Environmental Policy
Act (NEPA; 42 U.S.C. 4321 et seq.), and
the Act. However, in practice, these
statutes have not been able to provide
sufficient protection to prevent the
currently observed downward trend in
northern Mexican and narrow-headed
gartersnakes or their prey species, and
the concurrent upward trend in threats.
Section 404 of the Clean Water Act
regulates placement of fill into waters of
the United States, including the
majority of northern Mexican and
narrow-headed gartersnake habitat.
However, many actions with the
potential to be highly detrimental to
both species, their prey base, and their
habitat, such as gravel mining and
irrigation diversion structure
construction and maintenance, may be
exempted from the Clean Water Act.
Other detrimental actions, such as bank
stabilization and road crossings, are
covered under nationwide permits that
receive limited environmental review. A
lack of thorough, site-specific analyses
for projects can allow substantial
adverse effects to northern Mexican or
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narrow-headed gartersnakes, their prey
base, or their habitat.
The majority of the extant populations
of northern Mexican and narrow-headed
gartersnakes in the United States occur
on lands managed by the U.S. Bureau of
Land Management (BLM) and U.S.
Forest Service. Both agencies have
riparian protection goals that may
provide habitat benefits to both species;
however, neither agency has specific
management plans for northern Mexican
or narrow-headed gartersnakes. As a
result, some of the significant threats to
these gartersnakes, for example, those
related to nonnative species, are not
necessarily addressed on these lands.
The BLM considers the northern
Mexican gartersnake as a ‘‘Sensitive
Species’’ by default, due to its status
under the Act (U.S. Bureau of Land
Management (USBLM) 2010), and
agency biologists actively attempt to
identify gartersnakes for their records
for snakes observed incidentally during
fieldwork (Young 2005). BLM policy
(BLM Manual Section 6840) requires
consideration of sensitive species
during planning of activities and
projects and mitigation of specific
threats. The BLM’s Resource
Management Plans include objectives
and management actions to benefit
riparian habitat and native fish; with
some addressing ‘‘invasive wildlife
species’’ (USBLM 2013, p. 2). When the
Agua Fria National Monument was
created in January 2000, lowland
leopard frogs, native fish, northern
Mexican gartersnakes, and riparian
habitat were designated as ‘‘monument
objects’’ under protection by the
National Monument (USBLM 2013, p.
3). Similar conservation provisions are
in place on the BLM’s National
Conservation Areas (NCAs), such as the
Las Cienegas NCA, San Pedro River
NCA, and the Gila Box Riparian NCA.
While these measures likely minimize
the effect of otherwise adverse regional
land use activities on the aquatic
community, gartersnake populations in
these areas remain in a precarious
status.
The U.S. Forest Service does not
include northern Mexican or narrowheaded gartersnakes on their
Management Indicator Species List, but
both species are included on the
Regional Forester’s Sensitive Species
List (USFS 2007, pp. 38–39). This
means they are considered in land
management decisions, and protective
measures can be implemented to
minimize adverse effects of otherwise
lawful activities. However we found no
examples of specific protective
measures that have been implemented
for these species. Individual U.S. Forest
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Service biologists who work within the
range of either northern Mexican or
narrow-headed gartersnakes may
opportunistically gather data for their
records on gartersnakes observed
incidentally in the field or coordinate
with other collaborators on surveys,
although it is not required. The Gila
National Forest mentions the narrowheaded gartersnake in their land and
resource management plan, which
includes standards relating to forest
management for the benefit of
endangered and threatened species as
identified through approved
management and recovery plans (Center
for Biological Diversity (CBD) et al.
2011, p. 18). Neither species is
mentioned in any other land and
resource management plan for the
remaining national forests where they
occur (CBD et al. 2011, p. 18).
The New Mexico Department of Game
and Fish lists the northern Mexican
gartersnake as State-endangered and the
narrow-headed gartersnake as Statethreatened (NMDGF 2006, Appendix H).
A species is State-endangered if it is in
jeopardy of extinction or extirpation
within the State; a species is Statethreatened if it is likely to become
endangered within the foreseeable
future throughout all or a significant
portion of its range in New Mexico
(NMDGF 2006, p. 52). ‘‘Take,’’ defined
as ‘‘to harass, hunt, capture or kill any
wildlife or attempt to do so’’ by New
Mexico Statutes Annotated (NMSA) 17–
2–38.L., is prohibited without a
scientific collecting permit issued by the
New Mexico Department of Game and
Fish as per NMSA 17–2–41.C and New
Mexico Administrative Code (NMAC)
19.33.6. However, while the New
Mexico Department of Game and Fish
can issue monetary penalties for illegal
take of either northern Mexican
gartersnakes or narrow-headed
gartersnakes, the same provisions are
not in place for actions that result in
loss or modification of their habitats
(NMSA 17–2–41.C and NMAC 19.33.6)
(Painter 2005).
Prior to 2005, the AGFD allowed for
take of up to four northern Mexican or
narrow-headed gartersnakes per person
per year as specified in Commission
Order 43. The AGFD defines ‘‘take’’ as
‘‘pursuing, shooting, hunting, fishing,
trapping, killing, capturing, snaring, or
netting wildlife or the placing or using
any net or other device or trap in a
manner that may result in the capturing
or killing of wildlife.’’ The AGFD
subsequently amended Commission
Order 43, effective January 2005. Take
of northern Mexican and narrow-headed
gartersnakes is no longer permitted in
Arizona without issuance of a scientific
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collecting permit (Ariz. Admin. Code
R12–4–401 et seq.) or special
authorization. While the AGFD can seek
criminal or civil penalties for illegal
take of these species, the same
provisions are not in place for actions
that result in destruction or
modification of the gartersnakes’
habitat. In addition to making the
necessary regulatory changes to promote
the conservation of northern Mexican
and narrow-headed gartersnakes, the
AGFD’s Nongame Branch continues to
be a strong partner in research and
survey efforts that further our
understanding of current populations,
and assist with conservation efforts and
the establishment of long-term
conservation partnerships.
Throughout Mexico, the Mexican
gartersnake is listed at the species level
of its taxonomy as ‘‘Amenazadas,’’ or
Threatened, by the Secretaria de Medio
Ambiente y Recursos Naturales
(SEMARNAT) (SEDESOL 2010, p. 71).
Threatened species are ‘‘those species,
or populations of the same, likely to be
in danger of disappearing in a short or
medium timeframe, if the factors that
negatively impact their viability, cause
the deterioration or modification of their
habitat or directly diminish the size of
their populations continue to operate’’
´
(Secretarıa de Desarrollo Social
(SEDESOL) 2010, p. 5). This designation
prohibits taking of the species, unless
specifically permitted, as well as
prohibits any activity that intentionally
destroys or adversely modifies its
habitat. Additionally, in 1988, the
Mexican Government passed a
regulation that is similar to the National
Environmental Policy Act of the United
States. This Mexican regulation requires
an environmental assessment of private
or government actions that may affect
wildlife or their habitat (SEDESOL 1988
´
Ley General del Equilibrio Ecologico y
´
la Proteccion al Ambiente (LGEEPA)).
The Mexican Federal agency known
´
as the Instituto Nacional de Ecologıa
(INE) is responsible for the analysis of
the status and threats that pertain to
species that are proposed for listing in
the Norma Oficial Mexicana NOM–059
(the Mexican equivalent to an
endangered and threatened species list),
and, if appropriate, the nomination of
species to the list. INE is generally
considered the Mexican counterpart to
the United States’ Fish and Wildlife
Service. INE developed the Method of
Evaluation of the Risk of Extinction of
the Wild Species in Mexico (MER),
which unifies the criteria of decisions
on the categories of risk and permits the
use of specific information fundamental
to listing decisions. The MER is based
on four independent, quantitative
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criteria: (1) Size of the distribution of
the taxon in Mexico; (2) state (quality)
of the habitat with respect to natural
development of the taxon; (3) intrinsic
biological vulnerability of the taxon;
and (4) impacts of human activity on the
taxon. INE began to use the MER in
2006; therefore, all species previously
listed in the NOM–059 were based
solely on expert review and opinion in
many cases. Specifically, until 2006, the
listing process under INE consisted of a
panel of scientific experts who
convened as necessary for the purpose
of defining and assessing the status and
threats that affect Mexico’s native
species that are considered to be at risk,
and applying those factors to the
definitions of the various listing
categories. In 1994, when the Mexican
gartersnake was placed on the NOM–
059 (SEDESOL 1994 (NOM–059–ECOL–
1994), p. 46) as a threatened species, the
decision was made by a panel of
scientific experts.
Although the Mexican gartersnake is
listed as a threatened species in Mexico
and based on our experience
collaborating with Mexico on transborder conservation efforts, no recovery
plan or other conservation planning
occurs because of this status, and
enforcement of the regulation protecting
the gartersnake is sporadic, depending
on available resources and location.
Based upon the best available scientific
and commercial information on the
status of the species, and the historic
and continuing threats to its habitat in
Mexico, our analysis concludes that
regulatory mechanisms enacted by the
Mexican Government to conserve the
northern Mexican gartersnake are not
adequate to address threats to the
species or its habitat.
In summary, we reviewed a number of
existing regulations that potentially
address issues affecting the northern
Mexican and narrow-headed
gartersnakes and their habitats. Mexican
law prohibits take of the northern
Mexican gartersnake and the intentional
destruction or modification of northern
Mexican gartersnake habitat. However
that law has not led to a reduction in
threats such that they no longer meet
the definition of endangered or
threatened under the Act. Furthermore,
most existing regulations in the United
States within the range of northern
Mexican and narrow-headed
gartersnakes were not specifically
designed to protect the gartersnakes or
their habitats, which is the overarching
threat to the species. For example,
Arizona and New Mexico both have
statutes designed for protection of statelisted species that prohibit the direct
collection of individuals. However
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neither state law is designed to provide
protection of habitat and ecosystems.
Therefore, these laws are not reducing
threats to the species such that they no
longer meet the definition of
endangered or threatened under the Act.
Current Conservation of Northern
Mexican and Narrow-Headed
Gartersnakes (Factor E)
Several conservation measures
implemented by land and resource
managers, private land owners, and
other stakeholders can directly or
indirectly benefit populations of
northern Mexican and narrow-headed
gartersnakes. For example, the AGFD’s
conservation and mitigation program
(CAMP; implemented under an existing
section 7 incidental take permit) has
committed to either stocking (with
captive-bred stock) or securing two
populations each of northern Mexican
and narrow-headed gartersnakes to help
minimize adverse effects to these
species from their sport fish stocking
program through 2021 (USFWS 2011,
Appendix C). Other CAMP
commitments include: (1) Developing a
gartersnake monitoring, research, and
restocking plan to guide CAMP
activities to establish or secure
populations; (2) developing outreach
material to reduce the deliberate killing
or injuring of gartersnakes (placed in
high angler access areas); (3) ensuring
that chemically renovated streams are
quickly restocked with native fish as
gartersnake prey; (4) conducting a live
bait assessment team to develop
recommendations to amend live bait
management; (5) reviewing and
updating outreach programs on the risks
to native aquatic species from the
transport of nonnative aquatic species;
(6) developing and implementing a
public education program on
gartersnakes; and (7) working with the
New Mexico Department of Game and
Fish to examine the roll of escaped
rainbow trout from Luna Lake into
tributaries to the San Francisco River in
supporting narrow-headed gartersnakes.
The programs’ management strategy is
encapsulated in AGFD (2014a, entire)
and progress on activities through June
2013 is reported in AGFD (2012c, pp.
26–30; 2013b, pp. 37–44).
Significant challenges will have to be
met for creating or securing two
populations each of northern Mexican
or narrow-headed gartersnakes. Captive
propagation, if used to create stock for
reintroductions, has only been possible
for northern Mexican gartersnakes.
Specifically, after approximately 6 years
of experimentation with captive
propagation at five institutions, using
two colonies of northern Mexican
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gartersnakes and three colonies of
narrow-headed gartersnakes, success
has been limited (see Gartersnake
Conservation Working Group (GCWG)
2007, 2008, 2009, 2010). In 2012 and
2013, approximately 60 northern
Mexican gartersnakes were produced at
one institution, 40 of which were
subsequently marked and released along
Cienega Creek. These were the first
gartersnakes of either species to be
produced under this program, but the
current status of released individuals
remains unknown. No narrow-headed
gartersnakes have been produced in
captivity under this program since its
inception. Secondly, in order to have
the greatest chance for success, the
process of ‘‘securing’’ a population of
either species will likely involve an
aggressive nonnative removal strategy,
and will have to account for habitat
connectivity to prevent reinvasion of
unwanted species. Therefore, securing a
population of either species may
involve removal of harmful nonnatives
from an entire subbasin or on a
landscape scale (Cotton et al. 2014, pp.
12–13). In situations where harmful
nonnatives do not pose a threat to a
given population, other types of
recovery actions may suffice.
To protect habitat for candidate,
threatened, and endangered species,
including northern Mexican
gartersnakes in the Agua Fria subbasin,
the AGFD purchased the approximate
200-acre (81-ha) Horseshoe Ranch along
the Agua Fria River located near the
Bloody Basin Road crossing, east of
Interstate 17 and southeast of Cordes
Junction, Arizona. The AGFD plans
(presumably in the next 5–10 years) to
introduce northern Mexican
gartersnakes, as well as lowland leopard
frogs and native fish species, into a large
pond, protected by bullfrog exclusion
fencing, located adjacent to the Agua
Fria River. The bullfrog exclusion
fencing around the pond will permit the
dispersal of northern Mexican
gartersnakes and lowland leopard frogs
from the pond, allowing the pond to act
as a source population to the Agua Fria
River. The AGFD’s short- to mid-term
conservation planning for Horseshoe
Ranch will help ensure the northern
Mexican gartersnake persists in this
historical locality.
In 2007, the New Mexico Department
of Game and Fish completed a recovery
plan for narrow-headed gartersnakes in
New Mexico (Pierce 2007, pp. 13–15)
that included the following management
objectives: (1) Researching the effect of
known threats to, and natural history of,
the species; (2) acquiring funding
sources for research, monitoring, and
management; (3) enhancing education
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and outreach; and (4) managing against
known threats to the species.
Implementation of the recovery plan
was to occur between the second half of
2007 through 2011, and was divided
into three main categories: (1) Improve
and maintain knowledge of potential
threats to the narrow-headed
gartersnake; (2) improve and maintain
knowledge of the biology of the narrowheaded gartersnake; and (3) develop and
maintain high levels of cooperation and
coordination between stakeholders and
interested parties (Pierce 2007, pp. 16–
17). Our review of the plan found that
it lacked specific threat-mitigation
commitments on the landscape, as well
as stakeholder accountability for
implementing activities prescribed in
the plan. We also found that actions
calling for targeted nonnative species
removal or management were absent in
the implementation schedule provided
in Pierce (2007, p. 17). As we have
discussed at length, harmful nonnative
species are the primary driver of
continued declines in both gartersnake
species. No recovery plan, conservation
plan, or conservation agreement
currently exists in New Mexico with
regard to the northern Mexican
gartersnake (NMDGF 2006, Table 6–3).
In Arizona’s State Wildlife Action
Plan 2012–2022 (SWAP) (AGFD 2012b,
Appendix E), both the northern Mexican
and narrow-headed gartersnake are Tier
1A Species of Greatest Conservation
Need (SGCN). SGCN include those
‘‘species that each State identified as
most in need of conservation actions’’
and Tier 1A species include ‘‘those
species for which the Department has
entered into an agreement or has legal
or other contractual obligations, or
warrants the protection of a closed
season’’ (AGFD 2012b, p. 16). The
SWAP is not a regulatory document,
and does not provide any specific
protections for either the gartersnakes
themselves, or their habitats. The AGFD
does not have specified or mandated
recovery goals for either the northern
Mexican or narrow-headed gartersnake,
nor has a conservation agreement or
recovery plan been developed for either
species.
Indirect benefits for both gartersnake
species occur through recovery actions
designed for their prey species. Since
the Chiricahua leopard frog was listed
as threatened under the Act, significant
strides have been made in its recovery,
and the mitigation of its known threats.
The northern Mexican gartersnake, in
particular, has likely benefitted from
these actions, at least in some areas,
such as at the Las Cienegas Natural
Conservation Area and in Scotia Canyon
of the Huachuca Mountains. However,
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much of the recovery of the Chiricahua
leopard frog has occurred in areas that
have not directly benefitted the northern
Mexican gartersnake, either because
these activities have occurred outside
the known distribution of the northern
Mexican gartersnake or because they
have occurred in isolated lentic systems
that are far removed from large
perennial streams that typically provide
source populations of northern Mexican
gartersnakes. In recent years, significant
strides have been made in controlling
bullfrogs on local landscape levels in
Arizona, such as in the Scotia Canyon
area, in the Las Cienegas National
Conservation Area, on the BANWR, and
in the vicinity of Pena Blanca Lake in
the Pajarito Mountains. Recent efforts to
return the Las Cienegas National
Conservation Area to a wholly native
biological community have involved
bullfrog eradication efforts, as well as
efforts to recover the Chiricahua leopard
frog and native fish species. These
actions should assist in conserving the
northern Mexican gartersnake
population in this area. Bullfrog control
has been shown to be most effective in
simple, lentic systems such as stock
tanks. Therefore, we encourage livestock
managers to work with resource
managers in the systematic eradication
of bullfrogs from stock tanks where they
occur, or at a minimum, ensure they are
never introduced.
An emphasis on native fish recovery
in fisheries management and enhanced
harmful nonnative species control to
favor native communities may be the
single most efficient and effective
manner to recover these gartersnakes, in
addition to appropriate management for
all listed or sensitive native fish and
amphibian species upon which they
prey. Alternatively, resource
management policies that are intended
to directly benefit or maintain harmful
nonnative communities, and which will
likely exclude native species, will
significantly reduce the potential for the
conservation and recovery of northern
Mexican and narrow-headed
gartersnakes, in those areas where they
overlap with habitat occupied by either
gartersnake.
Fisheries managers strive to balance
the needs of the recreational angling
community against those required by
native aquatic communities. Fisheries
management has direct implications for
the conservation and recovery of
northern Mexican and narrow-headed
gartersnakes in the United States.
Clarkson et al. (2005) discuss
management conflicts as a primary
factor in the decline of native fish
species in the southwestern United
States, and declare the entire native fish
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fauna as imperiled. The investigators
cite nonnative species as the most
consequential factor leading to
rangewide declines of native fish, and
that such declines prevent or negate
species’ recovery efforts from being
implemented or being successful
(Clarkson et al. 2005, p. 20).
Maintaining the status quo of current
management of fisheries within the
southwestern United States will have
serious adverse effects to native fish
species (Clarkson et al. 2005, p. 25),
which will affect the long-term viability
of northern Mexican and narrow-headed
gartersnakes and their potential for
recovery. Clarkson et al. (2005, p. 20)
also note that over 50 nonnative species
have been introduced into the
Southwest as either sportfish or baitfish,
and some are still being actively
stocked, managed for, and promoted by
both Federal and State agencies as
nonnative recreational fisheries.
To help resolve the fundamental
conflict of management between native
fish and recreational sport fisheries,
Clarkson et al. (2005, pp. 22–25)
propose the designation of entire
subbasins as having either native or
nonnative fisheries and manage for
these goals aggressively. The idea of
watershed-segregated fisheries
management is also supported by Marsh
and Pacey (2005, p. 62). As part of the
AGFD’s overall wildlife conservation
strategy, the AGFD has planned an
integrated fisheries management
approach (AGFD 2012b, p. 106), which
is apparently designed to manage
subbasins specifically for either
nonnative or native fish communities.
This strategy is described in detail in
AGFD (2009, entire), but the AGFD has
not yet initiated implementation of this
strategy or decided how fisheries will be
managed in Arizona’s subbasins, and we
are not aware of a specific
implementation timeline. However, the
‘‘current fish assemblage,’’ ‘‘current
recovery or conservation category,’’ and
‘‘current angling category’’ inform what
is referred to as Step 2c: Identification
of Current Fishery Values’’ (AGFD 2009,
pp. 10–11). Factors such as angler
access (which contributes directly to
angler use days (AUD)), existing fish
communities, and stream flow
considerations are likely to inform such
broadly based decisions.
Due to the relative scarcity of
perennial streams in arid regions such
as Arizona, several of Arizona’s large
perennial rivers present an array of
existing sport fishing opportunities and
angler access points, and already
contain harmful nonnative fish species
that are considered sport fish. We
anticipate that these rivers may be
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preferred as nonnative fisheries under
the watershed designation process.
Another significant and confounding
factor is the AGFD’s ‘‘no net loss’’
policy that addresses sport fishery
resources statewide. There is no official
written AGFD Commission guidance on
‘‘no net loss’’ according to AGFD (2009,
Appendix D), but ‘‘Commission policy
DOM [Arizona Game Fish Department
Operating Manual] A2.24, Wildlife
Management Program Goal and
Objective #6 states, ‘provide and
promote fishing opportunities to sustain
a minimum of 8,000,000 AUD per year
by June 30, 1997.’ Although this policy
has yet to be revised by the
Commission, based on current data, we
remain below 8,000,000 AUD’s
statewide (AGFD 2009, Appendix D). As
such, it was determined the
Department’s goal to manage for no net
loss is consistent with current
Commission policy (A2.24). The ‘‘no net
loss’’ policy is a guiding tenet, and its
implementation is directed as follows
(AGFD 2009, Appendix D):
‘‘When a sport fishery is valued less than
a native aquatic conservation value within a
management unit, the loss of sport fishing
opportunity will be compensated for by gain
of an equal number of AUDs in another area
or management unit. This opportunity will
be created within the same watershed when
possible. For this purpose, a watershed is
defined as a six-digit-numbered area
referenced on the USGS’s Hydrological Unit
Map. If this is not possible, the opportunity
will be created within the same Department
regional boundaries. Again, if this is not
possible, the opportunity will be created
somewhere within the State with extensive
coordination between regional staff. If a net
loss cannot be avoided, the Director will
evaluate if the loss is acceptable by gauging
the input from the public process leading to
the recommendation and may take the
information to the Commission at his
discretion. The replacement opportunity will
be initiated no more than two years following
the loss to anglers.’’
Extensive coordination between
AGFD and the Service will be required
under the no net loss policy with regard
to gartersnake conservation and
recovery because the amount of suitable
riparian and aquatic habitat is finite,
yet, somehow, the existing opportunity
for AUD must be maintained. This
increases the uncertainty for the
persistence of existing gartersnake
populations in Arizona.
Large perennial rivers that serve as
sport fisheries also currently serve as
important habitat for northern Mexican
or narrow-headed gartersnake. If
designated for sportfishing, fisheries
management of these rivers would likely
include the maintenance of predatory
sport fish species, which would likely
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diminish the recovery potential for
gartersnakes in these areas, and,
perhaps, even result in the local
extirpations of populations of northern
Mexican and narrow-headed
gartersnakes. Alternatively, subbasins
that are targeted for wholly native
species assemblages would likely secure
the persistence of northern Mexican and
narrow-headed gartersnakes that occur
there, if not result in their complete
recovery in these areas. Specific
subbasins where targeted fisheries
management is to occur were not
provided in AGFD (2012b), but
depending on which areas are chosen
for each management emphasis, the
potential for future conservation and
recovery of northern Mexican and
narrow-headed gartersnakes could
either be significantly bolstered, or
significantly hampered. Close
coordination with the AGFD on the
delineation of fisheries management
priorities in Arizona’s subbasins will be
instrumental to ensuring that
conservation and recovery of northern
Mexican and narrow-headed
gartersnakes can occur.
Conservation of these gartersnakes has
been implemented in the scientific and
management communities as well. The
AGFD recently produced identification
cards for distribution that provide
information to assist field professionals
with the identification of each of
Arizona’s five native gartersnake
species, as well as guidance on
submitting photographic vouchers for
university museum collections. Arizona
State University and the University of
Arizona now accept photographic
vouchers in lieu of physical specimens,
in their respective museum collections.
These measures appreciably reduce the
necessity for physical specimens (unless
discovered postmortem) for locality
voucher purposes and, therefore, further
reduce impacts to vulnerable
populations of northern Mexican or
narrow-headed gartersnakes.
Despite these collective conservation
efforts we have described above,
northern Mexican and narrow-headed
gartersnakes have continued to decline
throughout their ranges due to past,
current, and future threats that have not
been addressed through conservation
efforts.
Summary of Changes From the
Proposed Rule
Based on information provided during
the comment period by the general
public, tribes, states, and peer
reviewers, we updated the information
contained in the proposed rule for
incorporation into this final rule. In
addition, new references were obtained,
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evaluated, and discussed in the
deliberation of information in the final
rule that were either not available or not
obtained during the development of the
proposed rule. For clarity, we also
revised the language used in our
Findings for the listing rule and in the
background and regulatory language of
the 4(d) rule. However, no substantive
changes were made to either the
conclusion of the final listing rule or the
scope of the final 4(d) rule.
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Summary of Comments and
Recommendations
In the proposed rule published on
July 10, 2013 (78 FR 41500), we
requested that all interested parties
submit written comments on the
proposal by September 9, 2013. We also
contacted appropriate Federal, State,
and Tribal agencies, scientific experts
and organizations, and other interested
parties and invited them to comment on
the proposal. Newspaper notices
inviting general public comment were
published in the Verde Valley
Independent, Camp Verde Bugle,
Arizona Daily Star, and the Silver City
Sun News. We received a request for a
public hearing from the Hereford
Natural Resource Conservation District
who later withdrew their request.
Our summary responses to the
substantive comments we received on
the proposed listing rules and proposed
4(d) rule are provided below. Comments
simply providing support for or
opposition to the proposed rule, without
any supporting information, were not
considered to be substantive and we do
not provide a response.
Peer Reviewer Comments
In accordance with our peer review
policy published on July 1, 1994 (59 FR
34270), we solicited expert opinion
from eight knowledgeable individuals
with scientific expertise that included
familiarity with northern Mexican and
narrow-headed gartersnakes and their
habitat, biological needs, and threats.
We received responses from five of the
peer reviewers.
We reviewed all comments received
from the peer reviewers for substantive
issues and new information regarding
the listing of northern Mexican and
narrow-headed gartersnakes. All peer
reviewers shared the opinion that a
thorough examination of all available
information was conducted in support
of listing these gartersnakes. Peer
reviewers also commented that the
quality of the information presented in
the proposed rule was very high and the
analyses were thorough. There were
concerns expressed regarding whether
listing these gartersnakes as threatened
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would interfere with ongoing recovery
actions for listed fish species where they
co-occur. Another concern was based on
how threats affecting these gartersnakes
were prioritized in their scope and
magnitude in the proposed rule. In
general, peer reviewers generally
concurred with our methods and
conclusions and provided additional
information, clarifications, and
suggestions to improve the final rule.
Peer reviewer comments are addressed
in the following summary and
incorporated into the final rule as
appropriate.
Comment 1: The term ‘‘spiny-rayed
fish’’ has a very specific scientific
meaning, which is not consistent with
its use in the proposed rule. While this
group includes some of the nonnative
species of concern, such as sunfish and
bass, it does not include others,
specifically the catfishes. Also, the term
spiny-rayed fishes as used here excludes
a suite of nonnative fishes that are
problematic for native fish species and
likely for northern Mexican gartersnake
and narrow-headed gartersnake, such as
nonnative trouts (especially highly
predaceous brown trout (Salmo trutta),
red shiner (Cyprinella lutrensis), and
mosquitofish (Gambusia affinis)). The
term ‘‘spiny-rayed fishes’’ should either
be eliminated from the document and
replaced with accurate terminology or
be defined specifically for its intended
use in the rule. The Service should
dispense entirely with use of ‘‘spinyrayed fishes’’ and use only the term
‘‘nonnative fishes.’’
Our Response: In the proposed rule,
we intended to identify those species of
nonnative fish that were both
considered highly predatory on
gartersnakes and also highly
competitive with gartersnakes in terms
of common prey resources. The
nonnative fish species we view as most
harmful to gartersnake populations
include bass (Micropterus sp.), flathead
catfish (Pylodictis sp.), channel catfish
(Ictalurus sp.), sunfish, bullheads
(Ameiurus sp.), bluegill (Lepomis sp.),
crappie (Pomoxis sp.,) and brown trout
(Salmo trutta). We agree that all
nonnative fish species pose some level
of threat to native aquatic ecosystems.
However, it is important to highlight
those nonnative fish species that pose
the greatest threat to assist in
prioritizing future conservation actions
that are most beneficial to northern
Mexican and narrow-headed
gartersnakes. Therefore, we have
specifically defined in the beginning of
this final rule, what nonnative fish
species are considered ‘‘predatory’’ and
what nonnative species we consider
‘‘harmful.’’
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Comment 2: It would be helpful to the
reader to visualize the historical and
current ranges of the two snakes if range
maps were included.
Our Response: Current distribution
maps were provided and are available in
the proposed rule to designate critical
habitat for the northern Mexican and
narrow-headed gartersnake, which
accompanied the proposed rule to list
the species in the Federal Register (78
FR 41550, July 10, 2013, p. 41586).
Comment 3: The sentence ‘‘Fleharty
(1967, p. 227) reported narrow-headed
gartersnakes eating green sunfish, but
green sunfish is not considered a
suitable prey item’’ needs clarification.
Specifically, the authors need to provide
evidence that green sunfish is not a
suitable prey item. Just because green
sunfish has spines in their medial
(caudal excluded) and lateral fins does
not mean that it is not suitable prey.
Our Response: We added further
clarification to this text to support this
statement in the final rule under
‘‘Habitat and Natural History’’ for the
narrow-headed gartersnake.
Comment 4: Please provide examples
of ‘‘barriers to movement’’ of narrowheaded gartersnakes and additional
information on the ‘‘salvage efforts’’ in
the discussion leading into Table 2.
Our Response: We provided examples
and additional information in the text in
the final rule under ‘‘Current
Distribution and Population Status.’’
Comment 5: With respect to
nonnative fish species in the Gila River
basin, all were either intentionally or
accidentally introduced by humans;
there is no evidence that any species
gained access to the basin through
natural colonization as inferred in the
proposed rule.
Our Response: We agree that no
evidence exists to support unassisted
migration of nonnative fish species into
the Gila River basin from outside the
basin. However, we acknowledge that
harmful nonnatives, once introduced,
are fully capable of naturally dispersing
within the watershed where habitat
connectivity permits. This latter concept
was the impetus for the notion of
‘‘natural colonization’’, which is also
referred to as dispersal.
Comment 6: The proposed rule
mentions only trout of the genus Salmo
as occurring in habitat occupied by
either gartersnake. Rainbow trout
(Oncorynchus mykiss) and brook trout
(Salvelinus fontinalis) also occur.
Our Response: This oversight has
been corrected in the final rule in the
subsection ‘‘Fish’’ within the
subheading ‘‘Decline of the Gartersnake
Prey Base.’’
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Comment 7: The statements that
nonnative fish ‘‘tend to occupy the
middle and upper zones in the water
column’’ while native fish tend to occur
‘‘along the bottom’’ is not entirely
accurate. For example, all of the
catfishes (all of which are nonnative in
the Gila River system) are benthic in
habit, and these are among the species
considered harmful to gartersnakes and
their prey. Among native fishes in the
Gila River system only loach minnow
would be characterized as benthic,
although most native suckers and
minnows (chubs largely excluded) do
forage along surfaces, including the
bottom. Moreover, large numbers of
native fish, longfin dace (Agosia
chrysogaster) in particular, occur in
shallow habitats where differentiating a
position in the water column is
problematic.
Our Response: We have amended the
discussion in the subsection ‘‘Fish’’
within the subheading ‘‘Decline of the
Gartersnake Prey Base’’ in the final rule
to specify which groups of native or
nonnative fish are likely to occur where
in the water column.
Comment 8: It seems unlikely that
Yaqui catfish were suitable prey for
gartersnakes, given their stiff pectoral
and dorsal spines, and humpback chub
likely never co-occurred with either
gartersnake. Woundfin, conversely, has
records from the lower Salt River at
Tempe and would have been a listed
prey species.
Our Response: We have removed
humpback chub and Yaqui catfish, and
added woundfin, as species noted that
were possible prey species of either
gartersnake and that are now listed
under the Act.
Comment 9: Brown trout are highly
predacious and should be considered as
harmful nonnative wildlife by the
Service.
Our Response: We have reevaluated
potential effects of brown trout
predation on native aquatic vertebrates
and concur that brown trout are highly
predatory in all size classes and in a
wide range of water temperatures. Thus,
we have identified the brown trout as a
‘‘predatory’’ nonnative fish species and
discuss its ecological significance in the
final rule in the subsection ‘‘Fish’’
within the subheading ‘‘Decline of the
Gartersnake Prey Base.’’
Comment 10: In the proposed rule,
the Service identified several streams in
Arizona or New Mexico where
nonnative fish present management
issues. However, nonnative fish are a
concern for management of native fish
throughout Arizona and New Mexico,
not only those streams specifically
mentioned. They are an issue where
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they already are present and in those
habitats where they may invade or be
introduced in the future, which
included virtually any watercourse or
body of water throughout the region.
Our Response: We added language to
reflect this fact in the subsection ‘‘Fish’’
within the subheading ‘‘Decline of the
Gartersnake Prey Base.’’
Comment 11: With respect to
potential effects from fisheries
management activities, it would appear
that gartersnakes still occur in many of
the streams that have received piscicide
treatments. If so, why are these streams
and their renovation history discussed
in the proposed rule because there is no
evidence that chemical treatment in any
of these instances eliminated, depleted,
or otherwise impacted a resident
gartersnake population. The loss of a
major portion, or entire, prey base of a
gartersnake population will result in the
loss of individuals from starvation,
which is expected to result in weakened
population viability and, potentially,
the loss of that population depending on
the presence of other stressors, the
proximity of the next-closest source
population, and the status of the
population prior to treatment.
Our Response: If the intent of a
renovation is to remove all fish from a
stream, and the stream is occupied by
either gartersnake, which wholly or
partially requires fish in their prey base,
the logical conclusion is that adverse
effects to gartersnakes, at least
temporarily, are likely under these
circumstances. The presence of either
gartersnake in a treated stream after the
treatment is not evidence that no
adverse effects to individuals have
occurred.
Comment 12: Traditionally, pretreatment salvage and post-treatment
restocking favor larger-bodied size
classes of native fish, which could
reproduce and provide smaller prey for
gartersnakes over a period of time.
Small-bodied species would also be
saved for salvage and restocking, but are
more difficult to find. How are the
interests of the gartersnakes rectified in
these situations? Alternatively,
gartersnakes themselves could be
salvaged and restocked at a later date
after a prey base has been established.
Our Response: We agree that fish
salvage operations, prior to treatment,
are likely to favor larger individuals that
may exceed the size classes most
preferred by gartersnakes as prey. For
this reason, we intend to explore
partnerships and opportunities for
raising native fish of appropriate size
classes in hatchery settings for
subsequent release into treated streams,
post treatment. Based upon our
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evaluation of the literature and
cooperative work with gartersnakes,
alternative prey species and appropriate
size classes are well-understood. We are
not, however, aware of any studies that
focused on how long a gartersnake
could go without food before
physiological stress or starvation. We do
know that, compared to snakes within
other genera or families, gartersnakes
have a relatively fast metabolism and
are active foragers, implying that
physiological stress or starvation may be
more of a concern in the absence of
prey.
There are significant challenges with
salvaging gartersnakes for long-term
captivity. First, facilities with the space,
equipment, and knowledge to care for
larger numbers of gartersnakes for long
periods of time are very few, and
currently those that are capable, are
nearly at full capacity because of their
involvement with captive breeding
efforts. Second, narrow-headed
gartersnakes have proven to be difficult
to maintain in captivity due to their
unique physiological and prey
requirements. Lastly, it may prove
difficult if not impossible to salvage
gartersnakes from low-density
populations within complex habitat and
therefore the risk of their complete
extirpation from a renovation activity is
elevated. In the event an isolated
population is extirpated, the risk of
forever losing their unique genetic
lineage is also elevated and
unacceptable.
Comment 13: The discussion about
electrofishing impacts to gartersnakes is
misleading and misinformed. The
statement that ‘‘gartersnakes present
within the water are often temporarily
paralyzed from electrical impulses
intended for fish’’ is true only to the
extent that the gartersnake actually is
present and available to intercept the
electrical current. Personal experience
and interviews with colleagues suggest
that encounters of electroshockers and
gartersnakes are exceptionally rare, not
‘‘often’’ as suggested by the Service.
Next, use of the term ‘‘electrocution’’ is
inappropriate as it by definition means
killing, which is not only rare for
electroshocked fishes, but unknown for
gartersnakes.
Our Response: The statement in the
proposed rule, ‘‘gartersnakes present
within the water are often temporarily
paralyzed from electrical impulses
intended for fish’’ was intended to mean
that gartersnakes had to be present in
the water and within the affected radius
of the electroshocker, otherwise the
assumption is they would not be
affected and thus, not detected. By use
of the term ‘‘electrocuted,’’ it was not
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our intention to imply that gartersnakes
which received an electrical charge
were mortally wounded. We have
removed the use of this term from the
final rule. ‘‘Detections’’ as cited in the
document are not ‘‘electrocutions.’’
Reports of gartersnakes detected during
electrofishing may be misleading
because it is unclear if those attributed
to Hellekson (2012, pers. comm.) were
during surveys for fishes or for reptiles
and amphibians, while detections
reported by Pettinger and Yori (2011)
apparently were during surveys for
Chiricahua leopard frog and not for
fishes. Lastly, the references cited where
gartersnakes were detected via
electroshocking referred to fisheries
surveys; electroshocking is not a
recognized method for aquatic
herpetofauna surveys. We amended the
text in this final rule under the heading
‘‘Risks to Gartersnakes from Fisheries
Management Activities,’’ subheading
‘‘Mechanical Methods’’ to better
communicate our assessment of the
potential effect of electrofishing surveys
on gartersnakes.
Comment 14: The term ‘‘self-baiting’’
is rarely if ever used by fisheries
professionals in reference to wire
minnow traps.
Our Response: We used the term
‘‘self-baiting’’ with respect to how these
types of mechanical traps work for
gartersnake surveys, which is indeed
through the function of self-baiting with
minnows, amphibian larvae, etc.
However, the term’s use in discussing
the use of these traps for fisheries
surveys was inaccurate, and the term
has been removed from the sentence
where it was used in the proposed rule.
Comment 15: The proposed rule
provides two references documenting
examples of gartersnakes that drowned
in wire minnow traps. One reported
from Holycross et al. (2006) and the
other from Boyarski (2011). Holycross et
al. (2006) never mentions the word
‘‘drown’’ in their report. It is also noted
that these few minnow-trap related
fatalities occurred during surveys
specifically to capture gartersnakes, that
is, the investigators were targeting
gartersnakes with this effort. The
inadvertent capture of a gartersnake is
an exceptionally rare occurrence and
has not been reported from fisheries
survey activities.
Our Response: The reference of
Holycross et al. (2006) describes the
flooding event, but not the death of an
individual gartersnake, which was
incidentally killed in a trap when
flooding occurred (observed by Service
biologists). We discuss the potential
threat of gartersnake fatality from
minnow traps used in fishery surveys
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because the threat is real. Gartersnakes
will forage at any position within the
water column; northern Mexican
gartersnakes often forage at the water
surface and in intermediate depths,
while the narrow-headed gartersnake
forages most frequently along the
bottom. The fact that minnow traps for
fishery surveys are generally set
overnight and checked at least twice
daily, and always during morning does
not alleviate this threat. The reason that
minnow traps used for gartersnake
surveys are set at the surface with half
of the trap above the water line is to
prevent drowning of captured
gartersnakes. When used for fisheries
purposes, these traps incidentally selfbait with gartersnake prey species (the
intended purpose is to capture fish) and
are set below the water line. Checking
the traps a few times daily will not
prevent air-breathing, nontarget
organisms from drowning if captured.
We also note that both gartersnake
species can be active at night, but are
not certain their activity includes
foraging. We did not intend to portray
that the incidental capture of
gartersnakes by minnow-trapping for
fishery surveys happens frequently, but
where it could incidentally result in the
loss of one or more reproductive females
in low population densities, a
population-level effect could result.
Lastly, we clarified in the final rule that
funnel traps are not used in fishery
surveys.
Comment 16: Relative to fisheries
management activities, it cannot be
stressed enough that there currently is
no effective strategy to eliminate
harmful nonnative fishes other than use
of piscicides and their use is critical for
native fish recovery. It should also be
noted that fisheries activities effects are
trivial compared to those attributed to
herpetological activities and other
human factors.
Our Response: We concur that
chemical renovations are vital to native
fish recovery. To further clarify the vital
importance of piscicide use in the
recovery of the gartersnakes’ native prey
base and the gartersnakes themselves,
we amended the passage in the final
rule under the heading ‘‘Risks to
Gartersnakes from Fisheries
Management Activities,’’ subheading
‘‘Piscicides.’’
We are confident that the discussion
in the proposed and final rules
attributed to the potential threats to
these gartersnakes from the
implementation of fishery management
activities is objective, thoroughly
referenced, and balanced. We agree that
other human-caused threats can pose
comparably greater risks to gartersnakes.
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But, we disagree with the notion that
incidental fatality from herpetological
surveys are potentially more significant
than activities that eliminate an entire
suite of prey species from habitat
occupied by gartersnakes. We also stress
that listing these two gartersnakes
should not be construed as an obstacle
to native fish recovery under any
circumstances. Rather, the recovery of
these gartersnakes is inextricably and
ecologically linked to native fish
recovery.
Comment 17: How many stock tanks
are known within the range of northern
Mexican gartersnake and what
proportion of these meet criteria for
being ‘‘well-managed?’’ Few stock tanks
are well-managed, and most lack
peripheral vegetation that would
function as suitable habitat for
gartersnakes. The Service provides no
information to address these questions,
which is necessary to evaluate the
actual or potential contribution of stock
tanks to gartersnake conservation.
Our Response: The actual number of
stock tanks that occur within the
distribution of the northern Mexican
gartersnake is not currently known
because not all tanks are georeferenced
in GIS databases. However, based upon
their common occurrence on the
landscape, we conclude that the number
is very large, possibly in the 100’s. We
also have no quantitative data on the
number of tanks that are ‘‘wellmanaged.’’ Regardless, based upon our
collective knowledge of how these
habitats are used by northern Mexican
gartersnakes and primary prey species,
particularly in southern Arizona, we
consider their existence as a vital
contribution to conservation of the
northern Mexican gartersnake. Based on
our knowledge of habitat variables that
best predict whether a gartersnake
population could be sustained, the
presence of a native prey community
and the absence of harmful nonnative
species appear to be the most predictive
factors. Peripheral vegetation may
provide cover for gartersnakes in stock
tanks where harmful nonnatives occur,
but it is not necessary for gartersnake
populations in all circumstances. It may
be possible that stock tanks have
replaced, in part, the role of natural
cienegas as important gartersnake
habitat, although no direct study has
been attributed to this hypothesis.
While stock tanks in different drainages
can be invaded by bullfrogs or crayfish
by means of natural dispersal, they can
also represent easily managed habitat to
protect against (or rectify) invasion of
harmful nonnative species. For these
reasons, we currently value the
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existence of stock tanks for northern
Mexican gartersnake conservation.
Comment 18: Mine spills are a threat
to gartersnakes and to their fish prey.
For example, mine spills made the San
Pedro River toxic for a time, and a
naturally occurring population of
endangered Gila topminnow in Cocio
Wash, Arizona, was exterminated by a
mine spill. Numerous other examples of
this threat are available and should be
included.
Our Response: We expanded our
discussion of the threat of mining
pollution under the heading
‘‘Environmental Contaminants,’’ to
include the example from the San Pedro
River.
Comment 19: Regarding the
discussion about management emphasis
relative to native and nonnative fishes,
it should be acknowledged that, at least
in Arizona, the management priority is
recreational fisheries, and the operative
AGFD’s policy is ‘‘no net loss’’ of sport
fishing opportunities when attempting
to balance sport fish and native fish
management. It is well documented by
literature cited in the proposed rule that
native fishes and nonnative fishes
cannot coexist in the long term other
than under exceptional circumstances.
Our Response: We understand the
concern for the future of native fish and
by extension, northern Mexican and
narrow-headed gartersnakes. We
included discussion of the ‘‘no net loss’’
policy in the final rule under the
heading ‘‘Current Conservation of
Northern Mexican and Narrow-headed
Gartersnakes.’’
Comment 20: The Service used the
presence of a native prey species as
evidence that a given area or stream may
be occupied by northern Mexican
gartersnakes. This approach seems
optimistic at best, and perhaps, when
the importance of habitat is also
considered, not scientifically justified. If
native prey species are present, but the
habitat extent is too small, it is possible
that northern Mexican gartersnakes did
not occur or will not persist.
Our Response: In determining
whether historically occupied habitat
remains occupied, we considered
habitat surrogates in the determination
where gartersnake survey data was
limited. Native prey species remain an
important attribute for northern
Mexican gartersnake habitat and their
presence in an area is evidence that the
resident, native biotic community may
still offer native prey. It is also
reasonable to assume that not every site
along a stream course is suitable habitat
for northern Mexican gartersnakes; these
sites may be occupied by dispersing
individuals, however. We think that
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using these habitat parameters as
surrogates for occupied areas by the
northern Mexican gartersnake is an
appropriate use of the best available
information, in the absence of more
detailed information.
Comment 21: We have recently
surveyed and trapped Little Ash Creek
(August 2013); it has abundant
nonnative fish species and crayfish,
scarce native dace populations, and very
few (n = 1 captured) bullfrogs. The
habitat extent (creek size) is small and
we suspect it no longer supports
northern Mexican gartersnakes so the
population is likely extirpated.
Our Response: We appreciate the
updated information. However, the
continued presence of some native fish
and limited bullfrog detections are signs
that northern Mexican gartersnakes
could still exist, albeit at low or very
low abundance, in Little Ash Creek.
Moreover, individual gartersnakes could
disperse from the Agua Fria River, to
which Little Ash Creek is a tributary.
We have not yet officially adopted a
protocol to establish population
extirpation, but at a minimum, we
expect such a protocol should include
robust survey data from multiple
consecutive years to account for
detectability constraints in low-density
populations. Until such a protocol is
adopted, we hesitate to conclude that
gartersnakes are extirpated from a given
area, such as Little Ash Creek.
Comment 22: Additional sites not
encompassed by Table 1 include:
Tavasci Marsh (Nowak et al. 2011;
population possibly not viable but likely
supported by recruitment from the
Verde River); Peck’s Lake (Schmidt et
al. 2005; population possibly not viable
but likely supported by recruitment
from the Verde River), and Dead Horse
Ranch State Park (Emmons and Nowak
2013; population likely viable).
Our Response: We are aware of these
populations and included them with the
Verde River mainstem due to their close
proximity.
Comment 23: The proposed rule cites
Rosen and Schwalbe (1988, pp. 34–35)
for a list of plant species associations for
narrow-headed gartersnake habitat.
Reliance on a single citation (whose
results were based on visual encounter
surveys) to infer distribution-wide
habitat use is inappropriate. Please
include intensive study data from
Nowak and Santana-Bendix (2002) and
Nowak (2006) for a more complete look
at narrow-headed gartersnake–plant
associations.
Our Response: Rosen and Schwalbe
(1988, entire) sampled narrow-headed
gartersnake populations in a multitude
of streams across their range in Arizona
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and, therefore, represent a more
comprehensive list of plant species
associations in a rangewide context.
Nowak and Santana-Bendix (2002) and
Nowak (2006) focus solely on one
population at Oak Creek and, therefore,
do not account for variability of
preferred habitat across the species’
range.
Comment 24: The Service stated that
sexual maturity in narrow-headed
gartersnakes occurs at 2.5 years of age in
males and at 2 years of age in females
(Deganhardt et al. 1996, p. 328). I
suspect this assertion is overstated and
scientifically inaccurate, based on field
studies and on animals currently
maintained in captivity. Captive-born
female narrow-headed gartersnakes from
the Black River (Arizona) maintained in
captivity did not lay eggs until their
third summer, even though they reached
adult size within their second year
(Nowak, unpublished data, 2012).
Our Response: In the absence of other
published data, we will continue to rely
on published information regarding the
sexual maturity data presented and
referenced. In addition, observations
made in captive situations may be
misleading because they may not reflect
factors affecting wild populations.
Comment 25: The proposed rule
provided a list of areas where narrowheaded gartersnakes could be reliably
found. The Upper Verde River, Tonto
Creek, and the Blue River should also be
included in this list. While occurring in
low densities, individuals in these
populations can still be reliably found
with minimal to moderate effort (e.g.,
Upper Verde River: Emmons and Nowak
2012a, Emmons and Nowak 2013; Tonto
Creek: Madara-Yagla 2010, 2011; and
Blue River: Rosen and Nowak unpubl.
data, 2012).
Our Response: The population and
survey data reported in Appendix A
provide the basis for where narrowheaded gartersnakes are reliably found.
Populations considered likely viable
have received significantly more field
study in most cases and, where they
haven’t, recent survey data show robust
population densities with minimal
survey effort. We understand the
inherent challenges with defining a
population’s status with a single phrase
or term, but the data do not currently
show that narrow-headed gartersnake
populations in the Upper Verde, Tonto
Creek, or the Blue River are near as
robust as those identified as likely
viable in Table 2. In the case of Tonto
Creek, narrow-headed gartersnake
records are comparably few, and
Madara-Yagla (2010, 2011) address only
northern Mexican gartersnakes.
Unpublished data from the Blue River
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were not provided to us, and until those
data are provided and reviewed, we are
unable to update the status of that
population, if warranted.
Comment 26: If only 8 to 10 percent
of historic populations are viable, with
significant post-fire concerns for
populations from Whitewater Creek and
the Black River, should this species be
proposed for listing as ‘‘Endangered?’’
Our Response: The current status of
the northern Mexican and narrowheaded gartersnakes meets the
definition of threatened, not
endangered. We found that both
gartersnakes are not currently in danger
of extinction because they remain extant
in most of the subbasins where they
historically occurred, and known threats
have not yet resulted in substantial
range reduction or substantial number
of population extirpations to put either
species on the brink of extinction.
However, we do find that the ongoing
effects of the threats make both species
likely to become endangered in the
foreseeable future. Please see the
sections entitled ‘‘Determination for
Northern Mexican Gartersnakes’’ and
‘‘Determination for Narrow-headed
Gartersnakes’’ for further discussion of
our determinations.
Comment 27: Regarding Table 2, state
that the population at Saliz Creek, New
Mexico is introduced; three recaptured
individuals were found there in 2013;
however, the population is likely not
viable. In addition, I do not know of any
post 1990’s records from the San
Francisco River in New Mexico; this
population is ‘‘likely extirpated’’
(Hibbitts et al. 2009).
Our Response: Saliz Creek is a
tributary to the San Francisco River. The
San Francisco River formerly had a
robust population of narrow-headed
gartersnakes. Saliz Creek lies between
two additional tributaries to the San
Francisco River, Whitewater Creek and
the Tularosa River, which historically
and currently (respectively) also had
robust populations. Saliz Creek also
boasts a largely native fish community,
with the exception of its lower-most
reach. Furthermore, prior to 2012, a
total of 10 person-search hours were
spent surveying for narrow-headed
gartersnakes attributed to Saliz Creek,
which does not constitute adequate
survey effort to determine presence or
absence. No compelling data suggest
that narrow-headed gartersnakes never
historically occurred in Saliz Creek
prior to their release in 2012. Regarding
population status in the San Francisco
River, more recent survey efforts from
2009–2011, consisting of approximately
100 person-search hours, reconfirmed
the narrow-headed gartersnake as extant
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in the San Francisco River in New
Mexico with documentation of three
narrow-headed gartersnakes (Hellekson
2012a, pers. comm.). Therefore, we treat
this population as likely not viable
rather than likely extirpated.
Comment 28: The statement attributed
to Rosen et al. (2001, p. 22) that the
presence and expansion of nonnative
predators is the primary cause of
decline in northern Mexican
gartersnakes and their prey in
southeastern Arizona may not have been
properly characterized. This paper does
not state that nonnative predators are
the only factor, but instead it explicitly
states the importance of other factors
such as climate and interspecific
competition. Also, the paper’s
conclusions are subjective and are
generally presented as testable
hypotheses, and should be cited with
caution rather than presented as
scientifically tested facts.
Our Response: We agree that Rosen
(2001) did not state that nonnative
species are the only reason for northern
Mexican gartersnake declines in
southern Arizona, rather harmful
nonnatives were considered as the
primary cause at most sites surveyed, as
described in the proposed rule. Rosen
(2001, p. 21) postulated that ‘‘natural
climatic fluctuation’’ may be
responsible for a northern Mexican
population decline at one site in
southern Arizona, which is not to say
that it was regarded in equal value as
harmful nonnative species in affecting
northern Mexican gartersnakes in
southern Arizona. Interspecific
competition was also discussed in
Rosen (2001) as a cause for concern at
some sites. We evaluated the role of
climate change and interspecific
competition in other sections of the
proposed and final rules as their
discussion is not appropriately placed
in the section referred to here. However,
we changed the word ‘‘concluded’’ in
this sentence to ‘‘hypothesized.’’
Comment 29: The proposed rule
discusses the importance of a varied
prey base and cites a study that
experimented with food deprivation on
the common gartersnake (T. sirtalis).
There is no scientifically valid reason to
conclude that a varied diet could not
include bullfrogs as a replacement for
native leopard frogs, especially where
bullfrogs are currently abundant. It may
not be scientifically valid to infer that
foraging, physiological, and behavioral
data collected from the common
gartersnakes will be representative of
the populations of southwestern
gartersnakes. As such, I disagree that the
common gartersnake is an ‘‘ecologically
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similar species’’ to northern Mexican
gartersnake.
Our Response: We state on several
occasions in the proposed rule that
larval and sub-adult bullfrogs are eaten
by northern Mexican gartersnakes in the
mid- to larger-size classes. However,
bullfrogs are not always available for
gartersnake populations that exist where
native ranid frogs have disappeared, and
bullfrogs pose a significant threat to
population recruitment of northern
Mexican gartersnakes in many areas.
This impact outweighs any benefit of
their existence as a source of prey. We
consider relevant data from the common
gartersnake as valid for a general biology
discussion as both species have a varied
prey base and both species occupy
varied habitats, albeit the northern
Mexican gartersnake may be more
aquatic.
Comment 30: In the discussion of the
role of harmful nonnative species
relative to other threats implicated in
the decline of native fisheries, the
proposed rule stated, ‘‘Aquatic habitat
destruction and modification is often
considered a leading cause for the
decline in native fish in the
southwestern United States. However,
Marsh and Pacey (2005, p. 60) predict
that despite the significant physical
alteration of aquatic habitat in the
southwest, native fish species could not
only complete all of their life functions
but could flourish in these altered
environments, but for the presence of
(harmful) nonnative fish species, as
supported by a ‘substantial and growing
body of evidence derived from case
studies.’’
I would like to see a more robust
consideration, including citations
beyond March and Pacey (2005), of the
importance of the loss of habitat in
native fish declines relative to harmful
nonnative species. It is my
understanding that many species of
native fish rely on seasonal flooding to
induce spawning.
Our Response: We agree that the role
of a natural flood regime is extremely
important to the maintenance of native
fish populations as well as important in
(temporarily) depressing resident
harmful nonnative fish populations, and
the proposed rule provides a thorough
review of this topic, citing numerous
references. Natural flood regimes have
largely disappeared from several large
perennial mainstem rivers and from a
small number of streams associated with
small reservoirs in Arizona and New
Mexico. However, many native fish are
doing markedly poorly across their
ranges where they co-occur with
harmful nonnative fish species,
regardless of whether a natural flood
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regime exists or not. No other threat is
as geographically ubiquitous as that
from harmful nonnative species, which
is clearly reflected, in robust fashion,
within the published literature. The
proposed and final rules review how
threats to aquatic habitat that are not
directly associated with nonnative
species have also resulted, in part, in
the decline of numerous native fish
species in the United States and Mexico.
Based on our consultations with native
fish experts in private and public
sectors and the breadth of available
literature, the findings of Marsh and
Pacey (2005) are consistent on the scope
and magnitude of the effect of harmful
nonnative fish on the decline of native
fish species.
Comment 31: In the discussion of the
effects of bullfrogs on gartersnake
populations, the proposed rule states
that bullfrogs may lower recruitment
and lead to population declines of
northern Mexican gartersnake
populations. This is an overgeneralization and is not supported by
scientific data across the range of the
species. In addition, the conclusion that
bullfrogs more effectively prey on young
age classes is likely true but has not
been substantiated by experimental
studies. This statement does not
accurately reflect the situation in the
Verde Valley (AZ), where all age classes
of northern Mexican gartersnakes are
well-documented to co-occur with
bullfrogs. Low recruitment could be due
to a number of factors other than
nonnative species predation.
Our Response: The scientific
community is in consensus, and we
agree, that bullfrogs negatively affect
recruitment of northern Mexican
gartersnakes in areas where gartersnakes
occur with bullfrogs in high densities.
The presence of other harmful
nonnatives or other possible threats can
confound our understanding of the
specific effects of bullfrogs, and we
presented an extensive discussion of
this issue citing numerous scientific
references. We believe our treatment of
the ecological effects of bullfrogs on
northern Mexican gartersnakes is well
supported by the best available
scientific information. It is true that
published examples of this concern
come from gartersnake populations in
southern Arizona, and we agree that any
gartersnake population could face a
unique array of potential threats that
could also effect successful recruitment
across its distribution.
Comment 32: Given that northern
Mexican gartersnakes have been
documented to prey on bullfrogs in
multiple locations, it is misleading and
scientifically inaccurate to imply that
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the recovery of northern Mexican
gartersnakes is dependent on recovery
of native leopard frogs.
Our Response: We agree that bullfrogs
in their larval and subadult age classes
can be prey for northern Mexican
gartersnakes and, in some populations,
may be their primary prey items.
However, unlike native leopard frogs,
bullfrogs in their adult age class become
a significant threat to resident northern
Mexican gartersnake populations and
can depress or eliminate recruitment of
young snakes into the reproductive age
classes within a population. Adult
bullfrogs can extirpate a population of
northern Mexican gartersnakes by
directly preying upon snakes and outcompeting them for available prey.
Bullfrogs can also prevent the
recolonization of an area by dispersing
gartersnakes via these same ecological
mechanisms. The view that bullfrogs are
an adequate substitute for native
leopard frogs in the ecosystems of the
northern Mexican gartersnake is not
supported by the best available
scientific information and, therefore, we
do not support this supposition.
Comment 33: Regarding the incidence
of tail injuries in gartersnake
populations, observations of this
phenomenon in upper Oak Creek,
Arizona, at sites where crayfish and
bullfrogs are absent, seem to point to
fish or bird predation attempts, given
wide oval injury marks with pointed
ends.
Our Response: We noted in the final
rule under the heading ‘‘The Effects of
Predation-Related Injuries to
Gartersnakes’’ that tail injuries could be
caused by other predators other than
strictly bullfrogs or crayfish.
Comment 34: A more quantitative
evaluation on habitat loss to dewatering
would be worth sharing, assuming any
is available. Extensive dry reaches in the
San Francisco River now exist,
including locations that have historic
records for the narrow-headed
gartersnake.
Our Response: We agree that a
quantitative evaluation of dewatered
stream habitat would be important to
fully characterize this threat. However,
we were unable to locate georeferenced
data to assist in this effort and had to
rely on existing literature to describe
this threat.
Comment 35: The adverse effects of
crayfish on narrow-headed gartersnakes
may be overstated, at least with respect
to New Mexico. A clear connection
between crayfish presence and
declining narrow-headed gartersnake
populations has yet to be definitely
made in field study. The two sites with
the highest apparent densities of
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narrow-headed gartersnakes in New
Mexico also have fairly abundant
crayfish and bullfrogs. When small- to
medium-sized native fish are abundant,
crayfish seem to be tolerated by the
gartersnakes. In New Mexico very few
sites have crayfish that can reach sizes
where they would be a potential
predator on narrow-headed
gartersnakes; in virtually all other sites,
the crayfish are uniformly small in size
due to periodic years with flooding that
extirpates them or drastically lowers
their numbers.
Our Response: We added discussion
under ‘‘Effects of Crayfish on Native
Aquatic Communities’’ to reflect
extraneous influences on the threat of
crayfish to gartersnake populations
while noting that the available literature
strongly suggests that crayfish in larger
size classes or in high densities are
cause for significant concern for
gartersnakes and their prey species,
especially with other threats
simultaneously affecting gartersnake
populations.
Comment 36: The Middle Fork Gila
River, Little Creek, and South Fork
Negrito Creek populations of narrowheaded gartersnakes were identified as
likely having been impacted by the 2012
Whitewater-Baldy Complex fire and
considered as not likely viable. Post-fire
condition data were largely not
available in 2012, but information from
2013 indicated that fish populations
were showing signs of recovery.
Our Response: Based on the
potentially significant effects of wildfire
on fish populations and, therefore, on
the narrow-headed gartersnake (detailed
in the proposed and final rules), we
conservatively assessed these narrowheaded gartersnake populations as
likely not viable, given the size and
scope of the Whitewater-Baldy Complex
Fire. We were also involved with
narrow-headed gartersnake salvage
operations from the Middle Fork Gila
River, strictly because it was assessed to
have been heavily impacted by wildfire.
We treat Appendix A as a ‘‘living’’
document and can update the status of
gartersnake populations as necessary
and as population data become
available, for sharing and conservation
and recovery planning purposes.
Comment 37: Narrow-headed
gartersnakes in the mainstem San
Francisco River are reliably detected,
and the population should be
considered as likely viable.
Our Response: Gartersnake captures
per unit effort have significantly
declined in the San Francisco River
since they first became regularly
monitored in the 1980’s. While
individuals are still detected,
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population data we present in Appendix
A clearly describe the narrow-headed
gartersnake population in the San
Francisco River as one in significant
decline.
Federal Agency Comments
Comment 38: The proposed rule
references the Management Indicator
Species, Regional Foresters’ Sensitive
Species List, and land management
decisions, but states that there are no
specific protective measures conveyed
to these species. However, the northern
Mexican and the narrow-headed
gartersnakes have been considered
sensitive species on the Regional
Forester’s sensitive species list for a
long time. An impact to these species is,
therefore, considered as part of the
environmental analysis for every forest
management action. The USFS Sensitive
Species Policy is to manage for viable
populations of these species. Further,
the USFS policy for sensitive species
provides protective measures such as
direction to ‘‘Avoid or minimize
impacts to species whose viability has
been identified as a concern’’ (Forest
Service Manual (FSM) 2670.32 #3). A
decision that would impact sensitive
species ‘‘. . . must not result in loss of
species viability or create significant
trends toward Federal listing’’ (FSM
2670.32 #4).
Our Response: We more accurately
summarized what protections are
afforded to ‘‘sensitive species’’ in the
final rule. We found no examples
(although we did not have the
opportunity to review all previous
planning documents the USFS has
developed in the past), and we were not
provided any examples of measures that
have been implemented by the USFS to
‘‘avoid or minimize impacts’’ to either
the northern Mexican or narrow-headed
gartersnake. We look forward to working
with the USFS in developing such
measures.
Comment 39: What is the basis for
assuming there is ‘‘continued anxiety’’
from the public regarding rotenone use?
Our Response: We have been an
active participant in the public debate
over potential threats to human health
from rotenone use. The new and very
process-rich procedures now in place
for planning and implementing
rotenone use in Arizona are testament
that piscicide use in the recovery of rare
and listed fish is still considered
controversial; although it is
scientifically well-supported that there
is no public harm from its use.
Comment 40: We disagree that, on the
Gila National Forest, heavy recreation
use within occupied narrow-headed
gartersnake habitat is thought to impact
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populations along the Middle Fork Gila
River, mainstem Gila River between
Cliff Dwellings and Little Creek, and
Whitewater Creek from Catwalk to
Glenwood. Recreation use along the
Middle Fork Gila River is certainly not
heavy; most use is by hikers and
backpackers utilizing the existing trail
to access the Gila Wilderness. The
stream between the Cliff Dwellings and
Little Creek is the West Fork Gila River
not the mainstem. This reach of stream
is located on National Park Service,
NMDGF, and USFS lands. The majority
of this reach is on the NMDGF’s Heart
Bar Wildlife Area. Whitewater Creek
from the Catwalk to Glenwood is
predominately private property.
Approximately 0.25 mile of stream,
downstream of the Catwalk, is USFS
lands and the remainder of this reach is
private property.
Our Response: We amended this
discussion in the final rule to state that
much of the recreation use in these
areas is related to hiking and
backpacking, which are generally not
considered a threat to gartersnakes
outside of the fact that increased human
visitation leads to more gartersnake
encounters and potentially more killing
of gartersnakes where the foot trail is
near the canyon bottom.
Comment 41: Throughout the
proposed rule and during personal
communications with the Service,
livestock grazing has not been identified
as a significant threat to these species.
However, the Service appears to be
saying that, unless livestock are
excluded by fencing, adverse effects
may occur. The Service goes further by
stating that the adverse effects of
livestock are somehow most likely to
occur when nonnative species are
present but that the species are resilient
to these disturbances if nonnatives are
absent. So, grazing along a stream
adversely affects the species if
nonnatives are present but does not
have these same impacts if nonnatives
are absent?
Our Response: We continue to believe
that livestock grazing is largely
compatible with northern Mexican and
narrow-headed gartersnakes based on
the species’ apparent resiliency to
perturbations to their physical habitat,
depending on the resident aquatic
community. In our literature review and
field experience, we found populations
of these gartersnakes to be resilient to
activities that affect their physical
habitat (vegetation abundance,
structure, composition) when harmful
nonnative species are absent or at low
levels that allow for effective
recruitment of snakes in the population.
When recruitment of gartersnakes
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within a population is hampered by
harmful nonnatives, this resiliency is
diminished and the presence of
adequate vegetation cover for protection
against these nonnatives becomes more
important. When Federal actions are
planned, all aspects of project
evaluations should consider potential
effects to whatever prey base the
gartersnake population is using in a
given area. This idea should be the
logical ‘‘framework’’ used in developing
projects in gartersnake habitat to
manage aggressively against harmful
nonnatives to improve population
resiliency and recruitment of
gartersnakes. We also note that ‘‘adverse
effects’’ can have varying degrees of
magnitude and scope and that, through
section 7 of the Act, most activities that
could adversely affect species include
measures to reduce effects and potential
for take though the issuance of an
incidental take permit.
Comment 42: While nonnative, spinyrayed fish such as green sunfish and
smallmouth bass were common in the
lower reach of Turkey Creek near its
confluence with the mainstem Gila
River prior to the Dry Lakes Fire, they
did not make up the majority of the fish
community. More upstream reaches
were occupied by native fishes
including Gila chub, speckled dace,
Sonora and desert suckers, and longfin
dace along with Gila X Rainbow trout
hybrids. All of the native species
survived the fire runoff events, and,
although populations were depressed
for some time, they had recovered well
until recent fires.
Our Response: We amended this
discussion in the final rule to more
accurately describe the fish community
and effects of wildfire on Turkey Creek.
Comment 43: We disagree that
significant threats to these gartersnakes,
such as those related to nonnative
species, are not addressed on USFS
lands. The role of the USFS is to manage
land, addressing the needs of species’
habitat. Management actions related to
nonnative fish and aquatic species
stocking, control, or eradication is under
direction of the State. Collaborative
efforts are occurring on USFS lands to
improve species’ habitat through
construction of fish barriers and stream
chemical renovations.
Our Response: We acknowledge the
proactive measures taken by the USFS
to assist in restoring fish communities to
wholly native assemblages.
Comment 44: The proposed rule states
that USFS management policies of the
past favored fire suppression. However,
new policies have allowed for managing
wildfires that have a resource benefit, as
well as prescribed fire. The Guidance
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for Implementation of Federal Wildland
Fire Management Policy is the
Department of Agriculture’s single
cohesive Federal fire policy. This policy
contributes to landscape restoration,
controls invasive species, reduces
uncharacteristic wildfire across the
broader landscape, and improves the
resiliency of these potential natural
vegetation types to adapt to climate
change.
Our Response: We have updated this
discussion under the heading, ‘‘HighIntensity Wildfires and Sedimentation
of Aquatic Habitat’’ in the final rule to
include reference to the updated fire
policy and what it hopes to achieve in
the mid to long term.
Comment 45: The proposed rule states
that the 2011 Wallow Fire impacted 97
percent of perennial streams in the
Black River subbasin and 70 percent of
perennial streams in the Gila River
subbasin. We request the Service clarify
how they are defining a subbasin.
Typically, a subbasin is a fourth code
Hydrologic Unit. We do not consider the
Wallow Fire to have affected any of the
Gila River subbasins in New Mexico.
Our Response: We use the term
subbasin in a general sense as a stream
basin within a larger stream basin. We
further defined the area impacted by the
2011 Wallow Fire as within ApacheSitgreaves National Forest, White
Mountain Apache Indian Tribe, and San
Carlos Apache Indian Reservation lands
in Apache, Navajo, Graham, and
Greenlee counties in Arizona, as well as
Catron County, New Mexico. We
recommend the review of InciWeb
(2011), Meyer (2011; p. 3, Table 1), and
Coleman (2011, pp. 2–3) for information
on the effects of the 2011 Wallow Fire.
Comment 46: On the ApacheSitgreaves National Forest forested
vegetation types, historic fire-return
intervals varied from frequent, lowintensity surface fires in ponderosa pine
types (every 2–17 years), to mixedseverity fires in wet mixed-conifer
forests (every 35–50 years), to highseverity, stand-replacement fires of the
spruce-fir ecosystems (every 150–400
years).
Our Response: We included these firereturn interval data under the heading,
‘‘High-Intensity Wildfires and
Sedimentation of Aquatic Habitat’’ in
the final rule.
Comments From States
Comment 47: The AGFD recognizes
that both species have declined
considerably throughout their respective
ranges in Arizona, and acknowledge
that listing under the Act is warranted.
We also applaud the Service’s decision
to propose a 4(d) rule that would
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exempt take of northern Mexican
gartersnakes as a result of livestock use
at or maintenance of livestock tanks
located on non-federal lands. We also
encourage the Service to continue to
work closely with the AGFD to effect
meaningful conservation actions for
both species.
Our Response: We agree, and we look
forward to continued coordination with
the AGFD in addressing the most
serious threats that affect either species
and to exploring opportunities for
recovery with Federal, State, and local
partners and stakeholders.
Comment 48: The statement that ‘‘The
decline of the northern Mexican
gartersnake is primarily the result of
predation by and competition with
harmful nonnative species . . .’’ should
be modified to reflect that this is a
leading theory, but not necessarily true.
Our Response: We think that harmful
nonnative species (bullfrogs, crayfish,
and warm-water, predatory fish) are the
primary driving factors behind the
decline of the northern Mexican and
narrow-headed gartersnake. In the
proposed and final rules to list these
gartersnakes, we reviewed the best
available scientific and commercial
information to reach this conclusion.
We do acknowledge that other threats
such as climate change-induced
drought, dewatering of habitat, largescale wildfires, and others may have
also significantly contributed to the
decline of these gartersnakes, often in
synergistic fashion with other threats
affecting primary prey species. We also
acknowledge that some populations of
northern Mexican gartersnakes in
particular, have persisted in the
presence of harmful nonnative species
to which further study is under way.
However, these ecological situations are
rare within the distribution of these
gartersnakes, as evidenced by
widespread population declines, and
they should not be construed as
evidence that either gartersnake is
ecologically compatible with harmful
nonnative species in the long term.
Rather, the scientific information is
convincing that harmful nonnative
species are largely responsible for the
declines in these gartersnakes.
Comment 49: Reducing the status of
the species at each historical locality as
either ‘‘likely viable,’’ ‘‘likely not
viable,’’ or ‘‘likely extirpated’’ as
described in tables 1 and 2 may not
accurately capture the status of
gartersnake populations. Perhaps an
‘‘Unknown’’ category would have been
useful. Also, a low-density population
does not always indicate that the
population is not viable.
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Our Response: We agree that
adequately describing the status of each
population at each historic locality as
falling into one of three categories is
challenging. However, the general lack
of data on many populations does not
allow us to refine these categories
further. In most cases, we have more
information on the presence of threats at
each locality than good information on
the resident gartersnake population. It
was our interpretation that, in the
presence of known, and in some cases
severe, threats that a low-density
population is, at a minimum, at risk of
losing viability, most notably from
effects to reproduction and recruitment
such as in the presence of harmful
nonnative species.
Additionally, the process of
designating critical habitat requires us
to create a rule set for determining
whether the species is present or not in
each historic locality, therefore, a
category called ‘‘Unknown’’ is not
appropriate. Appendix A provides
background information that
contributed to our site-by-site
determinations of population status.
Comment 50: We caution against
using percentages to express possible
population extirpations or shifts to low
densities because unrealistic
expectations of recovery can be
established.
Our Response: We use percentages in
this listing rule and others to capture
the rangewide context of the status of a
given species’ populations to allow the
public a coarse, quantitative assessment
of the perceived status of a species,
given the best available scientific and
commercial data.
Comment 51: We suggest removing
the word ‘‘harmful’’ when referring to
the suite of nonnative species that have
been identified as the most
incompatible with the gartersnakes.
While they may be incompatible, they
are not harmful in a general context.
Our Response: We use the adjective
‘‘harmful’’ to distinguish those
nonnative species that pose unique
ecological risks to sustaining wild
populations of northern Mexican and
narrow-headed gartersnakes and their
prey species. We consider bullfrogs,
crayfish, and warm-water, predatory
sport fish as ‘‘harmful nonnative
species.’’ This distinction is based on
the predatory, or otherwise, notably
adverse interactions these species have
with the gartersnakes and their prey.
This distinction is important because
not all nonnative species are completely
incompatible with gartersnakes, and
some are used as prey for wild
gartersnake populations; nonnative trout
are an example.
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Comment 52: There are no direct data
to prove that declines in native leopard
frogs have contributed to declines in
northern Mexican gartersnake
populations. The Service should caveat
the statement with a degree of
uncertainty.
Our Response: We specifically used
the word ‘‘contributed’’ to acknowledge
that leopard frog declines are a
contributing factor to northern Mexican
gartersnake declines, not the sole factor.
As noted by the AGFD, leopard frogs are
an extremely important component to
the northern Mexican gartersnake’s prey
base—a fact also accepted within the
scientific community and demonstrated
in field study.
Comment 53: Potential risks to
gartersnake populations from fisheries
management activities were
mischaracterized in the proposed rule.
Potential effects to gartersnakes are
evaluated by the AGFD though an
Environmental Assessment Checklist
process.
Our Response: In our evaluation of
how fisheries management activities
could adversely affect gartersnake
populations, we reviewed procedures
specific to fisheries management as
provided in adopted protocols. The
Environmental Assessment Checklist
process is a parallel, internal process
implemented by the AGFD in planning
exercises that applies to multiple types
of management activities considered by
the State. We have added discussion of
this process to the final rule under the
heading ‘‘Risks to Gartersnakes from
Fisheries Management Activities’’ and
appreciate that potential effects to these
gartersnakes (or any nontarget species)
are fully evaluated prior to
implementing any activity within
occupied or designated critical habitat
for the gartersnakes.
Comment 54: In Arizona, the trapping
and subsequent use of baitfish in
angling is generally constrained to areas
where sport fish and sport fishing
dominate, and, therefore, there is little
chance the activity would affect
gartersnakes. In addition, regulations
specify that bait fish must be used at the
point of capture and not transported
elsewhere for use.
Our Response: We agree that, where
angling activities are concentrated, it is
likely due to the presence of sport fish
and in the case where warm-water,
predatory fish species are present, it is
less likely that northern Mexican or
narrow-headed gartersnakes are
immediately present. However, there are
a few areas where angling is
concentrated in habitat that could be
occupied by either or both gartersnake
species such as Oak Creek, the Verde
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River, Tonto Creek, or Parker Canyon
Lake in Arizona where it is possible that
effects to resident gartersnakes could
occur. Regardless, we included a
statement in this final listing rule that
notes that AGFD requires that baitfish
must be used where they are captured
and appreciate being notified of the
regulation and its benefits for
gartersnake conservation.
Comment 55: Please elaborate on
what is meant by the statement in
reference to the rate of Lake Roosevelt
water level fluctuation as a benefit to
harmful nonnative fish species.
Reservoir levels there fluctuate
substantially.
Our Response: We agree that water
levels in Lake Roosevelt do fluctuate
and further qualified the statement on
this issue in the final rule. We intended
to frame this discussion for comparative
purposes. That is to say, that compared
to Horseshoe Reservoir, which is
managed to minimize reproduction of
harmful nonnative species in most
years, Lake Roosevelt has several times
the capacity of Horseshoe Reservoir and
fluctuation in water levels occur at a
slower rate. The rate at which water
levels decline in these reservoir systems
affects the reproduction and recruitment
of harmful nonnative fish species; the
faster the decline, the more negative the
effect.
Comment 56: It is not clear how
‘‘build-out’’ (in reference to human
population growth and urban
development) will affect Redrock
Canyon (in the vicinity of Patagonia,
Arizona).
Our Response: The discussion in the
proposed and final rules where the issue
of build-out is addressed refers to the
long-term development plan along the
major transportation corridors of I–19,
I–10, and I–17 in Arizona. We identified
extant gartersnake populations that were
geographically proximal to these
proposed corridors which could
experience indirect effects of
development and growth in the human
population (which is expected to double
by 2030). Redrock Canyon is near the
Town of Patagonia, which is near
Nogales and the I–19 corridor. If
predictions for development and human
population growth in Arizona are
accurate, we expect increased
development in the Patagonia area,
higher levels of human recreation on
public lands, and possible effects to
water availability as a result of
increased regional groundwater
pumping or additional diversions. We
acknowledge in the final rule that, of the
areas identified where there could be
effects to gartersnake populations,
Redrock Canyon is buffered
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geographically more so than other areas
identified.
Comment 57: The section of the
proposed rule that discusses the
Arizona Department of Water Resources
Active Management Areas (AMAs)
overstates the significance of the AMA
designation for both gartersnake species.
For example, the Phoenix AMA
includes no modern records of either
species and will not affect long-term
recovery. In another example, the Pima
AMA includes only short stretches of
the Gila River; the rest of the AMA is
outside the range of either gartersnake’s
distribution.
Our Response: In our evaluation of
the effect of groundwater pumping on
gartersnake habitat, we found several
references that discuss the known
hydrological connection between
groundwater and surface flow in
southwestern streams. This is an
established concept in the scientific
community and the basis for
widespread public concern in several
areas of Arizona with respect to surface
flows including the Verde and San
Pedro Rivers. We explained how
overdrafts in groundwater use exceed
aquifer recharge (conditions that result
in an AMA designation) and result in a
cone of depression that can reduce or
eliminate surface flows in affected
streams. We listed the AMAs that both
overlap with the historical range of
either gartersnake and provide context
for the discussion of effects of
increasing human population growth on
gartersnake populations through
indirect effects of groundwater
demands. In doing so, we accurately
captured the links in this cause and
effect relationship. With respect to the
Phoenix AMA, we acknowledge that
effects on gartersnake populations are
no longer occurring. However, it was
our intent to discuss the causes of
historical population extirpations,
which were a precursor to rangewide
declines observed today. Effects of the
development of the greater Phoenix
metropolitan area include effects from
increasing regional demands on
groundwater. Aquifer overdrafts were
likely contributing factors in the
extirpation of northern Mexican
gartersnake populations in the lower
Salt, lower Gila, and lower Agua Fria
River systems.
Comment 58: No scientific evidence
has been produced that confirms a
relationship between livestock grazing
in occupied gartersnake habitat in the
presence of harmful nonnative species
and that without their presence.
Our Response: We concur that no
specific scientific study has been
afforded to this specific issue with
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respect to either the northern Mexican
gartersnake or the narrow-headed
gartersnake. However, we have
documented observations made of
gartersnake populations in Mexico in
the presence of harmful nonnative
species, as well as in their absence, in
habitat heavily affected by other land
uses such as unmanaged livestock
grazing. As discussed at length in the
subsection below entitled ‘‘The
Relationship between Harmful
Nonnative Species and Adverse Effects
to Physical Habitat,’’ we found a unique
opportunity in Mexico to observe
populations in habitat significantly
compromised by land use activities
such as unmanaged livestock grazing
where the aquatic community was
considered wholly native. Opportunities
to observe this scenario in the United
States generally do not occur due to
applied grazing management
prescriptions that largely prohibit
extreme effects to riparian habitat, and
the fact that harmful nonnative species
are largely ubiquitous in habitat
occupied by these gartersnakes in the
United States. Species experts involved
in the Mexico survey effort were in
consensus that the most significant
predictor of gartersnake occupancy in
these affected habitats was the presence
or absence of harmful nonnative
species. The fact that gartersnakes will
use vegetative cover to hide from
harmful nonnative species, and the fact
that, in the United States, gartersnake
populations that currently persist at
seemingly adequate densities in the
presence of harmful nonnatives also
occur in habitat with adequate
vegetative cover, provides further
support of this relationship. The best
available scientific and commercial
data, coupled with the opinion of
species experts, suggests this
relationship is most likely real, and we
fully endorse further scientific study of
this issue, if that opportunity exists.
Comment 59: In Mexico, the Mexican
gartersnake is listed as threatened
throughout its range in that country and
at the species level of its taxonomy. The
discussion of the threatened status of
northern Mexican gartersnake, as it
applies to this rulemaking, is, therefore,
misleading given that there are currently
10 subspecies, and the northern
Mexican gartersnake in Mexico occurs
in some of the least accessible and least
likely disturbed aquatic habitats in the
country.
Our Response: In Mexico, the clear
majority of the distribution of the
Mexican gartersnake (T. eques) is
composed of the northern Mexican
gartersnake (T. e. megalops). The
Mexican gartersnake (T. e. eques)
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comprises the second highest
percentage of the species’ distribution
along the southwestern quadrant of the
species’ distribution in Mexico
(Rossman et al. 1996, p. 173). The
remaining eight subspecies have much
smaller distributions and in some cases
are highly endemic; constrained to
perhaps a single lake. In our analysis of
the status of northern Mexican
gartersnake in Mexico, we made every
attempt to analyze only those threats
that geographically overlap our
understanding of the subspecies’
distribution, which supports the
position of a weakened status,
commensurate with Mexico’s listing.
We do not disagree that there are likely
habitats within its distribution in
Mexico that remain largely intact,
physically and ecologically. We also
note that harmful nonnative species,
once introduced into a system, have an
ecological advantage over native species
and will expand their distribution and,
therefore, the scope of their effects on
the landscape, much like what has been
observed in Arizona for decades. This
fact, and the preponderance of scientific
and commercial data we evaluated that
pertained to threats in Mexico, supports
the position taken by the Mexican
Government in listing the Mexican
gartersnake (T. eques) as threatened and
is largely applicable to the northern
Mexican gartersnake.
Comment 60: We recommend
removing the discussion referring to the
fact that many of the recovery projects
for the Chiricahua leopard frog have not
provided direct benefits to the northern
Mexican gartersnake. The Service does
not provide citations for their statement
that indirect benefits for both
gartersnake species occur through
recovery actions designed for their prey
species, and since the Chiricahua
leopard frog was listed under the Act,
significant strides have been made in its
recovery and the mitigation of its known
threats.
Our Response: In assessing how
recovery activities for currently listed
species may benefit either gartersnake, it
is important to discuss both the benefits
and limitations of these activities on
conserving or recovering nontarget
species such as the northern Mexican
gartersnake. We used reasonable
principles in conservation biology in
making the basic assertion that either
gartersnake may benefit by recovery
activities implemented for their native
prey species, such as the Chiricahua
leopard frog. For example, when
harmful nonnative species removal
projects are implemented on regional
scales, such as for bullfrogs, the
predation and competition pressure on
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gartersnake prey species are reduced,
which may lead to significant
expansions in prey species distribution
or increases in their biomass or
population densities. This activity
benefits the gartersnakes that use these
prey communities. In another example,
the construction of a fish barrier to
prevent the upstream migration of
harmful nonnative fish into a stream
provides direct benefits to the resident
gartersnake population by reducing
predation pressure on the gartersnakes
and their prey base. As for the recovery
achievements made for the Chiricahua
leopard frog, we agree that, in some
areas, these activities have benefited the
gartersnakes, particularly for the
northern Mexican gartersnake where
they have occurred in lentic habitat on
landscape scales, and specifically in
southern Arizona. However, many
recovery actions specific to the
Chiricahua leopard frog have occurred
at specific tanks higher in the
watershed, not within the floodplain of
larger perennial stream systems, where
they would yield much more significant
benefits to gartersnake populations.
Comment 61: Maintaining nonnative
sport fish populations does not
necessarily ‘‘significantly reduce the
potential for the conservation and
recovery on northern Mexican and
narrow-headed gartersnakes.’’ The
Biological and Conference Opinion
issued by the Service that addresses the
AGFD’s 10-year sport fish stocking
program (‘‘sport fish consultation’’)
includes mitigation measures to
‘‘address the effects of the proposed
action and improve the baseline
conditions for native aquatic species.’’
Our Response: We agree that
maintaining nonnative sport fish
populations in some areas may have
little effect or may even benefit some
gartersnake populations. Not all
nonnative species have the same
ecological effect on native aquatic
communities. For this reason, and for
the purposes of the greater listing
analysis afforded to these two
gartersnakes in this rulemaking, we
specifically use the phrase ‘‘harmful
nonnative species’’ when discussing
those which significantly threaten the
northern Mexican or narrow-headed
gartersnake. As previously stated, we
consider harmful nonnative species to
include bullfrogs, crayfish, and warmwater, predatory fish. The majority of
specific stocking activities that were
subject to the sport fish consultation
involved primarily salmonids (i.e.,
trout), which we do not consider to be
particularly harmful to these
gartersnakes or many of their prey
species. For example, in some areas,
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nonnative trout are an important
component to the narrow-headed
gartersnake prey base. Stocking
activities under the sport fish
consultation that involved harmful
nonnative species were few, were
constrained to lentic habitat (lakes,
ponds, etc.), and were a significant
factor behind the ‘‘likely to adversely
affect’’ determination made for these
gartersnakes and several of their prey
species.
Comment 62: In the discussion
regarding potential ramifications for
gartersnake recovery with respect to
watershed-level fisheries management
designations, the conclusions that were
drawn seem premature. Not all
nonnative fishes are considered as, or
managed as, sport fish in Arizona,
including many of the nonnative fishes
that are problematic for gartersnakes.
Our Response: Our intention was not
to predict which watersheds or
particular streams would likely be
designated as nonnative sport fisheries
in the future. Rather, we simply
acknowledged that surface water is
generally scarce in the arid Southwest
and large perennial streams, even more
so. We assume that some streams
currently occupied by the gartersnakes
are likely to be designated for nonnative
fisheries because of the scarcity of these
aquatic systems in Arizona, the existing
access infrastructure, and the fish
communities that currently reside in
larger perennial streams. We are
concerned that if large, perennial
streams, which are important occupied
habitat for northern Mexican and
narrow-headed gartersnakes (as well as
their prey species), are designated as
nonnative sport fisheries in the future,
they will be lost to the gartersnakes,
which would negatively affect their
recovery rangewide. Furthermore, we
have a high degree of certainty that if
any habitat occupied by either
gartersnake is designated strictly as a
nonnative fishery (that includes warmwater, predatory species), that habitat
will no longer possess the values that
are important (or imperative) for species
recovery and the value of these areas for
recovery will be largely eliminated.
Regarding nonnative species that are
problematic to gartersnakes and which
are not considered sport fish by the
AGFD, we look forward to partnering
with the AGFD and other public and
private stakeholders in the removal of
these species where they occur, and
view this and similar recovery actions
as the highest priority.
Comment 63: The proposed rule
discussed at length the issue of
declining native fishes and degradation
of aquatic systems in Mexico but did so
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without discussing the status of the
northern Mexican gartersnake. This type
of argument is an apparent effort to
build the case for listing the subspecies
throughout its range based on inferred
effects of the decline of native fish
communities and habitat degradation,
despite the fact that clear data for the
northern Mexican gartersnake decline
are only available for Arizona and New
Mexico.
Our Response: We do not have
population studies of northern Mexican
gartersnakes in Mexico. However, we
have used the best scientific and
commercial data available. The
information shows the status of native
aquatic vertebrates in habitat currently
or formerly occupied by the northern
Mexican gartersnake generally correlate
to the status of northern Mexican
gartersnakes. We cited examples of how
aquatic ecosystems are adversely
affected by leading threats, such as
dewatering or the expansion of harmful
nonnative species, can affect the
northern Mexican gartersnake and its
native prey species, such as fish. Native
fish comprise an important prey source
for northern Mexican gartersnakes.
Gartersnakes need them for nutrition in
order to carry out their life-history
functions. We found a significant
amount of information that concluded
that native fish communities were
significantly at risk, as documented by
declines of many species in several
subbasins across the distribution of the
northern Mexican gartersnake in
Mexico. Therefore, when a major source
of prey for northern Mexican
gartersnakes becomes rare or disappears
entirely, the gartersnake population will
be negatively affected through declines
in the fitness of individuals associated
with poor nutrition, stress, and
starvation. Several different factors that
are contributing to the decline in native
fish communities include harmful
nonnative species, dewatering of
habitat, and pollution of habitat. These
stressors also negatively affect northern
Mexican gartersnake populations both
directly and indirectly. Native fish are,
therefore, an effective surrogate for use
in determining how threats are acting on
individual northern Mexican
gartersnakes and their populations
throughout their distribution in Mexico.
Comment 64: We caution against
extrapolation, such as the statement that
there has been a 17-fold increase (since
1961) in the number of native fish
species in Mexico that have been listed
by the Mexican Federal Government as
either endangered, facing extinction,
under special protection, or likely
extinct. The data cited do not speak to
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the status of these native fish species
rangewide.
Our Response: We cited references
that discuss the status of native fish in
Mexico in our discussion of the status
of the northern Mexican gartersnake in
Mexico, and we did not imply those
trends represented their status
rangewide.
Comment 65: The Service identified a
number of streams or aquatic
communities in Mexico that have been
adversely affected by threats such as
declining native fisheries,
sedimentation from logging, pollution,
etc. Yet, our observations often point to
the inverse in several headwaters of
these identified streams. In other
´
examples, such as the Rıo Colorado in
Sonora, the vicinity of Mexico City, or
unnamed streams draining the Sierra
Madre, evidence that these areas were
occupied by the northern Mexican
gartersnake or occur within its
distribution was not clearly presented.
Our Response: Much like what has
been observed and documented in the
southwestern United States, headwater
streams are often less impacted than the
mainstem rivers they feed. This is often
because of the remote nature of these
headwaters, which can limit the effect
of human-caused threats (watershedscale effects increase in the downstream
direction), as well as the presence of
natural or man-made barriers that
prevent upstream migration of harmful
nonnative species. Therefore, it may not
be appropriate to infer that, simply
because a headwater system is intact,
that the same holds true for the system
lower in the watershed. With respect to
whether streams identified as being
impacted by various threats in Mexico
are within the distribution of the
northern Mexican gartersnake, the
references cited were not presented at a
geographic scale fine enough to
definitively conclude that a complete
overlap with the distribution of the
northern Mexican gartersnake exists, but
rather a portion of the stream overlaps.
In addition, a number of the streams
that were called into question by the
AGFD occur at the periphery of the
subspecies’ range in Mexico, which is
still not precisely understood by the
scientific community. Therefore, we
presented the data in a regional context,
as evidence that such threats could
affect the gartersnake where they
overlap.
Regarding whether the northern
Mexican gartersnake ever existed in the
´
Rıo Colorado in Sonora, there are two
verified records from the Colorado River
at Yuma from 1889 and 1890. We
assume the species also occurred
downstream into Mexico where suitable
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habitat historically existed. We also
presented data on threats to aquatic
habitat in the vicinity of Mexico City.
While we agree that this area represents
the extreme southern end of the
subspecies’ distribution, we also
acknowledge that threats, particularly
harmful nonnative species, can have a
larger geographic impact over time.
Lastly, we presented information that
suggested that threats may be affecting
streams that drain the Sierra Madre,
which in some cases were not
specifically identified by the principal
investigators. Considering that the
Sierra Madre represents a large portion
of the northern Mexican gartersnakes’
distribution in Mexico, it was
appropriate to include these data in our
evaluation in a conservative assumption
that many, if not most, of the streams
were historically or currently occupied
by this subspecies.
Comment 66: The New Mexico
Department of Game and Fish
encourages an expansion of activities
authorized under a special rule under
section 4(d) of the Act to exempt
landowners from prohibitions of take
under section 9 of the Act, for those
actions that benefit the two
gartersnakes, such as: (1) Enhancement
and restoration of native riparian
vegetation and stream structure; (2)
control of harmful nonnative species,
such as American bullfrogs and
crayfish; (3) intensive research into the
biology of the two species of
gartersnake; and (4) continuing research
into captive rearing and repatriation of
the northern Mexican and narrowheaded gartersnakes.
Our Response: We agree that section
4(d) of the Act can provide important
conservation potential in the recovery of
these two gartersnakes, and we
appreciate the New Mexico Department
of Game and Fish’s willingness to
explore such opportunities. We have
included a section 4(d) rule for the
northern Mexican gartersnake in this
rulemaking, which addresses the
management of livestock tanks on nonFederal lands. Of the four special rule
possibilities offered by the New Mexico
Department of Game and Fish,
controlling (removing) harmful
nonnative species is most likely to
provide the highest conservation benefit
for northern Mexican and narrowheaded gartersnakes, and we are
interested in looking further into this
issue with our cooperators and
stakeholders, such as the New Mexico
Department of Game and Fish. In order
to be most effective, such a 4(d) rule
would have to be developed in close
coordination with affected agencies,
explicitly authorize the removal of
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bullfrogs, crayfish, and predatory fish
species, and include precautions to
minimize potential harm to affected
gartersnake populations during project
implementation. However, at this time,
we do not have sufficient information to
allow us to adequately confirm whether
such a 4(d) rule would be necessary and
advisable for the conservation of the
species. We can consider such a rule in
the future. Permitting authority for
research needs is addressed through the
issuance of section 10(a)(1)(A) permits.
With respect to the enhancement and
restoration of native riparian vegetation
and stream structure, where water
occurs, the vegetative structure is not
viewed as limiting for gartersnake
occupation in most cases. Where water
has been removed from streams by
dams, diversions, or groundwater
pumping, correcting these scenarios and
returning water to the system would be
construed as a beneficial effect. For any
activity not explicitly addressed in our
proposed 4(d) rule that would result in
take of either gartersnake, a section 10
permit would be required to avoid a
violation of section 9 of the Act.
Tribes
Comment 67: In discussing the
potential impacts of dams and reservoirs
on resident fish communities, the
proposed rule identifies the San Carlos
Reservoir as an example of a reservoir
that benefits harmful nonnative species
and, therefore, negatively affects the
northern Mexican and narrow-headed
gartersnakes. This statement should be
omitted from the final rule for two
reasons. First, the proposed rule makes
this conclusory adverse effect
determination without any support
whatsoever. Second, this conclusory
determination is unnecessary to
establish that the northern Mexican
gartersnake or the narrow-headed
gartersnake should be designated as
threatened. In 1924, Congress enacted
the San Carlos Project Act, which
authorized the construction of the
Coolidge Dam and the creation of the
San Carlos Reservoir ‘‘for the purpose
. . . of providing water for the irrigation
of lands allotted to the Pima Indians on
the Gila River Reservation, Arizona.’’ A
statement in the proposed rule that the
San Carlos Reservoir adversely affects
northern Mexican and narrow-headed
gartersnakes could affect the federally
mandated delivery of water to the Gila
River Indian Community. Any
impediment to the Gila River Indian
Community’s irrigation system threatens
the Gila River Indian Community’s
agriculture, economy, and most
importantly, the survival of its culture,
the value of which is immeasurable.
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Our Response: In the final rule, we
deleted the reference to the San Carlos
Reservoir as an example of a reservoir
within the range of the gartersnakes that
may be benefitting harmful nonnative
species, because there are several other
examples. USFWS (2008, pp. 112–131)
provides a complete scientific analysis
of the relationship of reservoirs to
resident aquatic communities upstream
and downstream, includes many
scientific references that have been
incorporated by reference in this final
rule, and comprises the basis for the
issuance of a section 10(a)(1)(B)
incidental take permit for the operation
of Horseshoe and Bartlett Reservoirs, in
that case. We believe the same
relationships likely are true at San
Carlos Reservoir. We look forward to
work with interested parties to identify
solutions that meet water use interests
and the conservation needs of listed
species.
Public Comments
General
Comment 68: Threats to the
gartersnakes are those caused by Federal
and State fish and wildlife management
actions, or on Federal lands that can be
dealt with outside of the Act.
Approximately 85 percent of the habitat
for the northern Mexican gartersnake is
in Mexico. In Mexico, any activity that
intentionally destroys or adversely
modifies occupied northern Mexican
gartersnake habitat is prohibited.
Our Response: As stated in the
proposed rule, the Act requires us to
make listing determinations based on
the five threat factors, singly or in
combination, as set forth in section
4(a)(1) of the Act. The Act further
requires us to make listing
determinations solely on the basis of the
best scientific and commercial data
available after taking into account those
efforts, if any, being made by any State
or foreign nation, or any political
subdivision of a State or foreign nation,
to protect such species, whether by
predator control, protection of habitat
and food supply, or other conservation
practices within any area under its
jurisdiction. The Act requires us to give
consideration to species that have been
designated as requiring protection from
unrestricted commerce by any foreign
nation or pursuant to any international
agreement; or identified as in danger of
extinction or likely to become so within
the foreseeable future, by any State
agency or by any agency of a foreign
nation that is responsible for the
conservation of fish or wildlife or
plants.
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A number of existing regulations
potentially address issues affecting the
northern Mexican and narrow-headed
gartersnakes and their habitats.
However, existing regulations within
the range of northern Mexican and
narrow-headed gartersnakes typically
address only the direct take of
individuals without a permit and
provide little, if any, protection of
gartersnake habitat. Arizona and New
Mexico statutes do not provide
protection of habitat and ecosystems.
Legislation in Mexico prohibits
intentional destruction or modification
of northern Mexican gartersnake habitat,
but neither that, nor prohibitions of
take, appear to be adequate to address
ongoing threats. See ‘‘The Inadequacy of
Existing Regulatory Mechanisms’’ in the
proposed rule for further information.
Comment 69: There is more recent
data on surface activity of northern
Mexican gartersnakes than Rosen (1991,
pp. 308–309). More recent observations
indicate radio-tracked snakes were not
surface active 64 percent of the time at
Bubbling Ponds and 60 percent of the
time at Tavasci Marsh (upper Verde
River) and the middle Verde River.
Our Response: We have updated the
discussion under ‘‘Habitat and Natural
History’’ for the northern Mexican
gartersnake in this final rule to reflect
more recent information, such as the
information provided in the comment.
Comment 70: The proposed rule states
that the northern Mexican gartersnake
appears to be most active during July
and August, followed by June and
September. Based on recent survey
efforts it would probably be most
accurate to state that the species appears
to be most active between May and
September.
Our Response: We have updated the
discussion under ‘‘Habitat and Natural
History’’ for the northern Mexican
gartersnake in this final rule to reflect
more recent information, such as the
information provided in the comment.
Comment 71: The proposed rule so
broadly describes the species’ physical
habitat that it is difficult to determine
what types of riparian, wetland, and
terrestrial habitats are important to each
of the gartersnakes and is conflicting
with previous characterizations.
Our Response: The habitat
descriptions we provide in the proposed
and final rules reflect the current
understanding of the types of habitat
that are used by either gartersnake
species. The descriptions appear broad
because these gartersnakes, in particular
the northern Mexican gartersnake, can
occur in varied ecological settings.
Comment 72: All five of the waters
where there are viable populations of
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Mexican gartersnakes are already
protected and do not need further
protection under the Act. Oak Creek,
Tonto Creek, and the Upper Verde River
are protected by spikedace and loach
minnow critical habitat. The San Rafael
Valley is protected by The Nature
Conservancy and San Rafael State Park.
The Bill Williams River is a National
Wildlife Refuge.
Our Response: We acknowledged in
our proposed rule that other listed
species’ historic ranges overlap with the
historical distribution of northern
Mexican and narrow-headed
gartersnakes. However, as stated above
and in the proposed rule, the Act
requires us to make listing
determinations based on the five threat
factors, singly or in combination, after
taking into account those efforts being
made by any State or foreign nation to
protect such species. Management by
Federal or State agencies, or nongovernmental organizations does not
necessarily eliminate activities that
threaten these subspecies.
Comment 73: The northern Mexican
gartersnake in the United States is not
a distinct population segment and does
not require protection under the Act.
Our Response: We did not propose to
list either gartersnake as a distinct
population segment. We proposed to list
the northern Mexican and narrowheaded gartersnakes as threatened
throughout their ranges. We also
reviewed the best available scientific
and commercial information to
conclude that the northern Mexican
gartersnake is a valid subspecies as
defined under the Act.
Comment 74: The Service must follow
the guidance of Executive Order 13563
of January 18, 2011, concerning making
a new Federal rule.
Our Response: Executive Order (E.O.)
13563 reaffirms the principles of E.O.
12866 while calling for improvements
in the nation’s regulatory system to
promote predictability, to reduce
uncertainty, and to use the best, most
innovative, and least burdensome tools
for achieving regulatory ends. The
executive order directs agencies to
consider regulatory approaches that
reduce burdens and maintain flexibility
and freedom of choice for the public
where these approaches are relevant,
feasible, and consistent with regulatory
objectives. E.O. 13563 emphasizes
further that regulations must be based
on the best available science and that
the rulemaking process must allow for
public participation and an open
exchange of ideas. We have developed
this rule in a manner consistent with
these requirements.
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Comment 75: These gartersnakes are
already protected by the New Mexico
Department of Game and Fish.
Our Response: A number of existing
regulations potentially address issues
affecting the northern Mexican and
narrow-headed gartersnakes and their
habitats. However, existing regulations
within the range of northern Mexican
and narrow-headed gartersnakes
typically address only the direct take of
individuals without a permit, and
provide little, if any, protection of
gartersnake habitat. Arizona and New
Mexico statutes do not provide
protection of habitat and ecosystems.
Legislation in Mexico prohibits
intentional destruction or modification
of northern Mexican gartersnake habitat,
but neither that legislation, nor
prohibitions of take, completely address
ongoing threats. See ‘‘The Inadequacy of
Existing Regulatory Mechanisms’’ in
this final rule for further information.
Comment 76: The Strategic Water
Reserve, managed by the New Mexico
Interstate Stream Commission, already
holds and utilizes water rights to benefit
endangered fish and wildlife species in
New Mexico. Since the Service gives
strongest weight to statutes because they
are nondiscretionary and enforceable,
the New Mexico Interstate Stream
Commission expects the Service to give
weight to the Strategic Water Reserve
statute in this final rule.
Our Response: We considered the
Strategic Water Reserve managed by the
New Mexico Interstate Stream
Commission and have updated the
discussion in the final rule with this
new information. However, collectively,
existing regulations within the range of
northern Mexican and narrow-headed
gartersnakes are not fully ameliorating
ongoing threats such that the subspecies
would not meet the definition of
threatened. See ‘‘The Inadequacy of
Existing Regulatory Mechanisms’’ in
this final rule for further information.
Comment 77: Contrary to what is
implied in the proposed rule, Clean
Water Act section 404 nationwide
permits receive rigorous environmental
review by the Corps.
Our Response: We recognize that the
Clean Water Act section 404 nationwide
permits receive environmental review
by the Corps; however, this process does
not appear to be ameliorating ongoing
threats to northern Mexican or narrowheaded gartersnakes such that the
subspecies would not meet the
definition of threatened. See ‘‘The
Inadequacy of Existing Regulatory
Mechanisms’’ in this final rule for
further information.
Comment 78: What is the problem
with the management or resources at the
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Buenos Aires National Wildlife Refuge
(BANWR) that makes populations likely
not viable.
Our Response: The abundance of
bullfrogs on the BANWR, specifically in
the vicinity of Arivaca Lake and Arivaca
Cienega, contributes to the northern
Mexican gartersnake population being
categorized as likely not viable. As
stated in our proposed rule, bullfrogs
(and other harmful nonnatives) are a
primary threat to the gartersnakes. The
presence of a single juvenile northern
Mexican gartersnake was confirmed on
the BANWR in 2000 (Rosen et al. 2001,
Appendix I). The observation of this
juvenile suggests that at least some level
of reproduction had occurred and may
still be occurring but more recent survey
work has not occurred there. The
presence of dense cover probably helps
any remaining northern Mexican
gartersnakes to avoid predation.
In recent years, there has been a
concerted management effort on the
BANWR to recover the Chiricahua
leopard frog in an array of tanks and
their associated drainages, all of which
have been designated as critical habitat
for the Chiricahua leopard frog. As a
result, it is likely that any northern
Mexican gartersnakes that successfully
immigrate into the central tanks area of
the BANWR have an increased chance
of persistence because of improved
available habitat and a stable prey base
in an area that is likely free of nonnative
predators. We also expect that
dispersing Chiricahua leopard frogs
might help sustain a low-density
population of northern Mexican
gartersnakes on the refuge. We consider
the northern Mexican gartersnake to be
extant as a low-density population on
the BANWR based on historical and
recent records and the abundance of
available, suitable habitat and prey
populations in the vicinity of the most
recent record. Appendix A contains
additional details on the status of the
northern Mexican gartersnake at this
and other refuges.
Comment 79: What is the relationship
of the Arizona Department of Water
Resource laws and the proposed listing
of the two gartersnakes? For New
Mexico, the New Mexico State Engineer
indicated that any person in New
Mexico can apply to the State Engineer
for a permit for the lease of a valid
existing water right to augment or
maintain stream flow for the beneficial
use of fish and wildlife habitat,
maintenance or restoration. Further,
permits for the permanent transfer of
water rights for such purposes have
already been granted to the New Mexico
Interstate Stream Commission. Both the
Strategic Water Reserve option and the
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leasing option retain a water right’s
original priority date.
Our Response: Existing water laws in
Arizona and New Mexico may not be
fully adequate to protect gartersnake
habitat from the dewatering effects of
groundwater withdrawals. New Mexico
water law now includes provisions for
instream water rights to protect fish and
wildlife and their habitats. Arizona
water law also recognizes such
provisions; however, because this
change is relatively recent, instream
water rights have low priority and are
often never fulfilled because more
senior diversion rights have priority.
With respect to New Mexico, we have
updated the discussion on New Mexico
water rights laws in the final rule to
correct any inaccuracies.
Comment 80: The information in
Table 1 of the proposed rule does not
match the information on page 41515.
Page 41515 states that a former large,
local population of northern Mexican
gartersnakes at the San Bernardino
National Wildlife Refuge has
experienced correlative decline of
leopard frogs and are now thought to
occur at very low population density or
may be extirpated. Table 1 states likely
not viable.
Our Response: We consider
gartersnake populations with very low
population densities, and thus at higher
risk of extirpation, such as the one at
San Bernardino National Wildlife
Refuge, to be likely not viable. While the
population could already be extirpated,
we did not have sufficient information
to categorize it as likely extirpated and
so called it likely not viable.
Surveys and Monitoring
Comment 81: The proposed rule states
that the northern Mexican gartersnake
has declined significantly in the last 30
years, but then goes on to state that
there are several areas where the species
was known to occur but has received no
or very little survey effort in the past
decades.
Our Response: We based our
conclusions on the best scientific and
commercial data available at the time of
listing. We have concluded that, in as
many as 24 of 29 known localities in the
United States (83 percent), the northern
Mexican gartersnake population is
likely not viable and may exist at low
population densities that could be
threatened with extirpation or may
already be extirpated. In most localities
where the species may occur at low
population densities, existing survey
data are insufficient to verify
extirpation. Only five populations of
northern Mexican gartersnakes in the
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United States are considered likely
viable.
Comment 82: The Service assumes the
populations at Whitewater Creek and
Middle Fork Gila River are likely
deteriorated or have been severely
jeopardized after the Whitewater-Baldy
Complex Fire, but subsequent survey
data have not been collected. In the
absence of subsequent survey data, the
Service lacks information to supports its
assumption that the narrow-headed
gartersnake populations have
deteriorated. Further, we understand
that some of the northern Mexican
gartersnakes discovered in the Gila
National Forest in June 2013 were found
precisely in Whitewater Creek. Among
the discovered snakes were young males
and at least one viable reproducing
female, suggesting that the populations
of northern Mexican gartersnakes are
living and reproducing in the area. The
discovery of a reproducing population
of northern Mexican gartersnakes in this
area suggests that populations of
narrow-headed gartersnakes may not be
as likely deteriorated as the Service
suggests.
Our Response: The proposed rule
states that the status of those
populations has likely deteriorated as a
result of subsequent declines in resident
fish communities due to wildfires
followed by heavy ash and sediment
flows, resulting fish kills, and the
removal of snakes. Immediately after the
Whitewater-Baldy Complex Fire, but
before the subsequent monsoon, we
were actively working with other
agencies and species experts on
assessing the likely damage to the
resident fish community and planning
salvage operations for narrow-headed
gartersnakes. As stated in Appendix A
(available at https://www.regulations.gov,
Docket No. FWS–R2–ES–2013–0071),
populations are thought to remain
extant at Whitewater Creek and Middle
Fork Gila River, but in the short to mid
term we anticipate the density of the
narrow-headed gartersnake population
to be low due to the Whitewater-Baldy
Complex Fire. These sites may rebound
in the mid to long term when subbasin
conditions stabilize and fish begin to
recolonize the stream or are otherwise
reintroduced through restoration efforts.
See ‘‘High-Intensity Wildfires and
Sedimentation of Aquatic Habitat’’
section of the final rule for additional
information. The best available
scientific and commercial data
indicated that high-intensity wildfires
have the potential to eliminate
gartersnake populations through a
reduction or loss of their prey base.
Northern Mexican gartersnakes have
never been documented in Whitewater
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Creek, but were rediscovered in the Gila
River in 2013.
Comment 83: Haney et al. (2008, p.
61) declared the northern Mexican
gartersnake as nearly lost from the
Verde River, but also suggested that
diminished river flow may be an
important factor. Given the multiple
recent detections of northern Mexican
gartersnakes along the upper and
middle Verde River, this statement does
not seem relevant to include in the
proposed rule.
Our Response: More recent
population status data for the northern
Mexican gartersnake for the Verde River
were preliminary and unpublished at
the time the proposed rule was drafted.
These newer data have been
incorporated into the final rule and
Appendix A.
Comment 84: Is a consistent survey
protocol being followed each year? Is
data collected from different surveys
comparable? Without scientific survey
protocol implemented consistently for
at least 10 years, there can be no real
evidence of population trends.
Our Response: There is currently no
accepted protocol for northern Mexican
or narrow-headed gartersnake surveys;
however, some investigators have
attempted to revisit locations where
others have surveyed in the past in an
attempt to establish population trends.
Variability in survey design and effort
makes it difficult to compare population
sizes or trends among sites and between
sampling periods. For each of the sites
discussed in Appendix A, we have
attempted to translate and quantify
search and capture efforts into
comparable units (i.e., person-search
hours and trap-hours) and have
conservatively interpreted those results.
Where population trends have been
established, they have been reported
and reflect significant declines in both
species.
Comment 85: The Service has failed
to survey, analyze data, and incorporate
the effects of the thousands of livestock
tanks and other impoundments that
have been constructed in recent times
that are now occupied by the narrowheaded and northern Mexican
gartersnakes. These stock tanks and
manmade impoundments offer the best
opportunity for refugia for the narrowheaded and northern Mexican
gartersnakes and could prove to be very
important for the future survival of
these gartersnakes, as well as the
Chiricahua leopard frog. Given the
quantity of tanks and other
impoundments constructed in the last
50 years, the number of these structures
that are used by the gartersnakes could
be substantial, and, therefore, the
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potential population count for the
species could be significantly higher
than speculated.
Our Response: Surveys of every stock
tank that could occur within the
distribution of both gartersnake species
have not been done. The Act requires
that we base our evaluation on the best
scientific and commercial information
available. We agree that well-managed
stock tanks represent conservation and
recovery opportunities for the northern
Mexican gartersnake and have
consequently developed a rule under
section 4(d) of the Act that exempts
otherwise unauthorized take of northern
Mexican gartersnakes from livestock use
or maintenance of stock tanks on nonFederal lands. Stock tanks are not
considered suitable habitat for narrowheaded gartersnakes, and the species
has never been reported using a stock
tank.
Harmful Nonnative Species and Other
Threats
Comment 86: No information is
provided describing San Carlos
Reservoir operations and their effects on
nonnative and native aquatic species,
whether there are or ever has been
gartersnakes in or near the San Carlos
Reservoir and the status of any
nonnative fish populations on the Gila
River at San Carlos Reservoir. This is
not based on the best available science.
Our Response: Distribution data
strongly suggest that northern Mexican
and narrow-headed gartersnakes
historically occurred along the middle
Gila River, as this was formerly a major
perennial river with several known
populations both upstream and within
numerous tributaries, with suitable
habitat, and a robust native prey base.
Post-construction of the San Carlos
Reservoir, survey data are limited. Thus
it remains difficult to ascertain the
current status of gartersnake
populations upstream, downstream, or
within the reservoir itself. As far as the
effect of the reservoir on the up- or
downstream aquatic community, similar
analysis have been performed for the
Horseshoe and Bartlett Reservoirs,
which resulted in the issuance of a
section 10(a)(1)(B) permit for the
incidental take of native fish species,
the lowland leopard frog, the northern
Mexican gartersnake, and the narrowheaded gartersnake. USFWS (2008, pp.
112–131) supports our rationale as to
how adverse effects to native aquatic
species occur from the presence and
operation of reservoirs in the Gila River
basin of Arizona.
Comment 87: In the proposed rule,
the Service refers to the potential
development of the Hooker Dam on the
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mainstem Gila River above Mogollon
Creek and below Turkey Creek. The U.S.
Bureau of Reclamation has abandoned
any intention of completing Hooker
Dam, and its reference as a possible
future project should be deleted from
the final rule.
Our Response: We have confirmed
with the U.S. Bureau of Reclamation
that there are no current plans to
develop Hooker Dam, and it is not
referenced in the final rule.
Comment 88: Barriers to fish
movement out of Roosevelt Lake should
be acknowledged in the final rule. The
Roosevelt Dam on the Salt River serves
as an effective barrier to upstream fish
movement, which would prevent
nonnative fish from moving upstream.
Our Response: In the final rule, we
added a statement in our discussion of
dams to reflect this fact.
Comment 89: The proposed rule states
that additional land and water use
activities along Tonto Creek and the Salt
River, including areas upstream of
Roosevelt Lake, contribute to the
persistence of nonnative aquatic species
that negatively affect the gartersnakes.
However, the Tonto Creek exhibits
seasonally intermittent flows in the
lower reaches below Gun Creek.
Sections of dry streambed serve as a
barrier to upstream fish migration.
Further, high flow events have been
documented to remove nonnative
species by flushing them downstream.
In addition, nonnative spiny-rayed fish
are not typically motivated to migrate
upstream out of lakes because they
prefer lentic over lotic habitats.
Our Response: Connectivity between
otherwise spatially intermittent reaches
is established during seasonal periods of
snowmelt runoff as well as during
medium- to large-scale flood pulses.
These opportunities contribute to the
distribution of harmful nonnative fish
throughout Tonto Creek, as
demonstrated in fish survey data that
has been collected, reviewed, and
reported in Appendix A. With respect to
whether harmful nonnative fish are ‘‘not
typically motivated to migrate upstream
out of lakes,’’ the data are lacking to
clearly defend this statement, especially
when reservoir levels decrease, which
lessens the amount of space available in
reservoirs, which may in turn trigger
dispersal or movement behaviors in
harmful nonnative fish that are known
to be territorial by their nature.
Additionally, the simple presence of
otherwise ‘‘lentic’’ nonnative species in
lotic habitat upstream of reservoirs to
which they are hydrologically
connected, suggests this perceived
preference may not be altogether true;
green sunfish are an excellent example.
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Comment 90: A number of other
activities (both present and historical) in
the area of Tonto Creek and the Salt
River in the vicinity and upstream of
Roosevelt Lake are likely contributing to
the decline of gartersnakes and the
aquatic and riparian habitat on which
they depend. Specifically, a historical
stocking program of nonnatives,
manmade impoundments within the
Tonto Creek floodplain, and other
activities identified in the proposed
rule, such as groundwater pumping,
flood control projects, urbanization, and
livestock grazing. The major activities
reducing flows and dewatering habitat
are occurring upstream of Roosevelt
Lake. A bridge is proposed over Tonto
Creek, and 320 to 640 residences are
projected to be built on the east side of
Tonto Creek, under the Gila County’s
comprehensive plan. This would
increase water and recreational use. The
U.S. Forest Service’s Motorized Travel
Management Plan has the potential to
open 2,567 miles (4,131 km) of road to
high clearance vehicles and 967 miles
(1,556 km) to passenger vehicles. The
Tonto National Forest’s Salt River
Allotments Vegetative Management Plan
would allow continued grazing on more
than 275,000 acres (111,000 ha) along
the Upper Salt River. Potential impacts
to the narrow-headed gartersnake are
noted, and the potentially suitable
habitat for the northern Mexican
gartersnake that occurs along the Salt
River is the same area that the USFS
proposes for grazing.
Our Response: We agree that
numerous threats are affecting the status
of both gartersnake species in Tonto
Creek. The final rule (see ‘‘Altering or
Dewatering Aquatic Habitat’’) references
land use activities in this area that we
consider as having an effect on resident
gartersnake populations.
Comment 91: The Service’s
generalized and unsupported assertions
that all dams have the same impacts on
gartersnakes should be removed from
the final rule. The ‘‘Altering or
Dewatering Aquatic Habitat’’ section of
the proposed rule is not supported by
any citations regarding water level
fluctuations in reservoirs and crosssection profiles of a reservoir. This
section should provide citations and
recognize the diversity of the various
types of reservoirs.
Statements regarding the effect of
Roosevelt Lake on gartersnake
populations in Tonto Creek and the
upper Salt River lack any scientific or
technical basis and should be removed
from the final rule. Other than
referencing a biological opinion
(USFWS 2008, pp. 112–131), the
proposed rule provides no basis for the
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assertion that harmful nonnative fish are
moving upstream out of Roosevelt Lake
into Tonto Creek or the Salt River. Since
the biological opinion in 2008,
monitoring conducted under the
Horseshoe-Bartlett Habitat Conservation
Plan has been implemented to
document the movement of nonnative
fish upstream of the Horseshoe
Reservoir into the Verde River, and
reaches of the Verde River have been
sampled, and to date no evidence of fish
movement has been detected.
Our Response: We agree that not
every dam has the same effect on the
stream on which it is located. We
disagree that our treatment of the effects
of dams on occupied lotic habitat are
unsupported. The identified section
discusses general effects of dams, based
on available literature, as a suite of
effects common in all instances in
various degrees. This same section also
includes referenced discussion of
specific dams or diversions and their
specific effects on certain gartersnake
populations. The relationship of the
cross-sectional profiles and water level
fluctuations of reservoirs to benefits to
harmful nonnative fish communities
was an integral part of a 4-year
evaluation, in close collaboration with
the operators of those reservoirs
themselves, dedicated to the
development of the habitat conservation
plan for Bartlett and Horseshoe
Reservoirs on the Verde River. We
incorporated by reference this
exhaustive analysis, which used the best
available data to date (see SRP 2008,
entire; USFWS 2008, pp. 112–131).
We are not aware of any analysis
afforded specifically to the potential
benefits of Roosevelt Dam operations to
the sustainment or production of
harmful nonnative fish populations in
Roosevelt Lake, Tonto Creek, or the Salt
River, upstream of Roosevelt Dam. The
exhaustive analysis of these effects as
they are attributed to similarly sized
dams and reservoirs on the Verde River
system referenced immediately above
represent the most applicable, current,
and robust analyses to date. We do note
that Roosevelt Lake does not fluctuate as
much as does Horseshoe Reservoir on
the Verde River and, therefore, most
likely provides greater benefits to the
resident harmful nonnative fish
community. With respect to fish
sampling data from the implementation
of the Horseshoe and Bartlett HCP,
sampling events do not occur during the
most appropriate time to capture
movement of fish out of the reservoir
(during periods of rapid drawdown or
during drawdown after periods of
prolonged storage) and thus may not
adequately capture these relationships.
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Additionally, more fish have to be
marked in the reservoir to create better
opportunities for their discovery
elsewhere in the watershed. Lastly,
recent northern Mexican gartersnake
records have been reported immediately
upstream, if not adjacent to, Roosevelt
Lake, which affirms that adverse effects
from harmful nonnative species that
occur in Roosevelt Lake present a
demonstrable threat to that population
of northern Mexican gartersnakes.
Comment 92: The proposed rule states
that, on the upper Verde River, native
species dominated the total fish
community at greater than 80 percent
from 1994 to 1996, before dropping to
approximately 20 percent in 1997 and
19 percent in 2001. This statement
points to specific empirical data
regarding declining native fish species
in the upper Verde River watershed, but
there is no reference to verify the
sources, context, or specific species to
which it is referring.
Our Response: Rinne et al. (2005, pp.
6–7) contains a discussion of shifting
fish communities in the Verde River,
and Bonar et al. (2004, entire) contains
a detailed analysis of the role harmful
nonnative fishes have had on the native
fish community of the Verde River. Also
Bonar et al. (2004, pp. 6–7) summarizes
this information.
Comment 93: If it is true that the
narrow-headed and northern Mexican
gartersnakes have declined substantially
in the United States and the decline of
these species is most likely due to the
introduction of nonnative predator and
competitor species as stated in the 2006
and 2008 status reports, then the listing
of these species as threatened will do
little for their recovery.
Our Response: As stated in the
proposed rule, conservation measures
provided to species listed as endangered
or threatened species under the Act
include recognition, recovery actions,
requirements for Federal protection, and
prohibitions against certain practices.
Recognition of conservation needs of
species through listing under the Act
results in public awareness and
conservation by Federal, State, tribal,
and local agencies, private
organizations, and individuals. The Act
encourages cooperation with the States
and recovery plans will identify
recovery actions that will benefit listed
species. See ‘‘Available Conservation
Measures’’ in this final rule for
additional information on this subject.
Comment 94: Local persons are
catching gartersnakes in contests and
seeing how many they can kill to win
the contest.
Our Response: We have no
information to indicate that collection of
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gartersnakes is a significant threat.
However, if this activity is occurring, it
will be considered a prohibited take of
the species, once listed.
Comment 95: The Service should take
into account the adverse effects of the
past Federal land management agency
burning programs and the recent
wildfires that have occurred in the
narrow-headed and northern Mexican
gartersnakes home ranges. Closer
scrutiny of the current Federal land
management burning program, and lack
of a coherent thinning and logging
program, coupled with a better
understanding of the effects of the
recent large wildfires, should be
completed in order to focus future
protection and restoration efforts
towards what is truly causing the
decline of the narrow-headed and
northern Mexican gartersnakes. There is
no benefit to immediately listing these
gartersnakes as threatened when there is
doubt concerning the current and future
potential cause for decline of the
species.
Our Response: In the proposed rule,
we discuss effects of recent fire
management policies on aquatic
communities in Madrean Oak
Woodland biotic communities in the
southwestern United States. Existing
wildfire suppression policies intended
to protect the expanding number of
human structures on forested public
lands have altered the fuel loads in
these ecosystems and increased the
probability of high-intensity wildfires
(Rinne and Neary 1996, p. 143). The
historical actions affecting a species are
considered as background in our
assessment in terms of their
contribution to the present-day status of
these species. However, in evaluating
the status of the species, the Act
requires that we assess present and
future factors that may threaten the
species. If past actions are continuing
threats, these threats are evaluated
under the five-factor analysis. If these
past actions are not continued factors,
then these actions are not assessed in
the analysis of the future status because
they are no longer present or future
factors threatening the species.
Section 7(a)(1) of the Act requires that
all Federal agencies shall utilize their
authorities in furtherance of the
purposes of the Act by carrying out
programs for the conservation of
endangered and threatened species.
Section 7(a)(2) of the Act requires
Federal agencies to ensure that activities
they authorize, fund, or carry out are not
likely to jeopardize the continued
existence of the species or destroy or
adversely modify its critical habitat. If a
Federal action may affect a listed
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species or its critical habitat, the
responsible Federal agency must enter
into formal consultation with us. Lastly,
while we acknowledge in the proposed
and final rules that large wildfires can
have significant adverse effects on
gartersnake populations and their prey
base (in particular for narrow-headed
gartersnakes), the literature is clear that
harmful nonnative species pose the
most significant threat to both species,
rangewide, through a variety of
ecological mechanisms.
Comment 96: The proposed rule states
that Cavazos and Arriaga (2010, entire)
found that average temperatures along
the Mexican Plateau in Mexico could
rise by as much as 1.8 °F (1 °C) in the
next 20 years and by as much as 9 °F (5
°C) in the next 20 years, according to
their models. This statement is
confusing because the reference cites
two different temperatures for the same
timeframe in the same area.
Our Response: Climate models often
report a range of scenarios, as was the
case in this instance. We did revise that
language for clarity. However, we expect
precipitation and temperature trends, as
modeled under future climate change
projections, to increase regional aridity
in Mexico within the distribution of the
northern Mexican gartersnake, which is
expected to place additional drought
stress on stream flow and reduce the
permanency of cienegas, marshes, and
livestock tanks. As streams dry, they
will become unsuitable as habitat for
this gartersnake and its prey base over
the next several decades.
Comment 97: We request that the
Service provide clarification and more
information regarding the presence of
mercury in Tonto Creek and likely
sources of this substance. No study was
cited for the claim that mercury appears
to be bioaccumulating in fish in the
lower reaches of the Tonto Creek, only
a personal communication with Arizona
Department of Environmental Quality.
The information in the proposed rule is
contrary to the Arizona Department of
Environmental Quality’s 2011 report on
‘‘Fish Consumption Risk Analysis for
Tonto Creek, Arizona.’’ Specifically,
desert suckers have the fourth highest
mercury levels, not the second.
Our Response: We updated this
discussion under ‘‘Environmental
Contaminants’’ in the final rule to
include data reported by ADEQ (2011,
entire), as well as other information, and
acknowledged in the proposed and final
rules that no study on the
bioaccumulation of mercury in resident
gartersnakes has been implemented that
we are aware of. The suggestion that
bioaccumulation of mercury could be
occurring is based on the accepted
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scientific premise regarding the
toxicology of mercury in ecosystems
and its ability to increase its
concentration in tissue with increasing
trophic orders. Gartersnakes are tertiary
consumers and, therefore, are expected
to bioaccumulate contaminants such as
mercury in their tissues.
Comment 98: The term excessive
sedimentation as used in the proposed
rule is open to interpretation and should
be defined to eliminate unnecessary
waste of resources of the Service in
defending its finding. Any large storm
event that changes the morphology of a
channel or adjoining riparian habitat
can be used to control all human
activities in that they can be construed
to have caused the resulting flooding.
Our Response: It is beyond our scope
to quantitatively define what level of
sedimentation is excessive for every
stream. However, we agree that flood
pulses naturally liberate sediment in
arid southwestern watersheds. In the
absence of absolute values or metrics,
we consider excessive sedimentation
that level in which resident gartersnake
prey species or gartersnakes themselves
are not able to adequately carry out lifehistory functions such as feeding,
sheltering, or breeding as a result of the
effects of sedimentation. Arizona and
New Mexico also have turbidity or total
dissolved solid standards for surface
water, which can also be used as a
reference.
Comment 99: The proposal to list is
based on the false premise that riparian
habitats are declining in the Southwest
(see Webb et al. 2007).
Our Response: A comprehensive
analysis of the scientific literature
supports our evaluation of the status of
habitat where these gartersnakes
historically or currently occur.
Comment 100: We request the Service
clarify the year of reference in their
projection that annual precipitation
amounts in the southwestern United
States may decrease by 10 percent by
the year 2100.
Our Response: Overpeck (2008,
entire) is a presentation where this
information was originally presented
although much of the information used
in Overpeck (2008) was from the
Intergovernmental Panel on Climate
Change (IPCC 2007). We presume the
year(s) of reference may be 2007–2008
because that is the time period when the
reference was created.
Comment 101: The Service should
acknowledge the uncertainty of broad
predictions associated with climate
change in their final rule.
Our Response: In our analyses, we use
our expert judgment to weigh relevant
information, including uncertainty, in
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our consideration of various aspects of
climate change and their predicted
effects on northern Mexican and
narrow-headed gartersnakes.
Comment 102: The Service states that
wildfire is a threat to the narrow-headed
gartersnake throughout its range.
However, the Service also discusses the
Dry Lakes Fire of 2002, which resulted
in a complete fish kill in Turkey Creek.
Turkey Creek has since been
recolonized by native fish species
almost exclusively. Consequently, it is
conceivable that snakes that survived a
period without fish might then find
themselves in an environment better
suited to their needs (i.e., devoid of
nonnative species) than before the fire.
Further, the Service states that both
species of gartersnakes are somewhat
resilient to physical habitat disturbance
where harmful nonnative species are
absent.
Our Response: We agree that if
enough individual narrow-headed
gartersnakes can survive the post-fire
period of ash flows and fish kills,
without risking genetic bottlenecking
within the population, that an ensuing
native-only fish community would be
highly beneficial. However, field
research has proven that over time and
without a barrier to upstream
movement, harmful nonnative fish
ultimately make their way back into
these streams and negatively affect the
native aquatic community. Therefore,
any plausible post-fire benefits to
surviving narrow-headed gartersnakes
are most likely short-lived.
Information Quality and Quantity
Comment 103: Personal
communications of a graduate student
are a weak basis for determining the
current status of the narrow-headed
gartersnake in New Mexico (or, as found
in other citations, the effects of the
Whitewater Baldy fire on the narrowheaded and northern Mexican
gartersnakes). Personal communications
or gray literature are not subject to the
necessary vigorous peer review and
substantiation that would meet the Act’s
requirements for science-based or
commercial data.
Our Response: As required by the Act,
we based our proposal and this final
rule on the best available scientific and
commercial data. Our Policy on
Information Standards Under the Act
(published in the Federal Register on
July 1, 1994 (59 FR 34271)), the
Information Quality Act (section 515 of
the Treasury and General Government
Appropriations Act for Fiscal Year 2001
(Pub. L. 106–554; H.R. 5658)), and our
associated Information Quality
Guidelines, provide criteria, establish
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procedures, and provide guidance to
ensure that our decisions are based on
the best scientific data available.
Information sources may include the
recovery plan for the species, articles in
peer-reviewed journals, conservation
plans developed by States and counties,
scientific status surveys and studies,
biological assessments, other
unpublished materials, or experts’
opinions or personal knowledge. We
receive and use information on the
biology, ecology, distribution,
abundance, status, and trends of species
from a wide variety of sources as part
of their responsibility to implement the
Act. This information includes status
surveys, biological assessments, and
other unpublished material (that is,
‘‘gray literature’’) from State natural
resource agencies and natural heritage
programs, Tribal governments, other
Federal agencies, consulting firms,
contractors, and individuals associated
with professional organizations and
higher educational institutions. We also
use published articles from juried
professional journals. The reliability of
the information contained in these
sources can be as variable as the sources
themselves. As part of their routine
activities, our biologists are required to
gather, review, and evaluate information
from these sources prior to undertaking
listing, recovery, consultation, and
permitting actions.
Comment 104: If science-based and
commercial data are not available for
populations, then any projections for
populations in the United States based
on northern Mexican gartersnake
populations would necessarily be
speculative.
Our Response: The Act requires that
we use the best scientific and
commercial data available at the time of
listing. Appendix A (available at https://
www.regulations.gov, Docket No. FWS–
R2–ES–2013–0071) discusses such
considerations as the physical condition
of habitat, the composition of the
aquatic biological community, the
existence of significant threats, and the
length of time since the last known
observation of the subspecies in
presenting rationale for determining
occupancy status at each locality.
Comment 105: The Service’s
statement that as much as 90 percent of
historical populations in the United
States either occur at low densities or
are extirpated due to the total number
of stream miles that are now
permanently dewatered appears to be
pure speculation and not supported by
factual data. It is doubtful that an
accurate accounting exists of stream
miles in the United States that
historically supported the northern
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Mexican gartersnakes, and it is further
doubtful that an accurate accounting
exists of stream miles that historically
were perennial and are now ephemeral.
This kind of information would require
dealing with specific time periods and
specific stream reaches, which is not
offered in the statement.
Our Response: This assessment is
based on the best available scientific
and commercial data for northern
Mexican gartersnakes in the United
States. Museum records and habitat
requirements indicate the species
technically occurred in every county
and nearly every subbasin within
Arizona. We used GIS and information
on threats and status of historical
populations as well as habitat
preferences, in arriving at the 90 percent
figure, which we consider to be
reasonably accurate given the
information available. Considering the
large number of stream miles that were
historically perennial within the
historical distribution of the northern
Mexican gartersnake in Arizona that are
now ephemeral, and the degraded status
of populations as a result of a multitude
of threats, our presentation of the data
represents the most accurate possible.
Effect of Listing on Non-Federal
Interests
Comment 106: The language in the
proposed rule that lists activities which
could result in the reduction of the
distribution or abundance of important
gartersnake prey species, as well as
reduce the distribution and amount of
suitable physical habitat on a regional
landscape for the gartersnakes
themselves, is an invitation for many
organizations to sue the Service for
allowing activities deemed to affect the
gartersnake on a regional landscape
basis. This gives the gartersnakes’ prey
species endangered status under the Act
also.
Our Response: The Act and its
implementing regulations set forth a
series of general prohibitions and
exceptions that apply to all wildlife
listed under the ESA. The prohibitions
of section 9(a)(2) of the Act make it
illegal for any person subject to the
jurisdiction of the United States to take
(includes harass, harm, pursue, hunt,
shoot, wound, kill, trap, capture, or
collect; or to attempt any of these),
import, export, ship in interstate
commerce in the course of commercial
activity, or sell or offer for sale in
interstate or foreign commerce any
listed species.
We may issue permits to carry out
otherwise prohibited activities
involving endangered and threatened
wildlife species under certain
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circumstances. A permit must be issued
for the following purposes: For
scientific purposes, to enhance the
propagation or survival of the species,
and for incidental take in connection
with otherwise lawful activities.
It is our policy, as published in the
Federal Register on July 1, 1994 (59 FR
34272), to identify to the maximum
extent practicable at the time a species
is listed, those activities that would or
would not constitute a violation of
section 9 of the Act. The intent of this
policy is to increase public awareness of
the effect of a proposed listing on
proposed and ongoing activities within
the range of species proposed for listing.
See the Available Conservation
Measures section in the proposed rule
for a list of activities that could
potentially result in a violation of
section 9 of the Act. Lastly, it is
important to note that our emphasis for
the recovery of listed species is to assess
and improve ecosystem function as a
basic tenant of conservation biology;
this includes the physical habitat and
biological community where a listed
species occurs. This management
construct is not unique to these
gartersnakes.
Comment 107: Listing will hinder
conservation efforts of the New Mexico
Department of Game and Fish.
Our Response: We disagree. Once
these species are listed, funding for
recovery actions may be more accessible
from a variety of sources, including
Federal grants, State programs, and costshare grants for non-Federal
landowners, the academic community,
and nongovernmental organizations. In
addition, pursuant to section 6 of the
Act, the States of Arizona and New
Mexico will be eligible for Federal funds
to implement management actions that
promote the protection or recovery of
the narrow-headed and northern
Mexican gartersnakes.
Section 4(d) Rule
Comment 108: If the Service decides
to list the species, then we recommend
the development of a 4(d) rule to
exempt landowners from prohibitions of
take under section 9 of the Act for those
actions benefitting the two species of
gartersnakes, as was the case for the
Chiricahua leopard frog.
Our Response: We proposed a special
rule for the northern Mexican
gartersnake under section 4(d) of the Act
that would exempt take of northern
Mexican gartersnakes as a result of
livestock use at or maintenance of
livestock tanks located on non-Federal
lands, and a final 4(d) rule is
incorporated into this final rule. We do
not have the necessary information at
this time to determine that general
actions benefitting the two species of
gartersnakes would meet the standard of
a 4(d) rule to be necessary and advisable
for the conservation of the species. We
would need more specific information
regarding the actions under
consideration.
Comment 109: Concerned with the
language in the proposed 4(d) rule,
which states: ‘‘Incidental take of
northern Mexican gartersnakes is not a
violation of section 9 of the Act if it
occurs from any other otherwise legal
activities involving northern Mexican
gartersnakes and their habitat that are
conducted in accordance with
applicable State, Federal, tribal, and
local laws and regulations.’’ This
language could be interpreted to allow
incidental take for any activity in the
snake’s habitat as long as the activity
was legal. We suggest the following
language: (3) What activities are
allowed? Incidental take of northern
Mexican gartersnakes is not a violation
of section 9 of the Act if it occurs from
(a) otherwise legal activities involving
northern Mexican gartersnakes and their
habitat that are conducted in accordance
with applicable State, Federal, tribal,
and local laws and regulations, and (b)
such activities occurring in northern
Mexican gartersnake habitat pertain to
maintenance activities at livestock tanks
located on private, State, or tribal lands.
A livestock tank is an existing or future
impoundment in an ephemeral drainage
or upland site constructed primarily as
a watering site for livestock.
Our Response: We have amended the
4(d) rule, in the final rule, to reflect this
recommendation. We revised the
language in the 4(d) rule to better
describe our intention for the rule to
exempt only activities related to the
construction, use, and maintenance of
stock tanks for livestock watering. These
changes did not alter the scope of the
4(d) rule.
Determination—Standard for Review
Section 4 of the Act (16 U.S.C. 1533),
and its implementing regulations at 50
CFR part 424, set forth the procedures
for adding species to the Federal Lists
of Endangered and Threatened Wildlife
and Plants. Under section 4(a)(1) of the
Act, we may list a species based on (A)
The present or threatened destruction,
modification, or curtailment of its
habitat or range; (B) Overutilization for
commercial, recreational, scientific, or
educational purposes; (C) Disease or
predation; (D) The inadequacy of
existing regulatory mechanisms; or (E)
Other natural or manmade factors
affecting its continued existence. Listing
actions may be warranted based on any
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of the above threat factors, singly or in
combination.
Until recently the Service has
presented its evaluation of information
under the five listing factors in an
outline format, discussing all of the
information relevant to any given factor
and providing a factor-specific
conclusion before moving to the next
factor. However, the Act does not
require findings under each of the
factors, only an overall determination as
to the species’ status (for example,
threatened, endangered, or not
warranted). Ongoing efforts to improve
the efficiency and efficacy of the
Service’s implementation of the Act
have led us to present this information
in a different format that we believe
leads to greater clarity in our
understanding of the science, its
uncertainties, and our application of our
statutory framework to that science.
Therefore, while the presentation of
information in this rule differs from past
practice, it differs in format only. We
have evaluated the same body of
information we would have evaluated
under the five listing factors outline
format in the past, we are applying the
same information standard, and we are
applying the same statutory framework
in reaching our conclusions.
Determination for Northern Mexican
Gartersnake
The Act defines an endangered
species as any species (or subspecies)
that is ‘‘in danger of extinction
throughout all or a significant portion of
its range’’ and a threatened species as
any species ‘‘that is likely to become
endangered throughout all or a
significant portion of its range within
the foreseeable future.’’ We have
carefully assessed the best scientific and
commercial information available
regarding the status of the northern
Mexican gartersnake and have
determined that this subspecies meets
the definition of a threatened subspecies
under the Act based on its current status
and the future threats to the subspecies.
We find that the northern Mexican
gartersnake is not currently in danger of
extinction because it remains extant in
most of the subbasins where it
historically occurred, and its known
threats have not yet resulted in
substantial range reduction or a
substantial number of population
extirpations to put the subspecies on the
brink of extinction. Currently, only 6
former United States populations were
found to be likely extirpated, and 29
populations are believed to remain
extant. Therefore, we determined that
the present risk of extinction is not
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sufficient to warrant a finding of
endangered under the Act.
However, the northern Mexican
gartersnake has undergone declines in
its abundance, and we found only 5 of
29 current populations in the United
States are likely viable into the
foreseeable future, or what we consider
to be the next several decades. While we
are not able to quantify the status of all
populations in Mexico, based on the
threats and the declining status of
aquatic communities there, we assume a
similar status in the Mexican portion of
its range. We expect the status of the
subspecies will decline in the next
several decades mainly as a result of the
continuing and expanding impacts of
harmful nonnative species and the
increasing nature of threats associated
with human population growth and
climate change. As the effects of these
threats escalate on the landscape (as
summarized below), we expect that
additional populations will be
extirpated, and that the northern
Mexican gartersnake will be in danger of
extinction in the foreseeable future.
In our review of the best available
scientific and commercial information,
we found that aquatic ecosystems upon
which the northern Mexican gartersnake
relies have been significantly degraded
by the introduction and proliferation of
harmful nonnative species (Factors C
and E). Harmful nonnative species
(mainly predatory fishes, bullfrogs, and
crayfish) have been intentionally
released or have naturally moved into
nearly every subbasin throughout the
range of the northern Mexican
gartersnake. This has resulted in
widespread declines in native fish and
amphibian communities, which are
integral to the continued survival of the
northern Mexican gartersnake because
they serve as their primary food source.
Harmful nonnative species have
indirectly impacted northern Mexican
gartersnakes by predation on their prey
base (native fish and amphibians) and
have directly impacted them through
preying on young gartersnakes (Factor
B), which impacts gartersnake
populations through declines in the
recruitment of young snakes into the
reproductive age class. In combination,
these factors have resulted in
population declines, range restrictions
within subbasins, and some population
extirpations. We found the threat related
to harmful nonnative species to be the
most significant and pervasive of all
threats affecting the subspecies.
Additional threats to the habitat of
northern Mexican gartersnakes include
water use activities, climate change, and
drought (Factor A). Dams, water
diversions, flood-control projects, and
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groundwater pumping have dewatered
entire reaches of historically occupied
habitat in some areas. The rapidly
growing human population in the arid
southwestern United States, combined
with a drought-limited supply of surface
water, will further increase future needs
for water supplies and associated
infrastructure (dams, diversions, and
groundwater pumping) that will also
contribute to habitat losses in the next
several decades. Losses of aquatic
habitats are also expected due to the
impacts of climate change, which
includes increased aridity, lower annual
precipitation totals, lower snow pack
levels, higher variability in flows (lower
low-flows and higher high-flows) in the
southwestern United States and
northern Mexico. The population-level
effect of factors that modify or destroy
the physical attributes of gartersnake
habitat is amplified when they act in the
presence of harmful nonnative species.
Other factors act in combination to
negatively affect the northern Mexican
gartersnake, including mismanaged or
unmanaged livestock grazing (Mexico;
Factor A); road construction, use, and
maintenance (Factor A); adverse human
interactions (Factor E); environmental
contaminants (Factor A); erosion control
techniques (Factor A); and possible
competitive pressures from sympatric
species (Factor E). These threats occur
within the distribution of this
gartersnake and contribute to further
population declines or extirpations
where gartersnakes already occur at low
population densities due to the impacts
of harmful nonnative species. The
existing regulatory mechanisms
currently in place (Factor D) do not
target the conservation of this
subspecies or its habitat in the United
States or Mexico.
Therefore, on the basis of the best
available scientific and commercial
information, we find the northern
Mexican gartersnake is likely to become
in danger of extinction throughout all of
its range within the foreseeable future,
and we are listing the northern Mexican
gartersnake as a threatened subspecies
in accordance with sections 3(20) and
4(a)(1) of the Act.
Determination for Narrow-Headed
Gartersnakes
The Act defines an endangered
species as any species that is ‘‘in danger
of extinction throughout all or a
significant portion of its range’’ and a
threatened species as any species ‘‘that
is likely to become endangered
throughout all or a significant portion of
its range within the foreseeable future.’’
We have carefully assessed the best
scientific and commercial information
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available regarding the status of the
narrow-headed gartersnake and have
determined that this species meets the
definition of a threatened subspecies
under the Act based on its current status
and the future threats to the species.
We find that the narrow-headed
gartersnake is not currently in danger of
extinction because it remains extant in
most of the subbasins where it
historically occurred, and its known
threats have not yet resulted in
substantial range reduction or a
substantial number of population
extirpations to put the species on the
brink of extinction. Currently, only 5
former populations were found to be
likely extirpated, and 36 populations are
believed to remain extant. Therefore, we
determined that the present risk of
extinction is not sufficient to warrant a
finding of endangered under the Act.
However, the narrow-headed
gartersnake has undergone declines in
its abundance, and we found only 5 of
36 current populations are likely viable
into the foreseeable future, or what we
consider to be the next several decades.
We expect the status of the species will
decline in the next several decades
mainly as a result of the continuing and
expanding impacts of harmful
nonnative species and the increasing
nature of threats associated with human
population growth and climate change.
As the effects of these threats escalate
on the landscape (as summarized
below), we expect that additional
populations will be extirpated, and that
the narrow-headed gartersnake will be
in danger of extinction in the
foreseeable future.
In our review of the best available
scientific and commercial information,
we found that native fish communities,
upon which the narrow-headed
gartersnake relies heavily, have been
significantly degraded by the
introduction and proliferation of
harmful nonnative species (Factors C
and E). Harmful nonnative species
(mainly predatory fishes, bullfrogs, and
crayfish) have been intentionally
released or have naturally moved into
nearly every subbasin throughout the
range of the narrow-headed gartersnake.
This has resulted in widespread
declines in native fish communities,
which are integral to the continued
survival of the narrow-headed
gartersnake because they serve as their
primary food source. Harmful nonnative
species have indirectly impacted
narrow-headed gartersnakes by
predation on their prey base (native
fish) and have directly impacted them
through preying on young gartersnakes
(Factor B), which impacts gartersnake
populations through the decline in
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recruitment of young snakes into the
reproductive age class. In combination,
these factors have resulted in
population declines, range restrictions
within subbasins, and some population
extirpations. We found the threat related
to harmful nonnative species to be the
most significant and pervasive of all
threats affecting the species.
Additional threats to the habitat of
narrow-headed gartersnakes include
water use activities, climate change, and
wildfires (Factor A). Dams, water
diversions, flood-control projects, and
groundwater pumping have dewatered
entire reaches of historically occupied
habitat in some areas. The rapidly
growing human population in the arid
southwestern United States, combined
with a drought-limited supply of surface
water, will further increase future needs
for water supplies and associated
infrastructure (dams, diversions, and
groundwater pumping) that will also
contribute to habitat losses in the next
several decades. Losses of aquatic
habitats are also expected due to the
impacts of climate change, which
includes increased aridity, lower annual
precipitation totals, lower snow pack
levels, higher variability in flows (lower
low-flows and higher high-flows), and
enhanced stress on ponderosa pine
communities in the southwestern
United States. Wildfires in the arid
southwestern United States have grown
more frequent and severe, due in part to
the fire management policies of past
decades. High-intensity wildfires that
affect large areas contribute to
significant flooding and sedimentation,
resulting in fish kills and the filling-in
of interstitial spaces in river cobble,
which the species uses for hunting fish),
as well as important pool habitat. These
impacts negatively affect the fish and
amphibian prey base for narrow-headed
gartersnakes for extended periods of
time. The frequency and intensity of
large wildfires is likely to increase in
the foreseeable future as an indirect
effect of drier and hotter landscape
conditions associated with climate
change. The population-level effect of
factors that modify or destroy the
physical attributes of gartersnake habitat
is amplified when they act in the
presence of harmful nonnative species.
Other factors act in combination to
negatively affect the narrow-headed
gartersnake, including road
construction, use, and maintenance
(Factor A); adverse human interactions
(Factor E); environmental contaminants
(Factor A); and erosion control
techniques (Factor A). These threats
occur within the distribution of this
gartersnake and contribute to further
population declines or extirpations
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where gartersnakes already occur at low
population densities due to the impacts
of harmful nonnative species. The
existing regulatory mechanisms
currently in place (Factor D) do not
target the conservation of this species or
its habitat.
Therefore, on the basis of the best
available scientific and commercial
information, we find the narrow-headed
gartersnake is likely to become in
danger of extinction throughout all of its
range within the foreseeable future, and
we are listing the narrow-headed
gartersnake as a threatened species in
accordance with sections 3(20) and
4(a)(1) of the Act.
Available Conservation Measures
Conservation measures provided to
species listed as endangered or
threatened under the Act include
recognition, recovery actions,
requirements for Federal protection, and
prohibitions against certain practices.
Recognition through listing results in
public awareness and conservation by
Federal, State, Tribal, and local
agencies, private organizations, and
individuals. The Act encourages
cooperation with the States and requires
that recovery actions be carried out for
all listed species. The protection
required by Federal agencies and the
prohibitions against certain activities
are discussed, in part, below.
The primary purpose of the Act is the
conservation of endangered and
threatened species and the ecosystems
upon which they depend. The ultimate
goal of such conservation efforts is the
recovery of these listed species, so that
they no longer need the protective
measures of the Act. Subsection 4(f) of
the Act requires the Service to develop
and implement recovery plans for the
conservation of endangered and
threatened species. The recovery
planning process involves the
identification of actions that are
necessary to halt or reverse the species’
decline by addressing the threats to its
survival and recovery. The goal of this
process is to restore listed species to a
point where they are secure, selfsustaining, and functioning components
of their ecosystems.
Recovery planning includes the
development of a recovery outline
shortly after a species is listed,
preparation of a draft and final recovery
plan, and revisions to the plan as
significant new information becomes
available. The recovery outline guides
the immediate implementation of urgent
recovery actions and describes the
process to be used to develop a recovery
plan. The recovery plan identifies sitespecific management actions that will
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38743
achieve recovery of the species,
measurable criteria that determine when
a species may be downlisted or delisted,
and methods for monitoring recovery
progress. Recovery plans also establish
a framework for agencies to coordinate
their recovery efforts and provide
estimates of the cost of implementing
recovery tasks. Recovery teams
(composed of species experts, Federal
and State agencies, nongovernmental
organizations, and stakeholders) are
often established to develop recovery
plans. When completed, the recovery
outline, draft recovery plan, and the
final recovery plan will be available on
our Web site (https://www.fws.gov/
endangered), or from our Arizona
Ecological Services Field Office (see FOR
FURTHER INFORMATION CONTACT).
Implementation of recovery actions
generally requires the participation of a
broad range of partners, including other
Federal agencies, States, Tribal,
nongovernmental organizations,
businesses, and private landowners.
Examples of recovery actions include
habitat restoration (e.g., restoration of
native vegetation), research, captive
propagation and reintroduction, and
outreach and education. The recovery of
many listed species cannot be
accomplished solely on Federal lands
because their range may occur primarily
or solely on non-Federal lands. To
achieve recovery of these species
requires cooperative conservation efforts
on private, State, and Tribal lands.
Following publication of this final
listing rule, funding for recovery actions
will be available from a variety of
sources, including Federal budgets,
State programs, and cost-share grants for
non-Federal landowners, the academic
community, and nongovernmental
organizations. In addition, under section
6 of the Act, the States of Arizona and
New Mexico would be eligible for
Federal funds to implement
management actions that promote the
protection and recovery of the northern
Mexican and narrow-headed
gartersnakes. Information on our grant
programs that are available to aid
species recovery can be found at: https://
www.fws.gov/grants.
Please let us know if you are
interested in participating in recovery
efforts for these species. Additionally,
we invite you to submit any new
information on these species whenever
it becomes available and any
information you may have for recovery
planning purposes (see FOR FURTHER
INFORMATION CONTACT).
Section 7(a) of the Act requires
Federal agencies to evaluate their
actions with respect to any species that
is proposed or listed as endangered or
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threatened and with respect to its
critical habitat, if any is designated.
Regulations implementing this
interagency cooperation provision of the
Act are codified at 50 CFR part 402.
Section 7(a)(4) of the Act requires
Federal agencies to confer with the
Service on any action that is likely to
jeopardize the continued existence of a
species proposed for listing or result in
destruction or adverse modification of
proposed critical habitat. If a species is
listed subsequently, section 7(a)(2) of
the Act requires Federal agencies to
ensure that activities they authorize,
fund, or carry out are not likely to
jeopardize the continued existence of
the species or destroy or adversely
modify its critical habitat. If a Federal
action may affect a listed species or its
critical habitat, the responsible Federal
agency must enter into formal
consultation with the Service.
Federal agency actions within the
species’ habitats that may require
conference or consultation or both as
described in the preceding paragraph
include management and any other
landscape-altering activities on Federal
lands administered by the Fish and
Wildlife Service, U.S. Bureau of
Reclamation, or U.S. Forest Service;
issuance of section 404 Clean Water Act
permits by the U.S. Army Corps of
Engineers; construction and
management of gas pipeline and power
line rights-of-way by the Federal Energy
Regulatory Commission; construction
and maintenance of roads or highways
by the Federal Highway Administration;
and other discretionary actions that
affect the species composition of biotic
communities where these species or
their habitats occur, such as funding or
permitting programs that result in the
continued stocking of nonnative,
predatory fish.
The Act and its implementing
regulations set forth a series of general
prohibitions and exceptions that apply
to all endangered wildlife. The
prohibitions of section 9(a)(2) of the Act,
codified at 50 CFR 17.21 for endangered
wildlife, in part, make it illegal for any
person subject to the jurisdiction of the
United States to take (includes harass,
harm, pursue, hunt, shoot, wound, kill,
trap, capture, or collect; or to attempt
any of these), import, export, ship in
interstate commerce in the course of
commercial activity, or sell or offer for
sale in interstate or foreign commerce
any listed species. Under the Lacey Act
(18 U.S.C. 42–43; 16 U.S.C. 3371–3378),
it is also illegal to possess, sell, deliver,
carry, transport, or ship any such
wildlife that has been taken illegally.
Certain exceptions apply to agents of the
Service and State conservation agencies.
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The prohibitions of section 9(a)(2) of the
Act, codified at 50 CFR 17.31 for
threatened wildlife, make it such that all
the provisions of 50 CFR 17.21 apply,
except § 17.21(c)(5).
We may issue permits to carry out
otherwise prohibited activities
involving endangered and threatened
wildlife species under certain
circumstances. Regulations governing
permits are codified at 50 CFR 17.22 for
endangered species, and at § 17.32 for
threatened species. A permit must be
issued for the following purposes: For
scientific purposes, to enhance the
propagation or survival of the species,
and for incidental take in connection
with otherwise lawful activities.
It is our policy, as published in the
Federal Register on July 1, 1994 (59 FR
34272), to identify to the maximum
extent practicable at the time a species
is listed, those activities that would or
would not constitute a violation of
section 9 of the Act. The intent of this
policy is to increase public awareness of
the effect of a proposed listing on
proposed and ongoing activities within
the range of species proposed for listing.
The following activities could
potentially result in a violation of
section 9 of the Act; this list is not
comprehensive:
(1) Unauthorized collecting, handling,
possessing, selling, delivering, carrying,
or transporting of the species, including
import or export across State lines and
international boundaries, except for
properly documented antique
specimens of these taxa at least 100
years old, as defined by section 10(h)(1)
of the Act;
(2) The unauthorized introduction of
harmful nonnative species that compete
with or prey upon northern Mexican
and narrow-headed gartersnakes or their
prey species, such as the stocking of
nonnative, predatory fish, or illegal
transport, use, or release of bullfrogs or
crayfish in the States of Arizona and
New Mexico;
(3) The unauthorized release of
biological control agents that attack any
age class of northern Mexican and
narrow-headed gartersnakes or any life
stage of their prey species;
(4) Unauthorized modification of the
channel, reduction or elimination of
water flow of any stream or water body,
or the complete removal or significant
destruction of riparian vegetation
associated with occupied northern
Mexican or narrow-headed gartersnake
habitat; and
(5) Unauthorized discharge of
chemicals or fill material into any
waters in which northern Mexican and
narrow-headed gartersnakes are known
to occur.
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Questions regarding whether specific
activities would constitute a violation of
section 9 of the Act should be directed
to the Arizona Ecological Services Field
Office (see FOR FURTHER INFORMATION
CONTACT). Requests for copies of the
regulations concerning listed animals
and general inquiries regarding
prohibitions and permits may be
addressed to the U.S. Fish and Wildlife
Service, Endangered Species Permits,
P.O. Box 1306, Albuquerque, New
Mexico 87103 (telephone (505) 248–
6920, facsimile (505) 248–6922).
Rule for the Northern Mexican
Gartersnake Under Section 4(d) of the
Act
The Act does not specify particular
prohibitions, or exceptions to those
prohibitions, for threatened species.
Instead, under section 4(d) of the Act,
the Secretary of the Interior has the
discretion to issue such regulations as
she deems necessary and advisable to
provide for the conservation of such
species. The Secretary also has the
discretion to prohibit by regulation with
respect to any threatened species, any
act prohibited under section 9(a)(1) of
the Act. Exercising this discretion, the
Service developed general prohibitions
(50 CFR 17.31) and exceptions to those
prohibitions (50 CFR 17.32) under the
Act that apply to most threatened
species. Alternately, for other
threatened species, the Service may
develop specific prohibitions and
exceptions that are tailored to the
specific conservation needs of the
species. In such cases, some of the
prohibitions and authorizations under
50 CFR 17.31 and 17.32 may be
appropriate for the species and
incorporated into a rule under section
4(d) of the Act. However, these rules,
known as 4(d) rules, will also include
provisions that are tailored to the
specific conservation needs of the
threatened species and may be more or
less restrictive than the general
provisions at 50 CFR 17.31.
Provisions of the Section 4(d) Rule
Under section 4(d) of the Act, the
Secretary may promulgate a special rule
that modifies the standard protections
for threatened species with measures
tailored to the conservation of the
species that are determined to be
necessary and advisable. Under this 4(d)
rule, all of the prohibitions under 50
CFR 17.31 and 17.32 will apply to the
northern Mexican gartersnake, except as
discussed below. The 4(d) rule will not
remove or alter in any way the
consultation requirements under section
7 of the Act.
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The creation, use, and maintenance of
stock tanks are important components of
livestock grazing in the southwestern
United States. A stock tank (or livestock
tank) is defined as an existing or future
impoundment in an ephemeral drainage
or upland site (as opposed to an active
stream channel) constructed primarily
as a watering site for livestock. Wellmanaged stock tanks can provide
important habitats for northern Mexican
gartersnakes and their prey base,
especially when the tank: (1) Remains
devoid of harmful nonnative species
while supporting native prey species;
(2) provides adequate vegetation cover
for predator aversion and prey base
support; and (3) provides reliable water
sources in periods of prolonged drought.
However, to create or maintain these
physical attributes of well-managed
tanks, management and maintenance
can be necessary, which may have
temporary negative effects to these
habitat attributes, but also long-term
beneficial effects to wildlife, including
the northern Mexican gartersnake and
its prey. Therefore, the management of
stock tanks is an important
consideration for northern Mexican
gartersnakes.
The 4(d) rule allows for use of stock
tanks by livestock and construction,
continued use, and maintenance of
those stock tanks. Stock tanks provide
habitat for northern Mexican
gartersnakes, and thus their presence
within the gartersnake’s range provides
a conservation benefit to the species.
This 4(d) rule allows landowners to
construct new stock tanks and to
continue to use and maintain those
stock tanks on non-Federal lands
without the need for Federal permitting
or oversight regarding compliance with
the Act.
This provision may result in some
harm or disturbance of individual
northern Mexican gartersnakes as a
result of livestock or human activities at
the stock tanks; however, the level of
disturbance is expected to be minimal
and outweighed by the benefit to the
species from the presence of these
habitats that are provided by stock
tanks.
Given the benefits of well-managed
stock tanks, the presence of wellmanaged stock tanks are an important
component to northern Mexican
gartersnake conservation and recovery.
This stock tank provision in the 4(d)
rule allows for construction, continued
use, and maintenance of stock tanks on
non-Federal lands, and, therefore,
because of the benefits associated with
the habitat provided by well-managed
stock tanks, the 4(d) rule is necessary
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and advisable for the conservation of the
northern Mexican gartersnake.
Nothing in this 4(d) rule changes in
any way the recovery planning
provisions of section 4(f) and
consultation requirements under section
7 of the Act or the ability of the Service
to enter into partnerships for the
management and protection of the
northern Mexican gartersnake. Livestock
use and maintenance of stock tanks on
Federal lands will be addressed through
the section 7 consultation process; this
4(d) rule applies only to non-Federal
lands.
4(d) Rule Determination
Section 4(d) of the Act states that ‘‘the
Secretary shall issue such regulations as
she deems necessary and advisable to
provide for the conservation’’ of species
listed as a threatened species.
Conservation is defined in the Act to
mean ‘‘to use and the use of all methods
and procedures which are necessary to
bring any endangered species or
threatened species to the point at which
the measures provided pursuant to (the
Act) are no longer necessary.’’
Additionally, section 4(d) states that the
Secretary ‘‘may by regulation prohibit
with respect to any threatened species
any act prohibited under section
9(a)(1).’’
The courts have recognized the extent
of the Secretary’s discretion under this
standard to develop rules that are
appropriate for the conservation of a
species. For example, the Secretary may
find that it is necessary and advisable
not to include a taking prohibition, or to
include a limited taking prohibition. See
Alsea Valley Alliance v. Lautenbacher,
2007 U.S. Dist. Lexis 60203 (D. Or.
2007); Washington Environmental
Council v. National Marine Fisheries
Service, and 2002 U.S. Dist. Lexis 5432
(W.D. Wash. 2002). In addition, as
affirmed in State of Louisiana v. Verity,
853 F.2d 322 (5th Cir. 1988), the rule
need not address all the threats to the
species. As noted by Congress when the
Act was initially enacted, ‘‘once an
animal is on the threatened list, the
Secretary has an almost infinite number
of options available to her with regard
to the permitted activities for those
species.’’ She may, for example, permit
taking, but not importation of such
species, or she may choose to forbid
both taking and importation but allow
the transportation of such species, as
long as the measures will ‘‘serve to
conserve, protect, or restore the species
concerned in accordance with the
purposes of the Act’’ (H.R. Rep. No. 412,
93rd Cong., 1st Sess. 1973).
Section 9 prohibitions make it illegal
for any person subject to the jurisdiction
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Fmt 4701
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38745
of the United States to take (including
harass, harm, pursue, shoot, wound,
kill, trap, capture, or collect; or attempt
any of these), import or export, ship in
interstate commerce in the course of
commercial activity, or sell or offer for
sale in interstate or foreign commerce
any wildlife species listed as an
endangered species, without written
authorization. It also is illegal under
section 9(a)(1) of the Act to possess, sell,
deliver, carry, transport, or ship any
such wildlife that is taken illegally.
Prohibited actions consistent with
section 9 of the Act are outlined for
threatened species in 50 CFR 17.31(a)
and (b). This 4(d) rule applies all of the
prohibitions in 50 CFR 17.31(a) and (b)
to the northern Mexican gartersnake,
except activities on non-Federal lands
that are incidental to construction,
continued use, and maintenance of
stock tanks. Based on the rationale
explained above, the provisions
included in this 4(d) rule are expected
to contribute to the conservation of the
northern Mexican gartersnake and are,
therefore, necessary and advisable to
provide for the conservation of the
northern Mexican gartersnake.
Required Determinations
National Environmental Policy Act (42
U.S.C. 4321 et seq.)
We have determined that
environmental assessments and
environmental impact statements, as
defined under the authority of NEPA,
need not be prepared in connection
with listing a species as an endangered
or threatened species under the Act. We
published a notice outlining our reasons
for this determination in the Federal
Register on October 25, 1983 (48 FR
49244). As documented in the Service’s
Endangered Species Listing Handbook
(Service 1994), it is the position of the
Service that rules promulgated under
section 4(d) of the Act concurrently
with listing of the species fall under the
same rationale as outlined in the
October 25, 1983, determination; thus
preparation of an environmental
assessment for the 4(d) rule is not
required.
Government-to-Government
Relationship With Tribes
In accordance with the President’s
memorandum of April 29, 1994
(Government-to-Government Relations
with Native American Tribal
Governments; 59 FR 22951), Executive
Order 13175 (Consultation and
Coordination with Indian Tribal
Governments), and the Department of
the Interior’s manual at 512 DM 2, we
readily acknowledge our responsibility
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to communicate meaningfully with
recognized Federal Tribes on a
government-to-government basis. In
accordance with Secretarial Order 3206
of June 5, 1997 (American Indian Tribal
Rights, Federal-Tribal Trust
Responsibilities, and the Endangered
Species Act), we readily acknowledge
our responsibilities to work directly
with tribes in developing programs for
healthy ecosystems, to acknowledge that
tribal lands are not subject to the same
controls as Federal public lands, to
remain sensitive to Indian culture, and
to make information available to tribes.
Native American tribes potentially
affected by the listing of these two
gartersnakes include the San Carlos
Apache Tribe, White Mountain Apache
Tribe, and Yavapai Apache Tribe. On
March 12, 2013, we mailed
correspondence to these three tribes to
request to meet with each tribe to
discuss our listing recommendations for
the gartersnakes. We met with
representatives of the San Carlos
Apache Tribe on May 1, 2013, and no
concerns regarding the proposed listings
were noted. We held a government-to-
government meeting with the White
Mountain Apache Tribe on September
27, 2013, to discuss the gartersnake
listing recommendations, and we agreed
to review their Native Fish Management
Plan for conservation benefit to
proposed and listed aquatic vertebrate
species that occur on their lands. We
provided comments on that plan during
a conference call discussion on
December 16, 2013. The Yavapai
Apache Tribe did not have any
comments on the proposed gartersnake
listings.
References Cited
A complete list of references cited in
this rulemaking is available on the
Internet at https://www.regulations.gov
and upon request from the Arizona
Ecological Services Field Office (see FOR
FURTHER INFORMATION CONTACT).
Authors
The primary authors of this final rule
are the staff members of the Arizona
Ecological Services Field Office.
Species
Historic range
Common name
Scientific name
*
*
Vertebrate population where
endangered or
threatened
*
*
Status
List of Subjects in 50 CFR Part 17
Endangered and threatened species,
Exports, Imports, Reporting and
recordkeeping requirements,
Transportation.
Regulation Promulgation
Accordingly, we amend part 17,
subchapter B of chapter I, title 50 of the
Code of Federal Regulations, as follows:
PART 17—[AMENDED]
1. The authority citation for part 17
continues to read as follows:
■
Authority: 16 U.S.C. 1361–1407; 1531–
1544; and 4201–4245, unless otherwise
noted.
2. Amend § 17.11(h) by adding entries
for ‘‘Gartersnake, narrow-headed’’ and
‘‘Gartersnake, northern Mexican’’ to the
List of Endangered and Threatened
Wildlife in alphabetical order under
Reptiles to read as follows:
■
§ 17.11 Endangered and threatened
wildlife.
*
*
*
(h) * * *
*
Critical
habitat
When listed
*
*
*
Special rules
*
Reptiles.
*
Gartersnake, narrowheaded.
Gartersnake, northern Mexican.
*
Thamnophis
rufipunctatus.
Thamnophis eques
megalops.
*
Special rules—reptiles.
*
*
*
*
*
(g) Northern Mexican gartersnake
(Thamnophis eques megalops). (1)
Prohibitions. Except as noted in
paragraph (g)(2) of this section, all
prohibitions and provisions of §§ 17.31
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*
T ..................
.....................
NA ...............
*
NA.
U.S.A. (AZ,
NM), Mexico.
Entire ................
T ..................
.....................
NA ...............
17.42(g).
*
3. Amend § 17.42 by adding a new
paragraph (g) to read as follows:
VerDate Mar<15>2010
*
Entire ................
*
■
§ 17.42
*
U.S.A. (AZ, NM)
17:11 Jul 07, 2014
Jkt 232001
*
*
and 17.32 apply to the northern
Mexican gartersnake.
(2) Exemptions from prohibitions.
Incidental take of the northern Mexican
gartersnake will not be considered a
violation of section 9 of the Act if the
take occurs on non-Federal land and is
incidental to activities pertaining to
construction, continued use, and
maintenance of stock tanks. A stock
tank is an existing or future
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*
Sfmt 9990
*
*
impoundment in an ephemeral drainage
or upland site constructed primarily as
a watering site for livestock.
Dated: June 9, 2014.
Stephen Guertin,
Acting Director, U.S. Fish and Wildlife
Service.
[FR Doc. 2014–14615 Filed 7–7–14; 8:45 am]
BILLING CODE 4310–55–P
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[Federal Register Volume 79, Number 130 (Tuesday, July 8, 2014)]
[Rules and Regulations]
[Pages 38677-38746]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: 2014-14615]
[[Page 38677]]
Vol. 79
Tuesday,
No. 130
July 8, 2014
Part II
Department of the Interior
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Fish and Wildlife Service
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50 CFR Part 17
Endangered and Threatened Wildlife and Plants; Threatened Status for
the Northern Mexican Gartersnake and Narrow-Headed Gartersnake; Final
Rule
Federal Register / Vol. 79 , No. 130 / Tuesday, July 8, 2014 / Rules
and Regulations
[[Page 38678]]
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DEPARTMENT OF THE INTERIOR
Fish and Wildlife Service
50 CFR Part 17
[Docket No. FWS-R2-ES-2013-0071: 4500030113]
RIN 1018-AY23
Endangered and Threatened Wildlife and Plants; Threatened Status
for the Northern Mexican Gartersnake and Narrow-Headed Gartersnake
AGENCY: Fish and Wildlife Service, Interior.
ACTION: Final rule.
-----------------------------------------------------------------------
SUMMARY: We, the U.S. Fish and Wildlife Service (Service), determine
threatened species status under the Endangered Species Act of 1973
(Act), as amended, for the northern Mexican gartersnake (Thamnophis
eques megalops) and the narrow-headed gartersnake (Thamnophis
rufipunctatus), native species from Arizona and New Mexico in the
United States. We also finalize a rule under authority of section 4(d)
of the Endangered Species Act of 1973, as amended (Act), that provides
measures that are necessary and advisable to provide for the
conservation of the northern Mexican gartersnake. Both species are
listed as threatened throughout their range, which, for the northern
Mexican gartersnake, also includes the Mexican states of Sonora,
Chihuahua, Durango, Coahuila, Zacatecas, Guanajuato, Nayarit, Hidalgo,
Jalisco, San Luis Potos[iacute], Aguascalientes, Tlaxacala, Puebla,
M[eacute]xico, Veracruz, and Quer[eacute]taro. The effect of this
regulation will be to add these species to the lists of Endangered and
Threatened Wildlife and Plants.
DATES: This rule becomes effective August 7, 2014.
ADDRESSES: This final rule is available on the internet at https://www.regulations.gov (Docket No. FWS-R2-ES-2013-0071) and https://www.fws.gov/southwest/es/arizona. Comments and materials we received,
as well as supporting documentation we used in preparing this rule, are
available for public inspection at https://www.regulations.gov. All of
the comments, materials, and documentation that we considered in this
rulemaking are available by appointment, during normal business hours
at: U.S. Fish and Wildlife Service, Arizona Ecological Services Field
Office, 2321 West Royal Palm Road, Suite 103, Phoenix, AZ 85021;
telephone: 602-242-0210; facsimile: 602-242-2513.
FOR FURTHER INFORMATION CONTACT: Steve Spangle, Field Supervisor, U.S.
Fish and Wildlife Service, Arizona Ecological Services Field Office,
2321 West Royal Palm Road, Suite 103, Phoenix, AZ 85021; telephone:
602-242-0210; facsimile: 602-242-2513. Persons who use a
telecommunications device for the deaf (TDD) may call the Federal
Information Relay Service (FIRS) at 800-877-8339.
SUPPLEMENTARY INFORMATION:
Executive Summary
Why we need to publish a rule. Under the Endangered Species Act, a
species may warrant protection through listing if it is endangered or
threatened throughout all or a significant portion of its range.
Listing a species as an endangered or threatened species requires
issuing a rule. This rule will finalize the listing of the northern
Mexican gartersnake (Thamnophis eques megalops) and narrow-headed
gartersnake (Thamnophis rufipunctatus) as threatened species, initiated
with our proposed listing rule published on July 10, 2013 (78 FR
41500), and finalize a rule under authority of section 4(d) of the Act
that provides measures that are necessary and advisable to provide for
the conservation of the northern Mexican gartersnake.
The basis for our action. Under the Endangered Species Act, we can
determine that a species is an endangered or threatened species based
on any of five factors: (A) The present or threatened destruction,
modification, or curtailment of its habitat or range; (B)
Overutilization for commercial, recreational, scientific, or
educational purposes; (C) Disease or predation; (D) The inadequacy of
existing regulatory mechanisms; or (E) Other natural or manmade factors
affecting its continued existence. We have determined that predation
from and competition with nonnative species such as bass (Micropterus
sp.), flathead catfish (Pylodictis sp.), channel catfish (Ictalurus
sp.), Chihuahuan catfish (Ictalurus chihuahua), bullheads (Ameiurus
sp.), sunfish (Lepomis sp.), and crappie (Pomoxis sp.), brown trout
(Salmo trutta), American bullfrogs (Lithobates catesbeiana), and
crayfish (northern (virile) crayfish (Orconectes virilis) and red swamp
crayfish (Procambarus clarkia)) are the most significant threat
affecting these gartersnakes across their range. Throughout the
remainder of this final rule, the nonnative species identified
immediately above will be referred to collectively as ``harmful
nonnative species.'' Large-scale wildfires and land uses that divert,
dry up, or significantly pollute aquatic habitat have also been found
to be significant threats. Collectively, these threats have adversely
affected gartersnake populations, and most of their native prey
species, such that the gartersnakes' resiliency, redundancy, and
representation across their ranges have been significantly compromised.
Peer review and public comment. We sought comments from independent
specialists to ensure that our designation is based on scientifically
sound data, assumptions, and analyses. We invited these peer reviewers
to comment on our listing proposal. We also considered all other
comments and information received during the comment period on the
proposed listing rule. All comments are available at https://www.regulations.gov (Docket No. FWS-R2-ES-2013-0071).
Previous Federal Action
Please refer to the proposed listing rule for the northern Mexican
gartersnake and narrow-headed gartersnake (78 FR 41500; July 10, 2013)
for a detailed description of previous Federal actions concerning this
species.
We will also be finalizing the designation of critical habitat for
the northern Mexican gartersnake and narrow-headed gartersnake in a
separate rule in the future. Information regarding designation of
critical habitat for these species is available at https://www.regulations.gov (Docket No. FWS-R2-ES-2013-0022).
Background
Northern Mexican Gartersnake
Subspecies Description
The northern Mexican gartersnake ranges in color from olive to
olive-brown or olive-gray with three lighter-colored stripes that run
the length of the body, the middle of which darkens toward the tail.
This species may inhabit the same area as other native gartersnake
species and can be difficult for people without specific expertise to
identify. The snake may reach a maximum known length of 44 inches (in)
(112 centimeters (cm)). The pale yellow to light-tan lateral (side of
body) stripes distinguish the northern Mexican gartersnake from other
sympatric (co-occurring) gartersnake species because a portion of the
lateral stripe is found on the fourth scale row, while it is confined
to lower scale rows for other species. Paired black spots extend along
the olive dorsolateral fields (region adjacent to the top of the
[[Page 38679]]
snake's back) and the olive-gray ventrolateral fields (region adjacent
to the area of the snake's body in contact with the ground). The scales
are keeled (possessing a ridge down the center of each scale). A more
detailed subspecies description can be found in our September 26, 2006
(71 FR 56227), or November 25, 2008 (73 FR 71788) 12-month findings for
this subspecies, or by reviewing Rosen and Schwalbe (1988, p. 4),
Rossman et al. (1996, pp. 171-172), Ernst and Ernst (2003, pp. 391-
392), or Manjarrez and Garcia (1993, pp. 1-5).
Taxonomy
The northern Mexican gartersnake (Thamnophis eques megalops) is a
member of the family Colubridae and subfamily Natricinae (harmless
live-bearing snakes) (Lawson et al. 2005, p. 596; Pyron et al. 2013, p.
31). The taxonomy of the genus Thamnophis has a complex history, partly
because many of the species are similar in appearance and arrangement
of scales and many of the early museum specimens were in such poor and
faded condition that it was difficult to study them (Conant 2003, p.
6).
Prior to 2003, Thamnophis eques was considered to have three
subspecies, T. e. eques, T. e. megalops, and T. e. virgatenuis (Rossman
et al. 1996, p. 175). In 2003, an additional seven new subspecies were
identified under T. eques: (1) T. e. cuitzeoensis; (2) T. e.
patzcuaroensis; (3) T. e. insperatus; (4) T. e. obscurus; (5) T. e.
diluvialis; (6) T. e. carmenensis; and (7) T. e. scotti (Conant 2003,
p. 3). Common names were not provided, so in this final rule, we use
the scientific name for all subspecies of Mexican gartersnake other
than the northern Mexican gartersnake. These seven new subspecies were
described based on morphological differences in coloration and pattern,
have highly restricted distributions, and occur in isolated wetland
habitats within the mountainous Transvolcanic Belt region of southern
Mexico, which contains the highest elevations in the country (Conant
2003, pp. 7-8). Additional information regarding this subspecies'
taxonomy can be found in de Queiroz et al. (2002, p. 323), de Queiroz
and Lawson (1994, p. 217), Rossman et al. (1996, pp. xvii-xviii, 171-
175), Rosen and Schwalbe (1988, pp. 2-3), Liner (1994, p. 107), and
Crother et al. (2012, p. 70). A description of the taxonomy of the
northern Mexican gartersnake is found in our September 26, 2006 (71 FR
56227) and November 25, 2008 (73 FR 71788) 12-month findings for this
subspecies.
Habitat and Natural History
Throughout its rangewide distribution, the northern Mexican
gartersnake occurs at elevations from 130 to 8,497 feet (ft) (40 to
2,590 meters (m)) (Rossman et al. 1996, p. 172) and is considered a
``terrestrial-aquatic generalist'' (Drummond and Marc[iacute]as-
Garc[iacute]a 1983, pp. 24-26). The northern Mexican gartersnake is a
riparian obligate (generally found in riparian areas when not engaged
in dispersal, gestation, or hibernation behaviors) and occurs chiefly
in the following general habitat types: (1) Small, often isolated
wetlands (e.g., cienegas (mid-elevation wetlands with highly organic,
reducing (basic or alkaline) soils), or stock tanks (small earthen
impoundment)); (2) large-river riparian woodlands and forests; and (3)
streamside gallery forests (as defined by well-developed broadleaf
deciduous riparian forests with limited, if any, herbaceous ground
cover or dense grass) (Hendrickson and Minckley 1984, p. 131; Rosen and
Schwalbe 1988, pp. 14-16). Emmons and Nowak (2013, p. 14) found this
subspecies most commonly in protected backwaters, braided side channels
and beaver ponds, isolated pools near the river mainstem, and edges of
dense emergent vegetation that offered cover and foraging opportunities
when surveying in the upper and middle Verde River region. Additional
information on the habitat requirements of the northern Mexican
gartersnake within the United States and Mexico can be found in our
2006 (71 FR 56227) and 2008 (73 FR 71788) 12-month findings for this
subspecies and in Rosen and Schwalbe (1988, pp. 14-16), Rossman et al.
(1996, p. 176), McCranie and Wilson (1987, pp. 11-17), Ernst and Ernst
(2003, p. 392), and Cirett-Galan (1996, p. 156).
The northern Mexican gartersnake is surface active at ambient (air)
temperatures ranging from 71 degrees Fahrenheit ([deg]F) to 91 [deg]F
(22 degrees Celsius ([deg]C) to 33 [deg]C) and forages along the banks
of waterbodies (Rosen 1991, p. 305, Table 2). While conducting visual
surveys, Rosen (1991, pp. 308-309) found that northern Mexican
gartersnakes spent up to 60 percent of their time moving, 13 percent of
their time basking on vegetation, 18 percent of their time basking on
the ground, and 9 percent of their time under surface cover. However,
preliminary telemetry data from a population of northern Mexican
gartersnakes at the Bubbling Ponds State Fish Hatchery show individuals
were surface active during 16 percent of telemetry observations, not
surface active during 64 percent of telemetry observations, and surface
activity was undetermined for 20 percent of the telemetry observations
(Boyarsky 2013, pers. comm.); at Tavasci Marsh along the upper Verde
River, they were inactive 60 percent of the time (Emmons 2013b, pers.
comm.). In the northern-most part of its range, the northern Mexican
gartersnake appears to be most active during July and August, followed
by June and September (Emmons and Nowak 2013, p. 14). Northern Mexican
gartersnakes may use different sites as hibernacula during a single
cold-season and will bask occasionally (Emmons 2014, pers. comm.).
Although considered a highly aquatic species, the northern Mexican
gartersnake uses terrestrial habitat for hibernation (Young and
Boyarski 2012b, pp. 25-28), gestation, seeking mates, and dispersal.
Along the middle Verde River preliminary telemetry data for the
northern Mexican gartersnake found that the species may travel at least
528 feet (161 m) from the nearest water and as much as 0.4 mi (0.6 km)
in a single day (total distance traveled) (Emmons 2014, pers. comm.).
Terrestrial habitat use in open, grassland-dominated landscapes with
scattered livestock tanks, such as in southern Arizona, may reflect
that greater distances are traveled as suggested by the observation of
a large female northern Mexican gartersnake observed in O'Donnell
Canyon, which was far from source populations and may have been
dispersing overland (Rosen and Schwalbe 1988, p. 14). Preliminary data
from the population at Bubbling Ponds State Fish Hatchery show that
home ranges vary from 1.7 acres (0.7 ha) to 10.4 acres (4.2 ha), with a
mean home range size of 6.2 acres (2.51 ha) (Young and Boyarski 2012b,
p. 23).
The northern Mexican gartersnake is an active predator and depends
on smaller animals for its prey base (Rosen and Schwalbe 1988, pp. 18,
20). Northern Mexican gartersnakes forage along vegetated banklines,
searching for prey in water and on land, using different strategies
(Alfaro 2002, p. 209), or may forage along the edges of open water and
thick stands of vegetation such as cattails. Generally, its diet
consists of native amphibians and fishes, such as adult and larval
(tadpoles) native leopard frogs (e.g., lowland leopard frog (Lithobates
yavapaiensis) and Chiricahua leopard frog (Lithobates chiricahuensis)),
as well as juvenile and adult native fish species (e.g., Gila topminnow
(Poeciliopsis occidentalis occidentalis), desert pupfish (Cyprinodon
macularius), Gila chub (Gila intermedia), and roundtail chub (Gila
robusta)) (Rosen and
[[Page 38680]]
Schwalbe 1988, p. 18). Drummond and Marc[iacute]as-Garc[iacute]a (1983,
pp. 25, 30) found that as a subspecies, Mexican gartersnakes fed
primarily on frogs. The northern Mexican gartersnake may congregate at
ephemeral amphibian breeding ponds to exploit high-density prey
populations as observed at New Mexican spadefoot toads (Spea
multiplicata) breeding sites (d'Orgeix et al. 2013, pp. 213-215).
Auxiliary prey items may also include young Woodhouse's toads (Anaxyrus
woodhousei), treefrogs (Family Hylidae), earthworms, deermice
(Peromyscus spp.), lizards of the genera Aspidoscelis and Sceloporus,
larval tiger salamanders (Ambystoma tigrinum), and leeches (Rosen and
Schwalbe 1988, p. 20; Holm and Lowe 1995, pp. 30-31; Degenhardt et al.
1996, p. 318; Rossman et al. 1996, p. 176; Manjarrez 1998, p. 465).
Salamanders (Ambystoma spp.) may be particularly important as prey for
northern Mexican gartersnake populations in northern Mexico, both at
lower elevations and along the Sierra Madre Occidental (Lemos-Espinal
2013, pers. comm.).
In situations where native prey species are rare or absent, this
snake's diet may be almost completely comprised of nonnative species,
including larval and juvenile bullfrogs (Lithobates catesbeianus),
mosquitofish (Gambusia affinis) (Holycross et al. 2006, p. 23), or
subadult green sunfish, bluegill, or largemouth bass (Emmons and Nowak
2013, p. 5; Emmons 2013a, pers. comm.). The most recent observations of
northern Mexican gartersnakes attempting to eat predatory fish was
discussed in Emmons and Nowak (2013, p. 6) where they found fish inside
traps with gartersnakes, and the fish appeared to have been partially
consumed and then regurgitated. These observations suggest that, while
northern Mexican gartersnakes may attempt to eat predatory fish (at
least in the artificial confines of a wire trap), they may often be
spontaneously regurtitated, potentially causing harm to the snake
(Nowak and Santana-Bendix 2002, p. 24), and may not be compatible prey
for northern Mexican gartersnakes. Interestingly, in a 2012 trapping
effort along the upper Santa Cruz River, minnow traps that become self-
baited with bullfrogs, mosquitofish, or macroinvertebrates captured
snakes, but those which contained green sunfish or largemouth bass
never caught a single northern Mexican gartersnake (Lashway 2012, p.
6).
Chinese mystery snails (Cipangopaludina chinensis) have also been
reported as a prey item for northern Mexican gartersnakes at the Page
Springs and Bubbling Ponds State Fish Hatcheries in Arizona, but some
predation attempts on snails have proven fatal for gartersnakes because
of their lower jaw becoming permanently lodged in the snails' shell
(Young and Boyarski 2012a, p. 498). Venegas-Barrera and Manjarrez
(2001, p. 187) reported the first observation of a snake in the natural
diet of any species of Thamnophis after documenting the consumption of
a Mexican alpine blotched gartersnake (Thamnophis scalaris) by a
Mexican gartersnake (T. eques; subspecies not reported); a behavior
termed ophiophagy. Ophiophagy has not been specifically reported in
northern Mexican gartersnakes, although they are a subspecies of the
Mexican gartersnake.
Marc[iacute]as-Garc[iacute]a and Drummond (1988, pp. 129-134)
sampled the stomach contents of Mexican gartersnakes and the prey
populations at (ephemeral) Lake Tecocomulco, Hidalgo, Mexico. Field
observations indicated, with high statistical significance, that larger
Mexican gartersnakes fed primarily upon aquatic vertebrates (fishes,
frogs, and larval salamanders) and leeches, whereas smaller Mexican
gartersnakes fed primarily upon earthworms and leeches (Marc[iacute]as-
Garc[iacute]a and Drummond 1988, p. 131). Marc[iacute]as-Garc[iacute]a
and Drummond (1988, p. 130) also found that the birth of newborn T.
eques tended to coincide with the annual peak density of annelids
(earthworms and leeches). There is also preliminary evidence that birth
may coincide with a pronounced influx of available prey in a given
area, especially with that of explosive breeders, such as toads, but
more research is needed to confirm such a relationship (Boyarski 2012,
pers. comm.). Positive correlations were also made with respect to
capture rates (which are correlated with population size) of T. eques
to lake levels and to prey scarcity; that is, when lake levels were low
and prey species scarce, Mexican gartersnake capture rates declined
(Marc[iacute]as-Garc[iacute]a and Drummond 1988, p. 132). While prey
scarcity could have driven snakes to become active or take shelter
underground, their results suggest the importance of available water
and an adequate prey base to maintaining viable populations of Mexican
gartersnakes. Marc[iacute]as-Garc[iacute]a and Drummond (1988, p. 133)
found that, while certain prey items were positively associated with
size classes of snakes, the largest of specimens consume any prey
available.
Native predators of the northern Mexican gartersnake include birds
of prey, other snakes (kingsnakes (Lampropeltis sp.), whipsnakes
(Coluber sp.), regal ring-necked snakes (Diadophis punctatus regalis),
etc.), wading birds, mergansers (Mergus merganser), belted kingfishers
(Megaceryle alcyon), raccoons (Procyon lotor), skunks (Mephitis sp.),
and coyotes (Canis latrans) (Rosen and Schwalbe 1988, pp. 18, 39;
Brennan et al. 2009, p. 123). Historically, large, highly predatory
native fish species such as Colorado pikeminnow (Ptychocheilus lucius)
may have preyed upon northern Mexican gartersnake where the subspecies
co-occurred. Native chubs (Gila sp.) may also prey on neonatal
gartersnakes, but has not been documented in the literature to our
knowledge.
Sexual maturity in northern Mexican gartersnakes occurs at 2 years
of age in males and at 2 to 3 years of age in females (Rosen and
Schwalbe 1988, pp. 16-17). Northern Mexican gartersnakes are viviparous
(bringing forth living young rather than eggs). Mating has been
documented in April and May followed by the live birth of between 7 and
38 newborns (average is 13.6) in June, July, and August (Rosen and
Schwalbe 1988, p. 16; Nowak and Boyarski 2012, pp. 351-352; Boyarski
2013, pers. comm.). However, field observations in Arizona provide
preliminary evidence that mating may also occur during the fall, but
further research is required to confirm this hypothesis (Boyarski 2012,
pers. comm.). Unlike other gartersnake species, which typically breed
annually, one study suggests that only half of the sexually mature
females within a population of northern Mexican gartersnake might
reproduce in any one season (Rosen and Schwalbe 1988, p. 17). We found
no information on the longevity of northern Mexican gartersnakes but
presume they may live as long as 10 years in the wild.
Historical Distribution
Within the United States, the northern Mexican gartersnake
historically occurred predominantly in Arizona at elevations ranging
from 130 to 6,150 ft (40 to 1,875 m). It was generally found where
water was relatively permanent and supported suitable habitat. The
northern Mexican gartersnake has been documented historically in every
county and nearly every subbasin within Arizona, but its historical
distribution was essentially the southern two-thirds of Arizona. It was
known from several perennial or intermittent creeks, streams, and
rivers as well as lentic (still, non-flowing water) wetlands such as
cienegas, ponds, or stock tanks. Records documenting northern Mexican
[[Page 38681]]
gartersnake exist within the following subbasins in Arizona: Colorado
River, Bill Williams River, Agua Fria River, Salt River, Tonto Creek,
Verde River, Santa Cruz River, Cienega Creek, San Pedro River,
Babocomari River, and the Rio San Bernardino (Black Draw) (Woodin 1950,
p. 40; Nickerson and Mays 1970, p. 503; Bradley 1986, p. 67; Rosen and
Schwalbe 1988, Appendix I; 1995, p. 452; 1997, pp. 16-17; Holm and Lowe
1995, pp. 27-35; Sredl et al. 1995b, p. 2; 2000, p. 9; Rosen et al.
2001, Appendix I; Holycross et al. 2006, pp. 1-2, 15-51; Brennan and
Holycross 2006, p. 123; Radke 2006, pers. comm.; Rosen 2006, pers.
comm.; Holycross 2006, pers. comm.; Cotton et al. 2013, p. 111).
Numerous records for the northern Mexican gartersnake (through 1996) in
Arizona are maintained in the Arizona Game and Fish Department's (AGFD)
Heritage Database (1996a).
Historically, the northern Mexican gartersnake had a limited
distribution in New Mexico that consisted of scattered locations
throughout the Upper Gila River watershed in Grant and western Hidalgo
Counties, including the Upper Gila River, Mule Creek in the San
Francisco River subbasin, and the Mimbres River (Price 1980, p. 39;
Fitzgerald 1986, Table 2; Degenhardt et al. 1996, p. 317; Holycross et
al. 2006, pp. 1-2).
One record for the northern Mexican gartersnake exists for the
State of Nevada, opposite Fort Mohave, in Clark County along the shore
of the Colorado River that was dated 1911 (De Queiroz and Smith 1996,
p. 155). The subspecies may have occurred historically in the lower
Colorado River region of California, although we were unable to verify
any museum records for California. Any populations of northern Mexican
gartersnakes that may have historically occurred in either Nevada or
California were likely associated directly with the Colorado River, and
we believe the northern Mexican gartersnake to be currently extirpated
in Nevada and California.
Within Mexico, northern Mexican gartersnakes historically occurred
within the Sierra Madre Occidental and the Mexican Plateau in the
Mexican states of Sonora, Chihuahua, Durango, Coahuila, Zacatecas,
Guanajuato, Nayarit, Hidalgo, Jalisco, San Luis Potos[iacute],
Aguascalientes, Tlaxacala, Puebla, M[eacute]xico, Veracruz, and
Quer[eacute]taro, comprising approximately 85 percent of the total
rangewide distribution of the subspecies (Conant 1963, p. 473; 1974,
pp. 469-470; Van Devender and Lowe 1977, p. 47; McCranie and Wilson
1987, p. 15; Rossman et al. 1996, p. 173; Lemos-Espinal et al. 2004, p.
83). We are not aware of any systematic, rangewide survey effort for
the northern Mexican gartersnake in Mexico. Therefore, we use other
related ecological surrogates (such as native freshwater fish) to
inform discussion on the status of aquatic communities and aquatic
habitat in Mexico, and therefore on the likely status of northern
Mexican gartersnake populations. We believe that gartersnakes and
native fish are closely ecologically connected because of the high
level of dependency of the gartersnakes on the fish as a food source.
This discussion is found below in the subheadings pertinent to Mexico.
Current Distribution and Population Status
Data on population status of northern Mexican gartersnakes in the
United States are largely summarized in unpublished agency reports. In
our literature review we found that reductions in range and population
densities have affected the status of the northern Mexican gartersnake
significantly in the last 30 years. We found that, in as much as 90
percent of the northern Mexican gartersnakes' historical distribution
in the United States, the subspecies occurs at low to very low
population densities or may even be extirpated. For example, Holycross
et al. (2006, p. 66) detected the northern Mexican gartersnake at only
2 of 11 historical localities within the northern-most part of its
range in the United States. The degraded status of the northern Mexican
gartersnake, in a rangewide context, is primarily the result of
predation by and competition with harmful nonnative species, that have
been legally released, illegally released, or have naturally dispersed
(explained below). However, ecological circumstances and potential
threats vary from site to site, and the same threats do not affect
every population with the same magnitude across their range. Regardless
of how they got into the wild, harmful nonnative species are now
widespread and present throughout the range of the northern Mexican
gartersnake. Land uses that result in the dewatering of habitat,
combined with increasing drought, have destroyed significant amounts of
habitat throughout the northern Mexican gartersnake's range and have,
therefore, reduced its distribution within several subbasins.
Where northern Mexican gartersnakes are locally abundant, they are
usually reliably detected with significantly less effort than
populations characterized as having low densities. Northern Mexican
gartersnakes are well-camouflaged, secretive, and can be very difficult
to detect in structurally complex, dense habitat (Emmons and Nowak
2013, p. 13) or where they occur at very low population densities,
which characterizes most occupied sites in lotic habitat. We considered
factors such as the date of the last known records for northern Mexican
gartersnakes in an area, as well as records of one or more native prey
species in making a conclusion on occupancy of the subspecies. We used
the year 1980 to qualify occupancy because the 1980s marked the first
systematic survey efforts for northern Mexican gartersnakes across
their range in the United States (see Rosen and Schwalbe (1988, entire)
and Fitzgerald (1986, entire)) and the last, previous records were
often dated several decades prior and may not accurately represent the
likelihood for current occupation. Several areas where northern Mexican
gartersnakes were known to occur have received no, or very little,
survey effort in the past several decades. Variability in survey design
and effort makes it difficult to compare population sizes or trends
among sites and between sampling periods. For each of the sites
discussed in Appendix A (available at https://www.regulations.gov,
Docket No. FWS-R2-ES-2013-0071), we have attempted to translate and
quantify search and capture efforts into comparable units (i.e.,
person-search hours and trap-hours) and have cautiously interpreted
those results. Because the presence of suitable prey species in an area
may provide evidence that the northern Mexican gartersnake may still
persist in low density where survey data are sparse, a record of a
native prey species was considered in our determination of occupancy of
this subspecies.
Currently, there are only five northern Mexican gartersnake
populations in the United States, where the subspecies remains reliably
detected and is considered viable, and all are located in Arizona. The
five known populations are: (1) The Page Springs and Bubbling Ponds
State Fish Hatcheries along Oak Creek, (2) lower Tonto Creek, (3) the
upper Santa Cruz River in the San Rafael Valley, (4) the Bill Williams
River, and (5) the upper and middle Verde River. In New Mexico, the
northern Mexican gartersnake was last documented in 2013 along the Gila
River in the vicinity of the Highway 180 crossing (Hotle 2013, entire)
and is considered to occur in extremely low population densities within
its historical distribution along the Gila River and Mule Creek. While
[[Page 38682]]
historically known to occur on tribal lands, the status of the northern
Mexican gartersnake on tribal lands, such as those owned by the White
Mountain or San Carlos Apache Tribes, is poorly known due to limited
survey access. As stated previously, less is known specifically about
the current distribution of the northern Mexican gartersnake in Mexico
due to limited access to information on survey efforts and field data
from Mexico.
In Table 1 below, we summarize the population status of northern
Mexican gartersnakes at all known 29 historical localities throughout
their United States distribution, as supported by museum records or
reliable observations. We categorized each population as either likely
viable, likely not viable, or likely extirpated based on the historical
survey records, suitable habitat, presence of native prey species, and
the presence of harmful nonnative species. For a detailed discussion
that explains the rationale for site-by-site conclusions on occupancy,
please see Appendix A (available at https://www.regulations.gov, Docket
No. FWS-R2-ES-2013-0071). General rationale is provided in the
introductory paragraph to this section, ``Current Distribution and
Population Status.''
Table 1--Current Population Status of the Northern Mexican Gartersnake in the United States
[References for This Information Are Provided in Appendix A]
--------------------------------------------------------------------------------------------------------------------------------------------------------
Suitable physical Native prey species Harmful nonnative
Location Last record habitat present present species present Population status
--------------------------------------------------------------------------------------------------------------------------------------------------------
Gila River (NM, AZ)............... 2013.................. Yes................... Yes................... Yes.................. Likely not viable.
Spring Canyon (NM)................ 1937.................. Yes................... Possible.............. Likely............... Likely extirpated.
Mule Creek (NM)................... 1983.................. Yes................... Yes................... Yes.................. Likely not viable.
Mimbres River (NM)................ Likely early 1900s.... Yes................... Yes................... Yes.................. Likely extirpated.
Lower Colorado River (AZ)......... 1904.................. Yes................... Yes................... Yes.................. Likely extirpated.
Bill Williams River (AZ).......... 2012.................. Yes................... Yes................... Yes.................. Likely viable.
Agua Fria River (AZ).............. 1986.................. Yes................... Yes................... Yes.................. Likely not viable.
Little Ash Creek (AZ)............. 1992.................. Yes................... Yes................... Yes.................. Likely not viable.
Lower Salt River (AZ)............. 1964.................. Yes................... Yes................... Yes.................. Likely extirpated.
Black River (AZ).................. 1982.................. Yes................... Yes................... Yes.................. Likely not viable.
Big Bonito Creek (AZ)............. 1986.................. Yes................... Yes................... Yes.................. Likely not viable.
Tonto Creek (AZ).................. 2005.................. Yes................... Yes................... Yes.................. Likely viable.
Upper Verde River (AZ)............ 2012.................. Yes................... Yes................... Yes.................. Likely viable.
Oak Creek (AZ).................... 2012.................. Yes................... Yes................... Yes.................. Likely viable.
(Page Springs and Bubbling Ponds
State Fish Hatcheries).
Spring Creek (AZ)................. 1986.................. Yes................... Yes................... Yes.................. Likely not viable.
Sycamore Creek (Yavapai/Coconino 1954.................. Yes................... Possible.............. Yes.................. Likely extirpated.
Co., AZ).
Upper Santa Cruz River/San Rafael 2013.................. Yes................... Yes................... Yes.................. Likely viable.
Valley (AZ).
Redrock Canyon (AZ)............... 2008.................. Yes................... Yes................... Yes.................. Likely not viable.
Sonoita Creek (AZ)................ 2013.................. Yes................... Possible.............. Yes.................. Likely not viable.
Scotia Canyon (AZ)................ 2009.................. Yes................... Yes................... No................... Likely not viable.
Parker Canyon (AZ)................ 1986.................. Yes................... Possible.............. Yes.................. Likely not viable.
Las Cienegas National Conservation 2012.................. Yes................... Yes................... Possible............. Likely not viable.
Area and Cienega Creek Natural
Preserve (AZ).
Lower Santa Cruz River (AZ)....... 1956.................. Yes................... Yes................... Yes.................. Likely extirpated.
Buenos Aires National Wildlife 2000.................. Yes................... Yes................... Yes.................. Likely not viable.
Refuge (AZ).
Bear Creek (AZ)................... 1987.................. Yes................... Yes................... Yes.................. Likely not viable.
San Pedro River (AZ).............. 1996.................. Yes................... Yes................... Yes.................. Likely not viable.
Babocomari River and Cienega (AZ). 1986.................. Yes................... Possible.............. Yes.................. Likely not viable.
Canelo Hills-Sonoita Grasslands 2012.................. Yes................... Yes................... Yes.................. Likely not viable.
Area (AZ).
[[Page 38683]]
San Bernardino National Wildlife 1997.................. Yes................... Yes................... Yes.................. Likely not viable.
Refuge (AZ).
--------------------------------------------------------------------------------------------------------------------------------------------------------
Notes: ``Possible'' means there were no conclusive data found. ``Likely extirpated'' means the last record for an area pre-dated 1980, and existing
threats suggest the species is likely extirpated. ``Likely not viable'' means there is a post-1980 record for the species, it is not reliably found
with minimal to moderate survey effort, and threats exist which suggest the population may be low density or could be extirpated, but there is
insufficient evidence to support extirpation. ``Likely viable'' means that the species is reliably found with minimal to moderate survey effort, and
the population is generally considered to be somewhat resilient.
We conclude that as many as 24 of 29 known northern Mexican
gartersnake localities in the United States (83 percent) are likely not
viable and may exist at low population densities that could be
threatened with extirpation or may already be extirpated. In most
localities where the species may occur at low population densities,
existing survey data are insufficient to support a conclusion of
extirpation. Only five populations of northern Mexican gartersnakes in
the United States are considered likely viable where the species
remains reliably detected. In our November 25, 2008, 12-month finding,
we evaluated the total number of stream miles in the United States that
historically supported the northern Mexican gartersnake that are now
permanently dewatered (except in the case of temporary flows in
response to heavy precipitation), and we concluded that the subspecies
has been extirpated from or occurs at low densities in as much as 90
percent of its historical range in the United States (73 FR 71788, pp.
71792-71793). As shown in Table 1, harmful nonnative species are
present in all but one northern Mexican gartersnake locality in the
United States.
The northern Mexican gartersnake is listed as threatened throughout
its range in Mexico by the Mexican Government. However, our
understanding of the northern Mexican gartersnake's specific population
status throughout its range in Mexico is less precise than that known
for its United States distribution because survey efforts are less and
available records do not exist or are difficult to obtain for many
regions. Some specific geographic distribution records for the Mexican
states of Sonora, Chihuahua, and San Luis Potos[iacute] were presented
in Lemos-Espinal (2013, pers. comm.). Lemos-Espinal (2013 pers. comm),
a Mexican herpetologist whose work is focused on the states of Sonora,
Chihuahua, and Coahuila, commented that the number and magnitude of
threats are not equal across the subspecies' range in Mexico. Habitat
alteration or removal, as a circumstance of human population growth in
Mexico, is reported as a primary concern for populations that occur in
the Sierra Madre Occidental (Lemos-Espinal 2013, pers. comm.). In other
regions of Mexico, such as the states of Sonora and Chihuahua, Lemos-
Espinal (2013, pers. comm.) observed the northern Mexican gartersnake
to be quite common. Another gartersnake researcher from Mexico has
observed the decline or disappearance of some populations in central
Mexico (Manjerrez 2008).
Narrow-Headed Gartersnake
Species Description
The narrow-headed gartersnake is a small to medium-sized
gartersnake with a maximum total length of 44 in (112 cm) (Painter and
Hibbitts 1996, p. 147). Its eyes are set high on its unusually
elongated head, which narrows to the snout, and it lacks striping on
the dorsum (top) and sides, which distinguishes its appearance from
other gartersnake species with which it could co-occur (Rosen and
Schwalbe 1988, p. 7). The base color is usually tan or grey-brown (but
may darken) with conspicuous brown, black, or reddish spots that become
indistinct towards the tail (Rosen and Schwalbe 1988, p. 7; Boundy
1994, p. 126). The scales are keeled. Degenhardt et al. (1996, p. 327),
Rossman et al. (1996, pp. 242-244), and Ernst and Ernst (2003, p. 416)
further describe the species.
Taxonomy
We recognize the narrow-headed gartersnake, Thamnophis
rufipunctatus, as a monotypic species (no currently recognized
subspecies exist). The narrow-headed gartersnake is a member of the
family Colubridae and subfamily Natricinae (harmless live-bearing
snakes) (Lawson et al. 2005, p. 596). The taxonomy of the genus
Thamnophis has a complex history partly because many of the species are
similar in appearance and scutelation (arrangement of scales) and
because many of the early museum specimens were in such poor and faded
condition that it was difficult to study them (Conant 2003, p. 6).
There are approximately 30 species described in the gartersnake genus
Thamnophis (Rossman et al. 1996, pp. xvii-xviii). Two large overlapping
clades (related taxonomic groups) of gartersnakes have been identified
called the ``Mexican'' and ``widespread'' clades, supported by allozyme
and mitochondrial DNA genetic analyses (de Queiroz et al. 2002, p.
321). The narrow-headed gartersnake (Thamnophis rufipunctatus) is a
member of the ``Mexican'' clade and is most closely related
taxonomically to the southern Durango spotted gartersnake (Thamnophis
nigronuchalis) (de Queiroz and Lawson 1994, p. 217; de Queiroz et al.
2002; p. 321).
Due to the narrow-headed gartersnake's morphology and feeding
habits, there has been considerable deliberation among taxonomists
about the correct association of this species within seven various
genera over time (Rosen and Schwalbe 1988, pp. 5-6); chiefly, between
the genera Thamnophis (the ``gartersnakes'') and Nerodia (the
``watersnakes'') (Pierce 2007, p. 5). Chaisson and Lowe (1989, pp. 110-
118) argued that the pattern of ultrastructural (as revealed by an
electron microscope) pores in the scales of narrow-headed gartersnakes
provided evidence that the species is more appropriately placed within
the genus Nerodia. However, De Queiroz and Lawson (1994, p. 217)
rejected this premise using mitochondrial DNA (mtDNA) genetic analyses
to refute the inclusion of the narrow-headed gartersnake in the genus
Nerodia and maintain the species within the genus Thamnophis.
The narrow-headed gartersnake was first described as Chilopoma
rufipunctatum by E. D. Cope (in Yarrow, 1875). Recently, Thamnophis
[[Page 38684]]
rufipunctatus nigronuchalis and T. r. unilabialis were recognized as
subspecies under T. rufipunctatus and comprised what was considered the
T. rufipunctatus complex (Rossman et al. 1996, p. 245). However,
Rossman et al. (1996, pp. 244-246) elevated T. r. nigronuchalis to full
species designation and argued that recognition of T. r. unilabialis be
discontinued due to the diagnostic differences being too difficult to
discern. Wood et al. (2011, p. 14) used genetic analysis of the T.
rufipunctatus complex to propose the elevation of these three formerly
recognized subspecies as three distinct species, as a result of a
combination of interglacial warming, ecological and life-history
constraints, and genetic drift, which promoted differentiation of these
three species throughout the warming and cooling periods of the
Pleistocene epoch (Wood et al. 2011, p. 15). We use these most recent
and complete data in acknowledging these three entities as unique
species: T. rufipunctatus (along the Mogollon Rim of Arizona and New
Mexico, the narrow-headed gartersnake, which is the subject of this
rule), T. unilabialis (Chihuahua, eastern Sonora, and northern Durango,
Mexico), and T. nigronuchalis (southern Durango, Mexico).
Several common names have been used for this species including the
red-spotted gartersnake, the brown-spotted gartersnake, and the
currently used, narrow-headed gartersnake (Rosen and Schwalbe 1988, p.
5). Further discussion of the taxonomic history of the narrow-headed
gartersnake is available in Crother (2012, p. 71), Degenhardt et al.
(1996, p. 326), Rossman et al. (1996, p. 244), De Queiroz and Lawson
(1994, pp. 213-229), Rosen and Schwalbe (1988, pp. 5-7), and De Queiroz
et al. (2002, p. 321).
Habitat and Natural History
The narrow-headed gartersnake, distributed across the Mogollon Rim
of Arizona and New Mexico, is widely considered to be one of the most
aquatic of the gartersnakes (Drummond and Marcias Garcia 1983, pp. 24,
27; Rossman et al. 1996, p. 246). This species is strongly associated
with clear, rocky streams, using predominantly pool and riffle habitat
that includes cobbles and boulders (Rosen and Schwalbe 1988, pp. 33-34;
Degenhardt et al. 1996, p. 327; Rossman et al. 1996, p. 246; Nowak and
Santana-Bendix 2002, pp. 26-37; Ernst and Ernst 2003, p. 417). Rossman
et al. (1996, p. 246) also note the species has been observed using
lake shoreline habitat in New Mexico. Narrow-headed gartersnakes occur
at elevations from approximately 2,300 to 8,000 ft (701 to 2,430 m),
inhabiting Petran Montane Conifer Forest, Great Basin Conifer Woodland,
Interior Chaparral, and the Arizona Upland subdivision of Sonoran
Desertscrub communities (Rosen and Schwalbe 1988, p. 33; Brennan and
Holycross 2006, p. 122).
An extensive evaluation of habitat use of narrow-headed
gartersnakes along Oak Creek in Arizona is provided in Nowak and
Santana-Bendix (2002, pp. 26-37). In the upper reaches of Oak Creek,
occupied habitat is found in a steep-walled, confined canyon with
shallow, braided stream segments, minimal silt, and good canopy
coverage, vegetated islands and significant amounts of aquatic
vegetation (Nowak and Santana-Bendix 2002, pp. 29-30). In the middle
reaches of Oak Creek, occupied habitat is found in a wider canyon with
less stream braiding, deeper pools, more silt, and high canopy coverage
and stream-side vegetation, but less aquatic vegetation (Nowak and
Santana-Bendix 2002, pp. 30-31). In the lower reaches of Oak Creek,
historically occupied habitat occurred outside of the canyon proper,
with predominant pool-run sequences, rare channel braiding, much silt,
significantly less canopy coverage or streamside vegetation and few
areas with aquatic vegetation (Nowak and Santana-Bendix 2002, p. 31).
Nowak and Santana-Bendix (2002, pp. 29-31) found the most narrow-
headed gartersnakes in the upper reaches of Oak Creek, followed by the
middle reaches; no narrow-headed gartersnakes were found in the lower
reaches. Nowak and Santana-Bendix (2002, p. 33) found that, in general,
narrow-headed gartersnakes in Oak Creek were more likely to be found
within reaches without crayfish and without silt. Population densities
of warm-water predatory fish increase on a gradient from the upper to
the lower reaches of Oak Creek, while the inverse is true for native
fish populations, and their presence confounds the analysis of physical
habitat preference of narrow-headed gartersnakes. Rosen and Schwalbe
(1988, p. 35) found that the relative abundance of narrow-headed
gartersnakes may be highest at the conjunction of cascading riffles
with pools, where waters were deeper than 20 in (0.5 m) in the riffle
and deeper than 40 in (1 m) in the immediately adjoining area of the
pool. However, more than twice the number of snakes was found in pools
rather than riffles, but this observation may not translate for smaller
streams. Despite their highly aquatic behavior, narrow-headed
gartersnakes in Oak Creek have been shown to use upland habitat within
328 feet (100 m) during early fall and spring months, strongly
associate with boulders in the floodplain during summer months, and use
upland habitat up to 656 feet (200 m) out of the floodplain as
hibernation sites (Nowak 2006, pp. 20, 26).
Bank-line vegetation is an important component to suitable habitat
for this species (Nowak and Santana-Bendix 2002, pp. 26-37). Narrow-
headed gartersnakes will usually bask in situations where a quick
escape can be made, whether that is into the water or under substrate
such as rocks (Fleharty 1967, p. 16). Common plant species associations
include Arizona alder (Alnus oblongifolia) (highest correlation with
occurrence of the narrow-headed gartersnake), velvet ash (Fraxinus
pennsylvanica), willows (Salix ssp.), canyon grape (Vitis arizonica),
blackberry (Rubus ssp.), Arizona sycamore (Platanus wrightii), Arizona
black walnut (Juglans major), Freemont cottonwood (Populus fremontii),
Gambel oak (Quercus gambelii), and ponderosa pine (Pinus ponderosa)
(Rosen and Schwalbe 1988, pp. 34-35). Rosen and Schwalbe (1988, p. 35)
noted that the composition of bank-side plant species and canopy
structure may be less important to the species' needs than was the size
class of the plant species present; narrow-headed gartersnakes use
shrub- and sapling-sized plants for thermoregulating (basking) at the
waters' edge (Degenhardt et al. 1996, p. 327), as well as islands
within the stream channel that are created by sedge (Carex spp.)
tussocks (Nowak and Santana-Bendix 2002, p. 34).
Narrow-headed gartersnakes may opportunistically forage within
dammed reservoirs formed by streams that are occupied habitat, such as
at Wall Lake, New Mexico, (located at the confluence of Taylor Creek,
Hoyt Creek, and the East Fork Gila River) (Fleharty 1967, p. 207) and
most recently at Snow Lake in 2012 (located near the confluence of Snow
Creek and the Middle Fork Gila River) (Hellekson 2012b, pers. comm.) in
New Mexico, but records from impoundments are rare. The species evolved
in the absence of such habitat, and impoundments are generally managed
as sport fisheries (Wall Lake and Snow Lake are) and often maintain
populations of harmful nonnative species that are incompatible with
narrow-headed gartersnakes.
The narrow-headed gartersnake is surface-active generally between
March and November (Nowak 2006, p. 16). Little information on suitable
temperatures for surface activity of the narrow-headed gartersnake
exists;
[[Page 38685]]
however, it is presumed to be rather cold-tolerant based on its natural
history and foraging behavior that often involves clear, cold streams
at higher elevations. Along Oak Creek in Arizona, Nowak (2006, Appendix
1) found the species to be active in air temperatures ranging from 52
to 89[emsp14][deg]F (11 to 32 [deg]C) and water temperatures ranging
from 54 to 72[emsp14][deg]F (12 to 22 [deg]C). Jennings and Christman
(2011, pp. 12-14) found body temperatures of narrow-headed gartersnakes
along the Tularosa River averaged approximately 68[emsp14][deg]F (20
[deg]C) during the mid-morning hours and 81[emsp14][deg]F (27 [deg]C)
in the late afternoon during the period from late July and August.
Variables that affect their body temperature include the temperature of
the microhabitat used and water temperature (most predictive), but
slope aspect and the surface area of cover used also influenced body
temperatures (Jennings and Christman 2011, p. 13). Narrow-headed
gartersnakes have a lower preferred temperature for activity as
compared to other species of gartersnakes (Fleharty 1967, p. 228),
which may facilitate their highly aquatic nature in cold streams.
Narrow-headed gartersnakes specialize on fish as their primary prey
item (Rosen and Schwalbe 1988, p. 38; Degenhardt et al. 1996, p. 328;
Rossman et al. 1996, p. 247; Nowak and Santana-Bendix 2002, pp. 24-25;
Nowak 2006, p. 22). They are believed to be mainly visual hunters
(Hibbitts and Fitzgerald 2005, p. 364) heavily dependent on visual cues
when foraging based on comparative analyses among other species of
gartersnakes (de Queiroz 2003, p. 381). Unlike many other species of
gartersnakes that are active predators (actively crawl about in search
of prey), narrow-headed gartersnakes are considered to be ambush
predators (sit-and-wait method) (Brennan and Holycross 2006, p. 122;
Pierce et al. 2007, p. 8). The specific gravity (ratio of the mass of a
solid object to the mass of the same volume of water) of the narrow-
headed gartersnake was found to be nearly 1, which means that the snake
can maintain its desired position in the water column with ease, an
adaptation to facilitate foraging on the bottom of streams (Fleharty
1967, pp. 218-219).
Native fish species most often associated as prey items for the
narrow-headed gartersnake include Sonora sucker (Catostomus insignis),
desert sucker (C. clarki), speckled dace (Rhinichthys osculus),
roundtail chub (Gila robusta), Gila chub (Gila intermedia), and
headwater chub (Gila nigra) (Rosen and Schwalbe 1988, p. 39; Degenhardt
et al. 1996, p. 328). Nonnative predatory fish species in their
fingerling size classes are also used as prey by narrow-headed
gartersnakes, including brown trout (Rosen and Schwalbe 1988, p. 39;
Nowak and Santana-Bendix 2002, p. 24; Nowak 2006, pp. 22-23), green
sunfish (Fleharty 1967, p. 223), and smallmouth bass (Micropterus
dolomieu) (M. Lopez, 2010, pers. comm.). Reports suggest that brown
trout are consumed more frequently than smallmouth bass. Trout species
are commonly stocked in, or near, occupied narrow-headed gartersnake
habitat. Fleharty (1967, p. 223) reported narrow-headed gartersnakes
eating green sunfish. But nonnative fish with spiny dorsal fins are not
generally considered suitable prey items due to the risk of injury to
the gartersnake during ingestion and because of where they tend to
occur in the water column (see discussion in the subsection ``Fish''
under the subheading ``Decline of the Gartersnake Prey Base'' and Nowak
and Santana-Bendix (2002, p. 24)).
Although the narrow-headed gartersnake has been reported to also
prey upon amphibians such as frogs, tadpoles, and salamanders (Stebbins
1985, p. 199; Deganhardt et al. 1996, p. 328; Ernst and Ernst 2003, p.
418), we believe these are not important items in their diet. Despite
several studies focusing on the ecology of narrow-headed gartersnakes
in recent times, there are no other records of narrow-headed
gartersnakes, under current taxonomic recognition, feeding on prey
items other than fish. Fitzgerald (1986, p. 6) referenced the Stebbins
(1985) account as the only substantiated account of the species eating
something other than fish as prey, apparently as the result of finding
a small salamander larvae in the stomach of an individual in Durango,
Mexico. Formerly recognized as a subspecies of Thamnophis
rufipunctatus, that individual is now recognized as T. unilabialis
(Wood et al. 2011, p. 3). We found one account of narrow-headed
gartersnakes consuming red-spotted toads in captivity (Woodin 1950, p.
40). Amphibian larvae (i.e. Hyla sp., Anaxyrus sp., Ambystoma sp.) are
generally available to narrow-headed gartersnakes as prey, yet
observations of narrow-headed gartersnakes using them are rare.
Therefore, we do not consider amphibians as ecologically important prey
for this species.
Native predators of the narrow-headed gartersnake include birds of
prey, such as black-hawks (Etzel et al. 2014, p. 56), other snakes such
as regal ring-necked snakes (Brennan et al. 2009, p. 123), wading
birds, mergansers, belted kingfishers, raccoons (Rosen and Schwalbe
1988, p. 39), and possibly other generalist mammalian predators.
Historically, large, highly predatory native fish species, such as
Colorado pikeminnow, may have preyed upon narrow-headed gartersnakes
where the species co-occurred. Native chubs (Gila spp.) may also prey
on neonatal gartersnakes.
Sexual maturity in narrow-headed gartersnakes occurs at 2.5 years
of age in males and at 2 years of age in females (Deganhardt et al.
1996, p. 328). Narrow-headed gartersnakes are viviparous. Narrow-headed
gartersnakes breed annually, and females give birth to 4 to 17
offspring from late July into early August, perhaps earlier at lower
elevations (Rosen and Schwalbe 1988, pp. 35-37). Narrow-headed
gartersnakes may live as long as 10 years in the wild (Rosen and
Schwalbe 1988, p. 38).
Historical Distribution
The historical distribution of the narrow-headed gartersnake ranged
across the Mogollon Rim and along associated perennial stream drainages
from central and eastern Arizona, southeast to southwestern New Mexico
at elevations ranging from 2,300 to 8,000 ft (700 to 2,430 m) (Rosen
and Schwalbe 1988, p. 34; Rossman et al. 1996, p. 242; Holycross et al.
2006, p. 3). The species was historically distributed in headwater
streams of the Gila River subbasin that drain the Mogollon Rim and
White Mountains in Arizona, and the Gila Wilderness in New Mexico.
Major subbasins in its historical distribution included the Salt and
Verde River subbasins in Arizona, and the San Francisco and Gila River
subbasins in New Mexico (Holycross et al. 2006, p. 3). Holycross et al.
(2006, p. 3) suspect the species was likely not historically present in
the lowest reaches of the Salt, Verde, and Gila Rivers, even where
perennial flow persists. Numerous records for the narrow-headed
gartersnake (through 1996) in Arizona are maintained in the AGFD's
Heritage Database (1996b). The narrow-headed gartersnake as currently
recognized does not occur in Mexico.
Current Distribution and Population Status
Population status information suggests that the narrow-headed
gartersnake has experienced significant declines in population density
and distribution along streams and rivers where it was formerly well-
documented and reliably detected. Many areas where the species may
occur likely rely on emigration of individuals from occupied habitat
into those areas to maintain the species, provided there are no
potential
[[Page 38686]]
barriers to movement, such as extensive stretches of dewatered habitat,
or high densities of harmful nonnative species. Holycross et al. (2006,
entire) represents the most recent, comprehensive survey effort for
narrow-headed gartersnakes in Arizona. Narrow-headed gartersnakes were
detected in 5 of 16 historical localities in Arizona and New Mexico
surveyed by Holycross et al. (2006) in 2004 and 2005. Population
densities have noticeably declined in many populations, as compared to
previous survey efforts (Holycross et al. 2006, p. 66). Holycross et
al. (2006, pp. 66-67) compared narrow-headed gartersnake detections
based on results from their effort and that of previous efforts in the
same locations and found that significantly more effort is required to
detect this species in areas where it was formerly robust, such as
along Eagle Creek (AZ), the East Verde River (AZ), the San Francisco
River (NM), the Black River (AZ), and the Blue River (AZ).
Where narrow-headed gartersnakes are locally abundant, they can
usually be detected reliably and with significantly less effort than
populations characterized as having low densities. Narrow-headed
gartersnakes are well-camouflaged, secretive, and very difficult to
detect in structurally complex, dense habitat where they could occur at
very low population densities, which characterizes most occupied sites.
We considered factors such as the date of the last known records for
narrow-headed gartersnakes in an area, as well as records of one or
more native prey species, in making a conclusion on species occupancy.
We used all records that were dated 1980 or later because the 1980s
marked the first systematic survey efforts for narrow-headed
gartersnake species across their range (see Rosen and Schwalbe (1988,
entire) and Fitzgerald (1986, entire)), and the last, previous records
were often dated several decades prior and may not accurately represent
the likelihood for current occupation. Several areas where narrow-
headed gartersnakes were known to occur have received no, or very
little, survey effort in the past several decades. Variability in
survey design and effort makes it difficult to compare population sizes
or trends among sites and between sampling periods. Thus, for each of
the sites discussed in Appendix A (available at https://www.regulations.gov, Docket No. FWS-R2-ES-2013-0071), we have attempted
to translate and quantify search and capture efforts into comparable
units (i.e., person-search hours and trap-hours) and have cautiously
interpreted those results. Where survey data are sparse, the presence
of suitable prey species in an area may provide evidence that narrow-
headed gartersnakes may still persist at low densities. Therefore, a
record of a native prey species was considered in our determination of
occupancy of this species.
As of 2011, the only remaining narrow-headed gartersnake
populations where the species could reliably be found were located at:
(1) Whitewater Creek (NM), (2) Tularosa River (NM), (3) Diamond Creek
(NM), (4) Middle Fork Gila River (NM), and (5) Oak Creek Canyon (AZ).
However, populations found in Whitewater Creek and the Middle Fork Gila
River were likely significantly affected by the large Whitewater-Baldy
Complex Fire, which occurred in June 2012. In addition, salvage efforts
were initiated for these two populations, which included the removal of
25 individuals from Whitewater Creek and 14 individuals from the Middle
Fork Gila River before the onset of summer rains in 2012. These 39
individuals were transported to the Albuquerque BioPark where 22 remain
in captivity. The other 17 of the salvaged individuals were
translocated to Saliz Creek, where the resident native prey base
appears adequate, and beyond the effects from the Whitewater-Baldy
Complex Fire. The status of those populations in Whitewater Creek and
the Middle Fork Gila River has likely deteriorated as a result of
subsequent declines in resident fish communities due to heavy ash and
sediment flows, resulting fish kills, and the removal of snakes, but
subsequent survey data have not been collected. If the Whitewater Creek
and Middle Fork Gila River populations did decline as a result of these
factors, only three remaining populations of this species remain viable
today across their entire distribution. While historical records
confirm the narrow-headed gartersnake was found on tribal lands, its
current status on tribal land is poorly known due to limited survey
access.
In Table 2 below, we summarize the population status of the narrow-
headed gartersnake at all known localities throughout its distribution,
as supported by museum records or reliable observations. For a detailed
discussion that explains the rationale for site-by-site conclusions on
occupancy and status, please see Appendix A (available at https://www.regulations.gov, Docket No. FWS-R2-ES-2013-0071). General rationale
is provided in the introductory paragraph to this section, ``Current
Distribution and Population Status.''
Table 2--Current Population Status of the Narrow-Headed Gartersnake
[References for this information are provided in appendix A]
----------------------------------------------------------------------------------------------------------------
Suitable Harmful
Location Last record physical Native prey nonnative Population
habitat present species present species present status
----------------------------------------------------------------------------------------------------------------
West Fork Gila River (NM)... 2011 Yes............ Yes............ Yes............ Likely not
viable.
Middle Fork Gila River (NM). 2012 Yes............ Yes............ Yes............ Likely not
viable.
East Fork Gila River (NM)... 2006 Yes............ Yes............ Yes............ Likely not
viable.
Gila River (AZ, NM)......... 2009 Yes............ Yes............ Yes............ Likely not
viable.
Snow Creek/Snow Lake (NM)... 2012 Yes............ No............. Yes............ Likely not
viable.
Gilita Creek (NM)........... 2009 Yes............ Yes............ No............. Likely not
viable.
Iron Creek (NM)............. 2009 Yes............ Yes............ No............. Likely not
viable.
Little Creek (NM)........... 2010 Yes............ Possible....... Yes............ Likely not
viable.
Turkey Creek (NM)........... 1985 Yes............ Yes............ Possible....... Likely not
viable.
Beaver Creek (NM)........... 1949 Yes............ Possible....... Yes............ Likely
extirpated.
Black Canyon (NM)........... 2010 Yes............ Yes............ Yes............ Likely not
viable.
Taylor Creek (NM)........... 1960 Yes............ No............. Yes............ Likely
extirpated.
Diamond Creek (NM).......... 2011 Yes............ Yes............ Yes............ Likely viable.
Tularosa River (NM)......... 2012 Yes............ Yes............ Yes............ Likely viable.
Whitewater Creek (NM)....... 2012 Yes............ Yes............ Yes............ Likely not
viable.
San Francisco River (NM).... 2011 Yes............ Yes............ Yes............ Likely not
viable.
South Fork Negrito Creek 2011 Yes............ Possible....... Yes............ Likely not
(NM). viable.
Blue River (AZ)............. 2007 Yes............ Yes............ Yes............ Likely not
viable.
[[Page 38687]]
Dry Blue Creek (AZ, NM)..... 2010 Yes............ Possible....... Yes............ Likely not
viable.
Campbell Blue Creek (AZ, NM) 2010 Yes............ Possible....... Yes............ Likely not
viable.
Saliz Creek (NM)............ 2013 Yes............ Possible....... Yes............ Likely not
viable.
Eagle Creek (AZ)............ 2013 Yes............ Possible....... Yes............ Likely not
viable.
Black River (AZ)............ 2013 Yes............ Yes............ Yes............ Likely not
viable.
East Fork Black River (AZ).. 2004 Yes............ Possible....... Yes............ Likely not
viable.
Fish Creek (Tributary to 2004 Yes............ Yes............ Possible....... Likely viable.
East Fork Black River; AZ).
White River (AZ)............ 1986 Yes............ Yes............ Possible....... Likely not
viable.
Diamond Creek (AZ).......... 1986 Yes............ Possible....... Possible....... Likely not
viable.
Tonto Creek (tributary to 1915 Yes............ Possible....... Possible....... Likely
Big Bonita Creek, AZ). extirpated.
Canyon Creek (AZ)........... 1991 Yes............ Yes............ No............. Likely not
viable.
Upper Salt River (AZ)....... 1985 Yes............ Yes............ Yes............ Likely not
viable.
Cibeque Creek (AZ).......... 1991 Yes............ Yes............ Possible....... Likely not
viable.
Carrizo Creek (AZ).......... 1997 Yes............ Yes............ Possible....... Likely not
viable.
Big Bonito Creek (AZ)....... 1957 Yes............ Yes............ Yes............ Likely
extirpated.
Haigler Creek (AZ).......... 2008 Yes............ Yes............ Yes............ Likely not
viable.
Houston Creek (AZ).......... 2005 Yes............ Yes............ Yes............ Likely not
viable.
Tonto Creek (tributary to 2005 Yes............ Yes............ Yes............ Likely not
Salt River, AZ). viable.
Deer Creek (AZ)............. 1995 No............. No............. No............. Likely
extirpated.
Upper Verde River (AZ)...... 2012 Yes............ Yes............ Yes............ Likely not
viable.
Oak Creek (AZ).............. 2012 Yes............ Yes............ Yes............ Likely viable.
West Fork Oak Creek (AZ).... 2012 Yes............ Yes............ Yes............ Likely viable.
East Verde River (AZ)....... 1992 Yes............ Yes............ Yes............ Likely not
viable.
----------------------------------------------------------------------------------------------------------------
Notes: ``Possible'' means there were no conclusive data found. ``Likely extirpated'' means the last record for
an area pre-dated 1980, and existing threats suggest the species is likely extirpated. ``Likely not viable''
means there is a post-1980 record for the species, it is not reliably found with minimal to moderate survey
effort, and threats exist which suggest the population may be low density or could be extirpated, but there is
insufficient evidence to support extirpation. ``Likely viable'' means that the species is reliably found with
minimal to moderate survey effort, and the population is generally considered to be somewhat resilient.
Table 2 lists the 41 known localities for narrow-headed
gartersnakes throughout their range. We have concluded that, in as many
as 31 of 41 known localities (76 percent), the narrow-headed
gartersnake population is likely not currently viable and may exist at
low population densities that could be threatened with extirpation or
may already be extirpated, but survey data are lacking in areas where
access is restricted. In most localities where the species may occur at
low population densities, existing survey data are insufficient to
conclude extirpation. As of 2014, narrow-headed gartersnake populations
are considered currently likely viable in five localities (12 percent).
The remaining five populations (12 percent) are considered currently
likely extirpated. As displayed in Table 2, harmful nonnative species
are a concern for all but four narrow-headed gartersnake populations.
The status of these populations is expected to continue to decline.
Summary of Biological Status and Threats
Section 4 of the Act (16 U.S.C. 1533), and its implementing
regulations at 50 CFR part 424, set forth the procedures for adding
species to the Federal Lists of Endangered and Threatened Wildlife and
Plants. Under section 4(a)(1) of the Act, we may list a species based
on any of the following five factors: (A) The present or threatened
destruction, modification, or curtailment of its habitat or range; (B)
overutilization for commercial, recreational, scientific, or
educational purposes; (C) disease or predation; (D) the inadequacy of
existing regulatory mechanisms; and (E) other natural or manmade
factors affecting its continued existence. Listing actions may be
warranted based on any of the above threat factors, singly or in
combination.
In the following threats analysis, we treat both gartersnake
species in a combined discussion because of partially overlapping
ranges, similar natural histories, similar responses to threats, and
the fact that many threats are shared in common throughout their
ranges.
Weakened Status of Native Aquatic Communities (Northern Mexican and
Narrow-Headed Gartersnakes) (Factors A, C, and E)
The presence of harmful nonnative species constitutes the most
significant threat to the two gartersnake species. Harmful nonnative
species directly prey upon both species of gartersnake and compete with
them for prey. Harmful nonnative species also compete with gartersnake
prey species as well as modify habitat for both the gartersnakes and
their prey, to the detriment of both gartersnakes. Landscape-level
effects from the continued expansion of harmful nonnative species have
changed the spatial orientation of these gartersnakes' distributions,
creating greater isolation between populations. We expect the viability
of extant gartersnake populations to continue to degrade into the
foreseeable future as a result of ecological interactions with harmful
nonnative species. Riparian and aquatic communities in both the
southwestern United States and Mexico have been significantly impacted
by a shift in species' composition, from one of primarily native fauna,
to one dominated by an expanding assemblage of harmful nonnative animal
species. Harmful nonnative species have been introduced or have spread
into new areas through a variety of mechanisms, including intentional
and accidental releases, sport stocking, aquaculture, aquarium
releases, bait-bucket releases, or natural dispersal (Welcomme 1984,
entire). The ecological ramifications of
[[Page 38688]]
the adversarial relationships within southwestern aquatic communities
have been discussed and described in a broad body of literature,
extending from 1985 to the present (Meffe 1985, pp. 179-185; Propst et
al. 1986, pp. 14-31, 82; 1988, p. 64; 2009, pp. 5-17; Rosen and
Schwalbe 1988, pp. 28, 32; 1997, p. 1; Clarkson and Rorabaugh 1989, pp.
531, 535; Douglas et al. 1994, pp. 9-19; Rosen et al. 1995, pp. 257-
258; 2001, p. 2; Degenhardt et al. 1996, p. 319; Fernandez and Rosen
1996, pp. 8, 23-27, 71, 96; Richter et al. 1997, pp. 1089, 1092; Inman
et al. 1998, p. 17; Rinne et al. 1998, pp. 4-6; Nowak and Santana-
Bendix 2002, Table 3; Propst 2002, pp. 21-25; DFT 2003, pp. 1-3, 5-6,
19; 2004, pp. 1-2, 4-5, 10, Table 1; Bonar et al. 2004, pp. 13, 16-21;
Rinne 2004, pp. 1-2; Clarkson et al. 2005, p. 20; Fagan et al. 2005,
pp. 34, 34-41; Knapp 2005, pp. 273-275; Olden and Poff 2005, pp. 82-87;
Turner 2007, p. 41; Holycross et al. 2006, pp. 13-15; Brennan 2007, pp.
5, 7; Caldwell 2008a, 2008b; d'Orgeix 2008; Luja and Rodr[iacute]guez-
Estrella 2008, pp. 17-22; Propst et al. 2008, pp. 1242-1243; Rorabaugh
2008a, p. 25; Brennan and Rosen 2009, pp. 8-9; Minckley and Marsh 2009,
pp. 50-51; Pilger et al. 2010, pp. 311-312; Stefferud et al. 2009, pp.
206-207; 2011, pp. 11-12; Young and Boyarski 2013, pp. 159-160).
Decline of the Gartersnake Prey Base (Northern Mexican and Narrow-
Headed Gartersnakes) (Factors A and E)
The prey base of these gartersnakes includes native amphibians and
fish populations. Declines in their prey base have led to subsequent
declines in the distribution and density of gartersnake populations. In
most areas across their ranges, prey base declines are largely
attributed to the introduction and expansion of harmful nonnative
species.
Northern Mexican and narrow-headed gartersnakes may be particularly
vulnerable to the loss of native prey species (Rosen and Schwalbe 1988,
pp. 20, 44-45). Rosen et al. (2001, pp. 10, 13, 19) theorized that the
northern Mexican gartersnake: (1) Is unlikely to increase foraging
efforts at the risk of increased predation; and (2) needs adequate food
on a regular basis to maintain its weight and health. If forced to
forage more often for smaller prey items, a reduction in growth and
reproductive rates can result (Rosen et al. 2001, pp. 10, 13). Rosen et
al. (2001, p. 22) hypothesized that the presence and expansion of
nonnative predators (mainly bullfrogs, crayfish, and green sunfish
(Lepomis cyanellus)) are the primary causes of decline in northern
Mexican gartersnakes and in their prey in southeastern Arizona. In
another example, Drummond and Mac[iacute]as Garcia (1989, pp. 25, 30)
found that Mexican gartersnakes fed primarily on frogs, and when frogs
became unavailable, the species simply ceased major foraging
activities. This led the authors to conclude that frog abundance is
probably the most important correlate, and main determinant, of
foraging behavior in northern Mexican gartersnakes.
With respect to narrow-headed gartersnakes, the relationship
between harmful nonnative species, a declining prey base, and
gartersnake populations is clearly depicted in one population along Oak
Creek. Nowak and Santana-Bendix (2002, Table 3) found a strong
correlation in the distribution of fish communities and narrow-headed
gartersnake communities in the vicinity of Midgely Bridge. Downstream
of that point, nonnative, predatory fish species increase in abundance,
and narrow-headed gartersnakes notably decrease in abundance. Upstream
of that point, native fish and nonnative, soft-rayed fish species
increase in abundance as do narrow-headed gartersnakes (Nowak and
Santana-Bendix 2002, p. 23).
Fish (Northern Mexican and Narrow-headed Gartersnakes)--Fish are an
important prey item for the northern Mexican gartersnake and are the
only prey for the narrow-headed gartersnake. Native fish communities
throughout the range of these gartersnake have been on the decline,
both in terms of species composition and biomass, for many decades, and
largely as a result of predation and competition from and with
nonnative, predatory fish species. Stocked for sport, forage, or
biological control, nonnative fishes have been shown to become invasive
where released and do not require the natural flow regimes that native
species do (Kolar et al. 2003, p. 9), which has contributed to their
expansion in the Gila River basin and elsewhere. Northern Mexican and
narrow-headed gartersnakes can successfully use nonnative, soft-rayed
fish species as prey, such as mosquitofish, red shiner, and introduced
trout species, such as rainbow trout (Oncorynchus mykiss), brook trout
(Salvelinus fontinalis), or brown trout (Nowak and Santana-Bendix 2002,
pp. 24-25; Holycross et al. 2006, p. 23). However, predatory fish are
not generally considered prey species for northern Mexican or narrow-
headed gartersnakes and, in addition, are known to prey on neonatal and
juvenile gartersnakes (Young and Boyarski 2013, pp. 158-159). Nowak and
Santana-Bendix (2002, p. 24) propose two hypotheses regarding the
reluctance of narrow-headed gartersnakes to prey on nonnative,
predatory fish: (1) The laterally compressed shape and presence of
sharp, spiny dorsal spines of many nonnative, predatory fish present a
choking hazard to gartersnakes that can be fatal; and (2) nonnative,
predatory fish (with the exception of catfish) tend to occupy the
middle and upper zones in the water column, while narrow-headed
gartersnakes typically hunt along the bottom (where native suckers and
minnows often occur). As a result, nonnative, predatory fish may be
less ecologically available as prey.
Brown trout are highly predatory in all size classes in a wide
range of water temperatures, and they adversely affect native fish
communities wherever they are introduced (Taylor et al. 1984, pp. 343-
344). Predation on gartersnakes by adult brown trout may be a
particular problem for narrow-headed gartersnakes due to their
overlapping distributions and habitat preferences, both in terms of
direct predation on neonatal gartersnakes and through competitive
pressures for gartersnakes by preying on their food source.
Specifically, the younger age classes of brown trout present
competition problems for the narrow-headed gartersnake by eating small
fish. As brown trout mature into the medium to larger size classes,
they may prey upon neonatal narrow-headed gartersnakes. These issues
are confounded by the fact that young brown trout are also eaten by
narrow-headed gartersnakes and may represent an important component of
their prey base, depending on fish species composition and age classes
represented within the resident fish community. However, whatever
benefits fingerling brown trout present for narrow-headed gartersnakes
are likely off-set by effects of brown trout predation on important
native fish species, and possible effects to recruitment of narrow-
headed gartersnakes through predation.
Harmful nonnative species invasions can indirectly affect the
health, maintenance, and reproduction of northern Mexican and narrow-
headed gartersnakes by altering their foraging strategy and
compromising foraging success. Rosen et al. (2001, p. 19), in
addressing the northern Mexican gartersnake, proposed that an increase
in energy expended in foraging, coupled by the reduced number of small
to medium-sized prey fish available, results in deficiencies in
nutrition, affecting growth and reproduction. This occurs because
energy is allocated to maintenance and the increased energy costs of
intense foraging activity, rather than to growth and reproduction. In
[[Page 38689]]
contrast, a northern Mexican gartersnake diet that includes both fish
and amphibians, such as leopard frogs, reduces the necessity to forage
at a higher frequency, allowing metabolic energy gained from larger
prey items to be allocated instead to growth and reproductive
development. Myer and Kowell (1973, p. 225) experimented with food
deprivation in common gartersnakes, and found significant reductions in
lengths and weights of juvenile snakes that were deprived of regular
feedings versus the control group that were fed regularly at natural
frequencies. Reduced foraging success of both northern Mexican and
narrow-headed gartersnakes means that individuals are likely to become
vulnerable to effects from starvation, which may increase fatality
rates of juveniles and, consequently, affect recruitment.
Northern Mexican gartersnakes have a more varied diet than narrow-
headed gartersnakes. We are not aware of any studies that have
addressed the direct relationship between prey base diversity and
northern Mexican gartersnake recruitment and survivorship. However,
Krause and Burghardt (2001, pp. 100-123) discuss the benefits and costs
that may be associated with diet variability in the common gartersnake
(Thamnophis sirtalis), an ecologically similar species to the northern
Mexican gartersnake. Foraging for mixed-prey species may impede
predator learning, as compared to specialization on a certain prey
species, but it may also provide long-term benefits such as the ability
to capture prey throughout their lifespan (Krause and Burghardt 2001,
p. 101).
A wide variety of native fish species (many of which are now listed
as endangered, threatened, or candidates for listing under the Act)
were historically primary prey species for northern Mexican and narrow-
headed gartersnakes (Rosen and Schwalbe 1988, pp. 18, 39). Marsh and
Pacey (2005, p. 60) predict that, despite the significant physical
alteration of aquatic habitat in the southwestern United States, native
fish species could flourish in these altered environments but for the
presence of harmful nonnative fish species. Northern Mexican and, in
particular, narrow-headed gartersnakes depend largely on native fish as
a principal part of their prey base, although nonnative, soft-rayed
predatory fish have also been documented as prey where they overlap in
distribution with these gartersnakes (Nowak and Santana-Bendix 2002,
pp. 24-25; Holycross et al. 2006, p. 23; Emmons and Nowak 2013, p. 6).
Nonnative, predatory fish compete with northern Mexican and narrow-
headed gartersnakes for prey. In their extensive surveys, Rosen and
Schwalbe (1988, p. 44) only found narrow-headed gartersnakes in
abundance where native fish species predominated but did not find them
abundant in the presence of robust nonnative, predatory fish
populations. Minckley and Marsh (2009, pp. 50-51) found nonnative
fishes to be the single-most significant factor in the decline of
native fish species and also their primary obstacle to recovery. Of the
48 conterminous States in the United States, Arizona has the highest
proportion of nonnative fish species (66 percent) represented by
approximately 68 species (Turner and List 2007, p. 13).
Collier et al. (1996, p. 16) note that interactions between native
and nonnative fish have significantly contributed to the decline of
many native fish species from direct predation and, indirectly, from
competition (which has adversely affected the prey base for northern
Mexican and narrow-headed gartersnakes). Holycross et al. (2006, pp.
52-61) documented depressed or extirpated native fish prey bases for
northern Mexican and narrow-headed gartersnakes along the Mogollon Rim
in Arizona and New Mexico. Rosen et al. (2001, Appendix I) documented
the decline of several native fish species in several locations visited
in southeastern Arizona, further affecting the prey base of northern
Mexican gartersnakes in that area.
Harmful nonnative fish species tend to be nest-builders and
actively guard their young, which may provide them another ecological
advantage over native species that are broadcast spawners and provide
no parental care to their offspring (Marsh and Pacey 2005, p. 60). In
fact, nesting smallmouth bass will attack gartersnakes (Winemiller and
Taylor 1982, p. 270). It is, therefore, likely that recruitment and
survivorship is greater in nonnative species than native species where
they overlap, providing nonnative species with an ecological advantage.
Table 2-1 in Kolar et al. (2003, p. 10) provides a map depicting the
high degree of overlap in the distribution of native and nonnative
fishes within the Gila River basin of Arizona and New Mexico as well as
watersheds thought to be dominated by nonnative fish species.
The widespread decline of native fish species from the arid
southwestern United States and Mexico has resulted largely from
interactions with nonnative species and has been noted in the listing
rules of 11 fishes under the Act, and their historical ranges overlap
with the historical distribution of northern Mexican and narrow-headed
gartersnakes. Native fish species that were likely prey species for
these gartersnakes and are now listed under the Act, include the
bonytail chub (Gila elegans, 45 FR 27710, April 23, 1980), Yaqui chub
(Gila purpurea, 49 FR 34490, August 31, 1984), Yaqui topminnow
(Poeciliopsis occidentalis sonoriensis, 32 FR 4001, March 11, 1967),
beautiful shiner (Cyprinella formosa, 49 FR 34490, August 31, 1984),
Gila chub (Gila intermedia, 70 FR 66663, November 2, 2005), Colorado
pikeminnow (Ptychocheilus lucius, 32 FR 4001, March 11, 1967),
spikedace (Meda fulgida, 77 FR 10810, February 23, 2012), loach minnow
(Tiaroga cobitis, 77 FR 10810, February 23, 2012), razorback sucker
(Xyrauchen texanus, 56 FR 54957, October 23, 1991), desert pupfish
(Cyprinodon macularius, 51 FR 10842, March 31, 1986), woundfin
(Plagopterus argentissiums, 35 FR 16047, October 13, 1970), and Gila
topminnow (Poeciliopsis occidentalis, 32 FR 4001, March 11, 1967). In
total within Arizona, 19 of 31 (61 percent) native fish species are
listed under the Act. Arizona ranks the highest of all 50 States in the
percentage of native fish species with declining trends (85.7 percent),
and New Mexico ranks sixth (48.1 percent) (Stein 2002, p. 21; Warren
and Burr 1994, p. 14).
The fastest expanding nonnative species are red shiner (Cyprinella
lutrensis), fathead minnow (Pimephales promelas), green sunfish,
largemouth bass (Micropterus salmoides), western mosquitofish, and
channel catfish (Ictalurus punctatus). A nonnative species can become
invasive if ecological advantages exist for broad physical tolerances,
feeding habits and diet, or reproductive behavior (Taylor et al. 1984,
Table 16-1). These species are considered to be the most invasive in
terms of their negative impacts on native fish communities (Olden and
Poff 2005, p. 75). Many nonnative fishes, in addition to those listed
immediately above, including yellow and black bullheads (Ameiurus sp.),
flathead catfish (Pylodictis olivaris), and smallmouth bass, have been
introduced into formerly and currently occupied northern Mexican or
narrow-headed gartersnake habitat and are predators on these species
(Young and Boyarski 2013, pp. 158-159) and their prey (Bestgen and
Propst 1989, pp. 409-410; Marsh and Minckley 1990, p. 265; Sublette et
al. 1990, pp. 112, 243, 246, 304, 313, 318; Abarca and Weedman 1993,
pp. 6-12; Stefferud and Stefferud 1994, p. 364; Weedman and Young 1997,
pp. 1,
[[Page 38690]]
Appendices B, C; Rinne et al. 1998, pp. 3-6; Voeltz 2002, p. 88; Bonar
et al. 2004, pp. 1-108; Fagan et al. 2005, pp. 34, 38-39, 41; Propst et
al. 2008, pp. 1242-1243). Nonnative, predatory fish species, such as
flathead catfish, may be especially dangerous to narrow-headed
gartersnake populations through competition and direct predation
because they are primarily piscivorous (fish-eating) (Pilger et al.
2010, pp. 311-312), have large mouths, and have a tendency to occur
along the stream bottom, where narrow-headed gartersnakes principally
forage.
Rosen et al. (2001, Appendix I) and Holycross et al. (2006, pp. 15-
51) conducted large-scale surveys for northern Mexican gartersnakes in
southeastern and central Arizona and narrow-headed gartersnakes in
central and east-central Arizona, and documented the presence of
nonnative fish at many locations. Holycross et al. (2006, pp. 14-15)
found nonnative fish species in 64 percent of the sample sites in the
Agua Fria subbasin, 85 percent of the sample sites in the Verde River
subbasin, 75 percent of the sample sites in the Salt River subbasin,
and 56 percent of the sample sites in the Gila River subbasin. In
total, nonnative fish were observed at 41 of the 57 sites surveyed (72
percent) across the Mogollon Rim (Holycross et al. 2006, p. 14).
Entirely native fish communities were presumed in only 8 of 57 sites
surveyed (14 percent) (Holycross et al. 2006, p. 14). It is well
documented that nonnative fish have now infiltrated the majority of
aquatic communities in the southwestern United States as depicted in
Tables 1 and 2, above, as well as in Appendix A (available at https://www.regulations.gov, Docket No. FWS-R2-ES-2013-0071).
Several authors have identified both the presence of nonnative fish
as well as their deleterious effects on native species within Arizona.
Many areas have seen a shift from a predominance of native fishes to a
predominance of nonnative fishes. On the upper Verde River, native
species dominated the total fish community at greater than 80 percent
from 1994 to 1996, before dropping to approximately 20 percent in 1997
and 19 percent in 2001. At the same time, three nonnative species
increased in abundance between 1994 and 2000 (Rinne et al. 2005, pp. 6-
7). In an assessment of the Verde River, Bonar et al. (2004, p. 57)
found that, in the Verde River mainstem, nonnative fishes were
approximately 2.6 times more dense per unit volume of river than native
fishes, and their populations were approximately 2.8 times that of
native fishes per unit volume of river. Similar changes in the
dominance of nonnative fishes have occurred on the Middle Fork Gila
River, with a 65 percent decline of native fishes between 1988 and 2001
(Propst 2002, pp. 21-25). Abarca and Weedman (1993, pp. 6-12) found
that the number of nonnative fish species was twice the number of
native fish species in Tonto Creek in the early 1990s, with a stronger
nonnative species influence in the lower reaches, where the northern
Mexican gartersnake is considered to still occur (Burger 2010, p. 1,
Madera-Yagla 2010, p. 6, 2011, p. 6).
Beginning in 2014, the AGFD plans to stock 4.6 million Florida-
strain largemouth bass, 3.3 million bluegill, and 4.5 million black
crappie annually into Roosevelt Lake in order to control the gizzard
shad (Dorosoma cepedianum) population, which is currently the most
prevalent fish species in the lake and is thought to be depressing
sport fish populations in the reservoir (AGFD 2014, p. 3). Roosevelt
Lake is not, and will never be, suitable habitat for the northern
Mexican gartersnake because of its management as a sport fishery.
However, if the goal of this effort is achieved, we expect a higher
risk of predation of gartersnakes in lower Tonto Creek when a suitable
hydrologic connection is made between Tonto Creek and the lake body
(providing the opportunity for predatory nonnative fish to move into
lower Tonto Creek). We also expect high risk of predation of individual
snakes that may disperse downstream into the lake itself. Fish surveys
in the Salt River above Lake Roosevelt already indicate a decline of
roundtail chub and other native fishes, with an increase in flathead
and channel catfish numbers (Voeltz 2002, p. 49).
In New Mexico, nonnative fish have been identified as the main
cause for declines observed in native fish populations (Voeltz 2002, p.
40; Propst et al. 2008, pp. 1242-1243). Fish experts from the U.S.
Forest Service, U.S. Bureau of Reclamation, U.S. Bureau of Land
Management (BLM), University of Arizona, Arizona State University, The
Nature Conservancy, and others declared the native fish fauna of the
Gila River basin to be critically imperiled, and they cite habitat
destruction and nonnative species as the primary factors for the
declines (DFT 2003, p. 1). They call for the control and removal of
nonnative fish as an overriding need to prevent the decline, and
possible extinction, of native fish species within the basin (DFT 2003,
p. 1). In some areas, nonnative fishes may not dominate the system, but
their abundance has increased. This is the case for the Cliff-Gila
Valley area of the Gila River where nonnative fishes increased from 1.1
percent to 8.5 percent, while native fishes declined steadily over a
40-year period (Propst et al. 1986, pp. 27-32). At the Redrock and
Virden Valleys on the Gila River, the relative abundance in nonnative
fishes in the same time period increased from 2.4 percent to 17.9
percent (Propst et al. 1986, pp. 32-34). Four years later, the relative
abundance of nonnative fishes increased to 54.7 percent at these sites
(Propst et al. 1986, pp. 32-36). The percentage of nonnative fishes
increased by almost 12 percent on the Tularosa River between 1988 and
2003, while on the East Fork Gila River, nonnative fishes increased to
80.5 percent relative abundance in 2003 (Propst 2005, pp. 6-7, 23-24).
In addition to harmful nonnative species, various parasites may
affect native fish species that are prey for northern Mexican and
narrow-headed gartersnakes. Parasites affecting various species of
native fishes within the range of these gartersnakes include Asian
tapeworm (U.S. Fish and Wildlife Service (USFWS) National Wild Fish
Health Survey 2010), Ichthyophthirius multifiliis (Ich) (Mpoame 1982,
p. 46; Robinson et al. 1998, p. 603), anchor worm (Lernaea cyprinacea)
(Robinson et al. 1998, pp. 599, 603-605; Hoffnagle and Cole 1999, p.
24), yellow grub (Clinostomum marginatum) (Amin 1969, p. 436; Mpoame
and Rinne 1983, pp. 400-401; Bryan and Robinson 2000, p. 19; Maine
Department of Inland Fisheries and Wildlife 2002a, p. 1), and black
grub (Neascus spp.), also called black spot (Robinson et al. 1998, p.
603; Bryan and Robinson 2000, p. 21; Lane and Morris 2000, pp. 2-3;
Maine Department of Inland Fisheries and Wildlife 2002b, p. 1; Paroz
2011, pers. comm.). However, currently, we have no information on what
effect parasite infestation in native fish might have on gartersnake
populations.
Decline of Native Fish Communities in Mexico (Northern Mexican
Gartersnake)--The first tabulations of freshwater fish species at risk
in Mexico occurred in 1961, when 11 species were identified as being at
risk (Contreras-Balderas et al. 2003, p. 242). As of 2003, of the 506
species of freshwater fish recorded in Mexico, 185 (37 percent) have
been listed by the Mexican Federal Government as either endangered,
facing extinction, under special protection, or likely extinct
(Alvarez-Torres et al. 2003, p. 323), almost a 17-fold increase in
slightly over four decades; 25 species are believed to have gone
extinct (Contreras-Balderas et al. 2003, p. 241). In the lower
elevations of
[[Page 38691]]
Mexico, within the distribution of the northern Mexican gartersnake,
there are approximately 200 species of native freshwater fish
documented, with 120 native species under some form of threat and an
additional 15 that have gone extinct (Contreras-Balderas and Lozano
1994, pp. 383-384). The Fisheries Law in Mexico empowered the country's
National Fisheries Institute to compile and publish the National
Fisheries Chart in 2000, which found that Mexico's fish fauna has
seriously deteriorated as a result of environmental impacts
(pollution), water basin degradation (dewatering, siltation), and the
introduction of nonnative species (Alvarez-Torres et al. 2003, pp. 320,
323). The National Fisheries Chart is regarded as the first time the
Mexican Government has openly revealed the status of its freshwater
fisheries and described their management policies (Alvarez-Torres et
al. 2003, pp. 323-324).
Industrial, municipal, and agricultural water pollution, dewatering
of aquatic habitat, and the proliferation of nonnative species are
widely considered to be the greatest threats to freshwater ecosystems
in Mexico (Branson et al. 1960, p. 218; Conant 1974, pp. 471, 487-489;
Miller et al. 1989, pp. 25-26, 28-33; 2005, pp. 60-61; DeGregorio 1992,
p. 60; Contreras Balderas and Lozano 1994, pp. 379-381; Lyons et al.
1995, p. 572; 1998, pp. 10-12; Landa et al. 1997, p. 316; Mercado-Silva
et al. 2002, p. 180; Contreras-Balderas et al. 2003, p. 241;
Dom[iacute]nguez-Dom[iacute]nguez et al. 2007, Table 3). A shift in
land use policies in Mexico to encourage free market principles in
rural, small-scale agriculture has been found to promote land use
practices that threaten local biodiversity (Ortega-Huerta and Kral
2007, p. 2; Randall 1996, pp. 218-220; Kiernan 2000, pp. 13-23).
These threats have been documented throughout the distribution of
the northern Mexican gartersnake in Mexico and are best represented in
the scientific literature in the context of fisheries studies.
Contreras-Balderas et al. (2003, pp. 241, 243) named Chihuahua (46
species), Coahuila (35 species), Sonora (19 species), and Durango (18
species) as Mexican states that had some of the most reports of
freshwater fish species at risk. These states are all within the
distribution of the northern Mexican gartersnake, indicating an
overlapping trend of declining prey bases and threatened ecosystems
within the range of the northern Mexican gartersnake in Mexico.
Contreras-Balderas et al. (2003, Appendix 1) found various threats to
be adversely affecting the status of freshwater fish and their habitat
in several states in Mexico: (1) Habitat reduction or alteration
(Sonora, Chihuahua, Durango, Coahuila, San Luis Potos[iacute], Jalisco,
Guanajuato); (2) water depletion (Chihuahua, Durango, Coahuila, Sonora,
Guanajuato, Jalisco, San Luis Potos[iacute]); (3) harmful nonnative
species (Durango, Chihuahua, Coahuila, San Luis Potos[iacute], Sonora,
Veracruz); and (4) pollution (M[eacute]xico, Jalisco, Chihuahua,
Coahuila, Durango). Within the states of Chihuahua, Durango, Coahuila,
Sonora, Jalisco, and Guanajuato water depletion is considered serious,
with entire basins having been dewatered, or conditions have been
characterized as ``highly altered'' (Contreras-Balderas et al. 2003,
Appendix 1). All of the Mexican states with the highest numbers of fish
species at risk are considered arid, a condition hastened by increasing
desertification (Contreras-Balderas et al. 2003, p. 244).
Aquaculture and Nonnative Fish Proliferation in Mexico (Northern
Mexican Gartersnake)--Nonnative fish compete with and prey upon
northern Mexican gartersnakes and their native prey species. The
proliferation of nonnative fish species throughout Mexico happened
mainly by natural dispersal, intentional stockings, and accidental
breaches of artificial or constructed barriers by nonnative fish
(Welcomme 1984, entire). Lentic water bodies such as lakes, reservoirs,
and ponds are often used for flood control, agricultural purposes, and
most commonly to support commercial fisheries. The most recent
estimates indicate that Mexico has 13,936 of such water bodies, where
approximately 96 percent are between 2.47-247 acres (1-100 hectares)
and approximately half are artificial (Sugunan 1997, Table 8.3;
Alvarez-Torres et al. 2003, pp. 318, 322). Areas where these landscape
features are most prevalent occur within the distribution of the
northern Mexican gartersnake. For example, Jalisco and Zacatecas are
listed as two of four states with the highest number of reservoirs, and
Chihuahua is one of two states known for a high concentration of lakes
(Sugunan 1997, Section 8.4.2).
Based on the data presented in Sugunan (1997, Table 8.5), a total
of 422 dammed reservoirs are located within the 16 Mexican states where
the northern Mexican gartersnake is thought to occur. Mercado-Silva et
al. (2006, p. 534) found that, within the state of Guanajuato,
``Practically all streams and rivers in the (Laja) basin are truncated
by reservoirs or other water extraction and storage structures.'' On
the Laja River alone, there are two major reservoirs and a water
diversion dam; 12 more reservoirs are located on its tributaries
(Mercado-Silva et al. 2006, p. 534). As a consequence of dam
operations, the main channel of the Laja remains dry for extensive
periods of time (Mercado-Silva et al. 2006, p. 541). The damming and
modification of the lower Colorado River in Mexico, where the northern
Mexican gartersnake occurred, has facilitated the replacement of the
entire native fishery with nonnative species (Miller et al. 2005, p.
61). Each reservoir created by a dam is either managed as a nonnative
commercial fishery or has become a likely source population of
nonnative species, which have naturally or artificially colonized the
reservoir, dispersed into connected riverine systems, and damaged
native aquatic communities.
Mexico depends in large part on freshwater commercial fisheries as
a source of protein for both urbanized and rural human populated areas.
Commercial and subsistence fisheries rely heavily on introduced,
nonnative species in the largest freshwater lakes (Soto-Galera et al.
1999, p. 133) down to rural, small ponds (Tapia and Zambrano 2003, p.
252). At least 87 percent of the species captured or cultivated in
inland fisheries of Mexico from 1989-1999 included tilapia (Tilapia
spp.), common carp (Cyprinus carpio), channel catfish, trout, and black
bass (Micropterus sp.), all of which are nonnative (Alvarez-Torres et
al. 2003, pp. 318, 322). In fact, the northern and central plateau
region of Mexico (which comprises most of the distribution of the
northern Mexican gartersnake's distribution in Mexico) is considered
ideal for the production of harmful, predatory species such as bass and
catfish (Sugunan 1997, Section 8.3). Largemouth bass are now produced
and stocked in reservoirs and lakes throughout the distribution of the
northern Mexican gartersnake (Sugunan 1997, Section 8.8.1).
The Secretariat for Environment, Natural Resources and Fisheries
(SEMARNAP), formed in 1995, is the Mexican federal agency responsible
for management of the country's environment and natural resources.
SEMARNAP dictates the stocking rates of nonnative species into the
country's lakes and reservoirs. For example, the permitted stocking
rate for largemouth bass in Mexico is one fish per square meter in
large reservoirs (Sugunan 1997, Table 8.8); therefore, a 247-acre (100-
ha) reservoir could be stocked with 1,000,000 largemouth bass. The
common carp, the subject of significant aquaculture investment since
the 1960s in Mexico, is known for altering aquatic habitat and
consuming the eggs and fry of native fish species, and is now
[[Page 38692]]
established in 95 percent of Mexico's freshwater systems (Tapia and
Zambrano 2003, p. 252).
Basins in northern Mexico, such as the Rio Yaqui, have been found
to be significantly compromised by harmful nonnative fish species.
Unmack and Fagan (2004, p. 233) compared historical museum collections
of nonnative fish species from the Gila River basin in Arizona and the
Yaqui River basin in Sonora, Mexico, to gain insight into the trends in
distribution, diversity, and abundance of nonnative fishes in each
basin over time. They found that nonnative species are slowly, but
steadily, increasing in all three parameters in the Yaqui Basin (Unmack
and Fagan 2004, p. 233). Unmack and Fagan (2004, p. 233) predicted
that, in the absence of aggressive management intervention, significant
extirpations or range reductions of native fish species are expected to
occur in the Yaqui Basin of Sonora, Mexico, which may have extant
populations of the northern Mexican gartersnake, as did much of the
Gila Basin before the introduction of nonnative species. Loss of native
fishes impacts prey availability for the northern Mexican gartersnake
and threatens its persistence in these areas. Black bullheads (Ameiurus
melas) were reported as abundant, and common carp were detected from
the Rio Yaqui in southern Sonora, Mexico (Branson et al. 1960, p. 219).
Bluegill (Lepomis macrochirus) were also reported at this location,
representing a significant range expansion that the authors expected
was the result of escaping nearby farm ponds or irrigation ditches
(Branson et al. 1960, p. 220). Largemouth bass, green sunfish, and an
undetermined crappie species have also been reported from this area
(Branson et al. 1960, p. 220).
Documented problems with aquatic habitats in Mexico include water
pollution, harmful nonnative species, and physical habitat alteration.
All of these factors lead to declines in native fish abundance and,
therefore, a decline in the food source for the northern Mexican
gartersnake. Dom[iacute]nguez-Dom[iacute]nguez et al. (2007, p. 171)
sampled 52 localities for a rare freshwater fish, the Picotee goodeid
(Zoogoneticus quitzeoensis), along the southern portion of the Mesa
Central (Mexican Plateau) of Mexico and found 21 localities had
significant signs of pollution. Of the 29 localities where the target
species was detected, 28 of them also had harmful nonnative species
present, such as largemouth bass, cichlids (Oreochromis sp.), bluegill,
and P[aacute]tzcuaro chub (Algansea lacustris) (Dom[iacute]nguez-
Dom[iacute]nguez et al. 2007, pp. 171, Table 3). The first assessment
of the impacts of largemouth bass on native fishes in Mexico was in
1941 during the examination of their effect in Lago de P[aacute]tzcuaro
(Contreras and Escalante 1984, p. 102). Other nonnative fish species
reported are soft-rayed and small bodied, and may be prey items for
younger age classes of gartersnakes.
Several examples of significant aquatic habitat degradation or
destruction were also observed by Dom[iacute]nguez-Dom[iacute]nguez et
al. (2007, Table 3) in this region of Mexico, including the draining of
natural lakes and cienegas for conversion to agricultural purposes,
modification of springs for recreational swimming, diversions, and dam
construction. It should be noted that approximately 17 percent of the
localities sampled by Dom[iacute]nguez-Dom[iacute]nguez et al. (2007,
entire) are within the likely range of the northern Mexican
gartersnake; chiefly sites located within the Rio Grande de Santiago
and Laja Basin. However, collectively, observations made by
Dom[iacute]nguez-Dom[iacute]nguez et al. (2007, entire) provide a
regional context to potential threats acting on northern Mexican
gartersnakes in their southern-most distribution. As of 2006, native
fish species dominated the fish community in both species composition
and overall abundance in the Laja Basin; however, the basin is now
trending toward a nonnative fishery compared to historical data. For
example, nonnative species were most recently collected from 16 of 17
sample sites in the basin, with largemouth bass significantly expanding
their distribution within the headwaters of the basin and bluegill
being widespread in the Laja River (Mercado-Silva et al. 2006, pp. 537,
542, Table 4). The decline of native fishes in this region of Mexico is
likely negatively affecting the status of the northern Mexican
gartersnakes there.
Harmful nonnative fish species in Mexico (Contraras and Escalante
1984, pp. 102-125) may be posing a significant threat to the native
fish prey base of northern Mexican gartersnakes and to the gartersnakes
themselves. The ecological risk of nonnative, freshwater fishes is only
expected to increase with increases in aquaculture production, most
notably in the country's rural, poorest regions (Tapia and Zambrano
2003, p. 252). Amendments to Mexico's existing fishing regulations
imposed by other government regulations have been relaxed, and
investment in commercial fishing has expanded to promote growth in
Mexico's aquaculture sector (Sugunan 1997, Section 8.7.1). Several
areas within the range of the northern Mexican gartersnake in Mexico
have experienced adverse effects associated with nonnative species.
Amphibian Decline (Northern Mexican Gartersnake)--Amphibians are a
principle prey item for the northern Mexican gartersnake, and
documented declines in amphibian population densities and distributions
have significantly contributed to the decline in northern Mexican
gartersnakes. As an example of these effects from another region,
Matthews et al. (2002, p. 16) examined the relationship of gartersnake
distributions, amphibian population declines, and nonnative fish
introductions in high-elevation aquatic ecosystems in California.
Matthews et al. (2002, p. 16) specifically examined the effect of
nonnative trout introductions on populations of amphibians and mountain
gartersnakes (Thamnophis elegans elegans). Their results indicated that
the probability of observing gartersnakes was 30 times greater in lakes
containing amphibians than in lakes where amphibians have been
extirpated by nonnative fish. These results supported a prediction by
Jennings et al. (1992, p. 503) that native amphibian declines will lead
directly to gartersnake declines.
Declines in the native leopard frog populations in Arizona have
likely been a significant, contributing factor to declines in many
northern Mexican gartersnake populations. Native ranid (of the family
Ranidae) frog species, such as lowland leopard frogs, northern leopard
frogs, and federally threatened Chiricahua leopard frogs, have
experienced declines in various degrees throughout their distribution
in the Southwest, largely due to predation and competition with
nonnative species (Clarkson and Rorabaugh 1989, pp. 531, 535; Hayes and
Jennings 1986, p. 490). Rosen et al. (1995, pp. 257-258) found that
Chiricahua leopard frog distribution in the Chiricahua Mountain region
of Arizona was inversely related to nonnative species distribution.
Along the Mogollon Rim, Holycross et al. (2006, p. 13) found that only
8 sites of 57 surveyed (15 percent) consisted of an entirely native
anuran (of the order Anura) community and that native frog populations
in another 19 sites (33 percent) had been completely displaced by
invading bullfrogs. However, such declines in native frog populations
are not necessarily irreversible. Ranid frog populations have been
shown to rebound strongly when nonnative fish are removed (Knapp et al.
2007, pp. 15-18).
Scotia Canyon, in the Huachuca Mountains of southeastern Arizona,
is a location where corresponding declines of leopard frog and northern
Mexican
[[Page 38693]]
gartersnake populations have been documented through repeated survey
efforts over time (Holm and Lowe 1995, p. 33). Surveys of Scotia Canyon
occurred during the early 1980s and again during the early 1990s.
Leopard frogs in Scotia Canyon were infrequently observed during the
early 1980s and were nearly extirpated by the early 1990s (Holm and
Lowe 1995, pp. 45-46). Northern Mexican gartersnakes were observed in
decline during the early 1980s, with low capture rates continuing
through the early 1990s (Holm and Lowe 1995, pp. 27-35). Surveys
documented further decline of leopard frogs and northern Mexican
gartersnakes in 2000 (Rosen et al. 2001, pp. 15-16).
A former large, local population of northern Mexican gartersnakes
at the San Bernardino National Wildlife Refuge (SBNWR) in southeastern
Arizona has also experienced a correlative decline of leopard frogs,
and northern Mexican gartersnakes are now thought to occur at very low
population densities or may be extirpated there (Rosen and Schwalbe
1988, p. 28; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-
227; 2002c, pp. 31, 70; Rosen et al. 1996b, pp. 8-9; 2001, pp. 6-10).
Survey data indicate that declines of leopard frog populations,
often correlated with nonnative species introductions, the spread of a
chytrid fungus (Batrachochytrium dendrobatidis, Bd), and habitat
modification and destruction, have occurred throughout much of the
northern Mexican gartersnake's U.S. distribution (Nickerson and Mays
1970, p. 495; Vitt and Ohmart 1978, p. 44; Ohmart et al. 1988, p. 150;
Rosen and Schwalbe 1988, Appendix I; 1995, p. 452; 1996, pp. 1-3; 1997,
p. 1; 2002b, pp. 232-238; 2002c, pp. 1, 31; Clarkson and Rorabaugh
1989, pp. 531-538; Sredl et al. 1995a, pp. 7-8; 1995b, pp. 8-9, 1995c,
pp. 7-8; 2000, p. 10; Holm and Lowe 1995, pp. 45-46; Rosen et al.
1996b, p. 2; 2001, pp. 2, 22; Degenhardt et al. 1996, p. 319; Fernandez
and Rosen 1996, pp. 6-20; Drost and Nowak 1997, p. 11; Turner et al.
1999, p. 11; Nowak and Spille 2001, p. 32; Holycross et al. 2006, pp.
13-14, 52-61). Holycross et al. (2006, pp. 53-57, 59) documented
population declines and potential extirpations of lowland leopard frogs
(an important prey species of the northern Mexican gartersnake) in most
of the Agua Fria subbasin and areas of the Salt and Verde subbasins in
the period 1986-2006. Specifically, Holycross et al. (2006, pp. 53-57,
59) detected no lowland leopard frogs at several recently,
historically, or potentially occupied locations, including the Agua
Fria River in the vicinity of Table Mesa Road and Little Grand Canyon
Ranch, and at Rock Springs, Dry Creek from Dugas Road to Little Ash
Creek, Little Ash Creek from Brown Spring to Dry Creek, Sycamore Creek
(Agua Fria subbasin) in the vicinity of the Forest Service Cabin, the
Page Springs and Bubbling Ponds fish hatchery along Oak Creek, Sycamore
Creek (Verde River subbasin) in the vicinity of the confluence with the
Verde River north of Clarkdale, along several reaches of the Verde
River mainstem, Cherry Creek on the east side of the Sierra Ancha
Mountains, and Tonto Creek from Gisela to ``the Box,'' near its
confluence with Rye Creek. Rosen et al. (2013, p. 8) suggested that the
decline of leopard frogs in the Empire Valley of southern Arizona is
likely largely responsible for the decline of the northern Mexican
gartersnake there.
A primary factor in the decline of native amphibians as a food
source for northern Mexican gartersnakes in southern Arizona is likely
the result of impacts from nonnative species, mainly bullfrogs. Rosen
et al. (1995, pp. 252-253) sampled aquatic herpetofauna at 103 sites in
the Chiricahua Mountains region, which included the Chiricahua,
Dragoon, and Peloncillo Mountains, and the Sulphur Springs, San
Bernardino, and San Simon valleys. They found that 43 percent of all
ectothermic (cold-blooded) aquatic and semi-aquatic vertebrate species
detected were nonnative. The most commonly encountered nonnative
species was the bullfrog (Rosen et al. 1995, p. 254). Witte et al.
(2008, p. 1) found that the disappearance of ranid frog populations in
Arizona were 2.6 times more likely in the presence of crayfish. Witte
et al. (2008, p. 7) emphasized the significant influence of nonnative
species on the disappearance of ranid frogs in Arizona. In one area,
Rosen et al. (2001, p. 22) identified the expansion of bullfrogs into
the Sonoita grasslands, which contain occupied northern Mexican
gartersnake habitat, and the introduction of crayfish into Lewis
Springs as being of particular concern for the northern Mexican
gartersnake in that area.
In addition to harmful nonnative species, disease and nonnative
parasites have been implicated in the decline of the prey base of the
northern Mexican gartersnake. In particular, the outbreak of
chytridiomycosis or ``Bd,'' a skin fungus, has been identified as a
chief causative agent in the significant declines of many of the native
ranid frogs and other amphibian species. As indicated, Bd has been
implicated in both large-scale declines and local extirpations of many
amphibians, chiefly anuran species, around the world (Johnson 2006, p.
3011). Lips et al. (2006, pp. 3166-3169) suggest that the high
virulence and large number of potential hosts make Bd a serious threat
to amphibian diversity. In Arizona, Bd infections have been reported in
several of the native prey species of the northern Mexican gartersnake
within the distribution of the snake (Morell 1999, pp. 731-732; Sredl
and Caldwell 2000, p. 1; Hale 2001, pp. 32-37; Bradley et al. 2002, p.
207; USFWS 2002, pp. 40802-40804; USFWS 2007a, pp. 26, 29-32). Declines
of native prey species of the northern Mexican gartersnake from Bd
infections have contributed to the decline of this species in the
United States (Morell 1999, pp. 731-732; Sredl and Caldwell 2000, p. 1;
Hale 2001, pp. 32-37; Bradley et al. 2002, p. 207; USFWS 2002, pp.
40802-40804; USFWS 2007a, pp. 26, 29-32).
Evidence of Bd-related amphibian declines has been confirmed in
portions of southern Mexico (just outside the range of northern Mexican
gartersnakes), and data suggest declines are more prevalent at higher
elevations where northern Mexican gartersnakes can occur (Lips et al.
2004, pp. 560-562). However, much less is known about the role of Bd in
amphibian declines across much of Mexico, in particular the mountainous
regions of Mexico (including much of the range of northern Mexican
gartersnakes in Mexico) as the region is significantly understudied
(Young et al. 2000, p. 1218). Because narrow-headed gartersnakes feed
on fish, Bd has not affected their prey base. A recent study in Panama
by Kilburn et al. (2011, p. 132) found that reptiles may act as
reservoirs for Bd (at least in environments such as Panama) based on
the presence of the fungus at non-pathological levels on lizards that
occur in areas with significant Bd outbreaks in resident amphibians.
Their study did not conclude that Bd is a virulent reptile pathogen, or
that it causes disease-induced population declines in reptiles (Kilburn
et al. 2011, p. 132).
Effects of Bullfrogs on Native Aquatic Communities (Northern Mexican
and Narrow-Headed Gartersnakes) (Factors A, C, and E)
Direct predation by, and competition with, bullfrogs is a serious
threat to northern Mexican gartersnakes throughout their range (Conant
1974, pp. 471, 487-489; Rosen and Schwalbe 1988, pp. 28-30; Rosen et
al. 2001, pp. 21-22). Bullfrogs have and do threaten some populations
of narrow-headed
[[Page 38694]]
gartersnakes, but differing habitat preferences between bullfrogs and
narrow-headed gartersnakes lessen their effect on narrow-headed
gartersnake populations. Bullfrogs adversely affect northern Mexican
and narrow-headed gartersnake populations through direct predation of
juveniles and sub-adults. Bullfrogs also compete with northern Mexican
gartersnakes for prey species.
Bullfrogs are not native to the southwestern United States or
Mexico, and they first appeared in Arizona in 1926 as a result of a
systematic introduction effort by the State Game Department (now, the
AGFD) for the purposes of sport hunting and as a food source (Tellman
2002, p. 43). The first bullfrog record from New Mexico is dated 1885
(Degenhardt et al. 1996, p. 85). Bullfrogs are extremely prolific, are
strong colonizers, can reach high densities, are persistent via
cannibalism, and may disperse distances of up to 10 mi (16 km) across
uplands and likely further within drainages (Bautista 2002, p. 131;
Rosen and Schwalbe 2002a, p. 7; Casper and Hendricks 2005, p. 582;
Suhre 2008, pers. comm.; Rosen et al. 2013, pp. 35-36).
Bullfrogs are large-bodied, voracious, opportunistic, even
cannibalistic predators that readily attempt to consume any living
thing smaller than them. Bullfrogs have a highly varied diet, which has
been documented to include vegetation, invertebrates, fish, birds,
mammals, amphibians, and reptiles, including numerous species of snakes
(eight genera, including six different species of gartersnakes, two
species of rattlesnakes, and Sonoran gophersnakes (Pituophis catenifer
affinis)) (Bury and Whelan 1984, p. 5; Clarkson and DeVos 1986, p. 45;
Holm and Lowe 1995, pp. 37-38; Carpenter et al. 2002, p. 130; King et
al. 2002; Hovey and Bergen 2003, pp. 360-361; Casper and Hendricks
2005, pp. 543-544; Combs et al. 2005, p. 439; Wilcox 2005, p. 306;
DaSilva et al. 2007, p. 443; Neils and Bugbee 2007, p. 443; Rowe and
Garcia 2012, pp. 633-634). In one study, three different species of
gartersnakes (Thamnophis sirtalis, T. elegans, and T. ordinoides)
totaling 11 snakes were found inside the stomachs of resident bullfrogs
from a single region (Jancowski and Orchard 2013, p. 26). Bullfrogs can
significantly reduce or eliminate the native amphibian populations
(Moyle 1973, pp. 18-22; Conant 1974, pp. 471, 487-489; Hayes and
Jennings 1986, pp. 491-492; Rosen and Schwalbe 1988, pp. 28-30; 2002b,
pp. 232-238; Rosen et al. 1995, pp. 257-258; 2001, pp. 2, Appendix I;
Wu et al. 2005, p. 668; Pearl et al. 2004, p. 18; Kupferberg 1994, p.
95; Kupferburg 1997, pp. 1736-1751; Lawler et al. 1999; Bury and Whelan
1986, pp. 9-10; Hayes and Jennings 1986, pp. 500-501; Jones and Timmons
2010, pp. 473-474), which are vital for northern Mexican gartersnakes.
Different age classes of bullfrogs can affect native ranid
populations via different mechanisms. Juvenile bullfrogs affect native
ranids through competition; male bullfrogs affect native ranids through
predation; and female bullfrogs affect native ranids through both
mechanisms depending on body size and microhabitat (Wu et al. 2005, p.
668). Pearl et al. (2004, p. 18) also suggested that the effect of
bullfrog introductions on native ranids may be different based on
specific habitat conditions but also suggested that an individual ranid
frog species' physical ability to escape influences the effect of
bullfrogs on each native ranid community. Bullfrogs can also negatively
affect native ranid frog populations, both locally and regionally, as
carriers or reservoir species for Bd, depending on the strain of Bd
(Gervasi et al. 2013, p. 169).
Bullfrogs have been documented to occur throughout Arizona.
Holycross et al. (2006, pp. 13-14, 52-61) found bullfrogs at 55 percent
of sample sites in the Agua Fria subbasin, 62 percent of sites in the
Verde River subbasin, 25 percent of sites in the Salt River subbasin,
and 22 percent of sites in the Gila River subbasin. In total, bullfrogs
were observed at 22 of the 57 sites surveyed (39 percent) across the
Mogollon Rim (Holycross et al. 2006, p. 13). A number of authors have
also documented the presence of bullfrogs throughout many subbasins in
Arizona and New Mexico adjacent to the historical distribution of the
northern Mexican or narrow-headed gartersnake, including northern
Arizona (Sredl et al. 1995a, p. 7; 1995c, p. 7), central Arizona and
along the Mogollon Rim of Arizona and New Mexico (Nickerson and Mays
1970, p. 495; Hulse 1973, p. 278; Sredl et al. 1995b, p. 9; Drost and
Nowak 1997, p. 11; Nowak and Spille 2001, p. 11; Holycross et al. 2006,
pp. 15-51; Wallace et al. 2008; pp. 243-244; Hellekson 2012a, pers.
comm.), southern Arizona (Rosen and Schwalbe 1988, Appendix I; 1995, p.
452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-227; 2002c, pp. 31, 70;
Holm and Lowe 1995, pp. 27-35; Rosen et al. 1995, p. 254; 1996a, pp.
16-17; 1996b, pp. 8-9; 2001, Appendix I; Turner et al. 1999, p. 11;
Sredl et al. 2000, p. 10; Turner 2007; p. 41), and along the Colorado
River (Vitt and Ohmart 1978, p. 44; Clarkson and DeVos 1986, pp. 42-49;
Ohmart et al. 1988, p. 143). In one of the more conspicuous examples,
bullfrogs were identified as the primary cause for collapse of the
northern Mexican gartersnake and its prey base on the SBNWR (Rosen and
Schwalbe 1988, p. 28; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b,
pp. 223-227; 2002c, pp. 31, 70; Rosen et al. 1996b, pp. 8-9).
Once established, bullfrogs are persistent in an area and very
difficult to eradicate. Rosen and Schwalbe (1995, p. 452) experimented
with bullfrog removal at various sites on the SBNWR, in addition to a
control site with no bullfrog removal in similar habitat on the Buenos
Aires National Wildlife Refuge (BANWR). Removal of adult bullfrogs,
without removal of eggs and tadpoles, resulted in a substantial
increase in younger age-class bullfrogs where removal efforts were the
most intensive (Rosen and Schwalbe 1997, p. 6). Contradictory to the
goals of bullfrog eradication, evidence from dissection samples from
young adult and subadult bullfrogs indicated these age-classes readily
prey upon juvenile bullfrogs (up to the average adult leopard frog
size) as well as juvenile gartersnakes, which suggests that the
selective removal of only the large adult bullfrogs (presumed to be the
most dangerous size class to leopard frogs and gartersnakes), favoring
the young adult and sub-adult age classes, could indirectly lead to
increased predation of leopard frogs and juvenile gartersnakes (Rosen
and Schwalbe 1997, p. 6). These findings illustrate that, in addition
to large adults, sub-adult bullfrogs also negatively impact northern
Mexican gartersnakes and their prey species. The findings also indicate
the importance of including egg mass and tadpole removal during efforts
to control bullfrogs and timing removal projects to ensure reproductive
bullfrogs are removed prior to breeding. Recent success in regional
bullfrog eradication has been found in a few cases described below in
the section entitled ``Current Conservation of Northern Mexican and
Narrow-headed Gartersnakes.''
Bullfrogs not only compete with the northern Mexican gartersnake
for prey items but directly prey upon juvenile and, occasionally, sub-
adult northern Mexican and narrow-headed gartersnakes (Rosen and
Schwalbe 1988, pp. 28-31; 1995, p. 452; 2002b, pp. 223-227; Holm and
Lowe 1995, pp. 29-29; Rossman et al. 1996, p. 177; AGFD In Prep., p.
12; 2001, p. 3; Rosen et al. 2001, pp. 10, 21-22; Carpenter et al.
2002, p. 130; Wallace 2002, p. 116). A well-circulated photograph of an
adult bullfrog in the process of consuming a northern Mexican
gartersnake at Parker Canyon Lake, Cochise County, Arizona,
[[Page 38695]]
taken by John Carr of the AGFD in 1964, provides photographic
documentation of bullfrog predation (Rosen and Schwalbe 1988, p. 29;
1995, p. 452). The most recent, physical evidence of bullfrog predation
of northern Mexican gartersnakes is provided in photographs of a
dissected bullfrog at Pasture 9 Tank in the San Rafael Valley of
Arizona that had a freshly eaten neonatal northern Mexican gartersnake
in its stomach (Akins 2012, pers. comm.).
A common observation in northern Mexican gartersnake populations
that co-occur with bullfrogs is a preponderance of large, mature adult
snakes with conspicuously low numbers of individuals in the newborn and
juvenile age size classes. This occurs due to bullfrogs preying on
young small snakes more effectively, which leads to reduced survival of
young and depressed recruitment within populations (Rosen and Schwalbe
1988, p. 18; Holm and Lowe 1995, p. 34). In lotic (flowing water)
systems, bullfrogs prefer sites with low or limited flow, such as
backwaters, side channels, and pool habitat. These areas are also used
frequently by northern Mexican and narrow-headed gartersnakes, which
likely results in increased predation rates and likely depressed
recruitment of gartersnakes. Potential recruitment problems for
northern Mexican gartersnakes due to effects from nonnative species are
suspected at Tonto Creek (Wallace et al. 2008, pp. 243-244). Rosen and
Schwalbe (1988, p. 18) stated that the low recruitment at the SBNWR, a
typical characteristic of gartersnake populations affected by harmful
nonnative species, is the likely cause of that populations' decline and
possibly for declines in populations throughout their range in Arizona.
Specific localities within the distribution of northern Mexican and
narrow-headed gartersnakes where bullfrogs have been detected are
presented in Appendix A (available at https://www.regulations.gov,
Docket No. FWS-R2-ES-2013-0071).
Effects of Crayfish on Native Aquatic Communities (Northern Mexican and
Narrow-Headed Gartersnakes) (Factors A and C)
Crayfish are another nonnative species in Arizona and New Mexico
that threaten northern Mexican and narrow-headed gartersnakes through
competition by consuming prey species of the gartersnakes and through
direct predation on juvenile gartersnakes themselves (Fernandez and
Rosen 1996, p. 25; Voeltz 2002, pp. 87-88; USFWS 2007a, p. 22).
Rogowski et al. (2013, p. 1,280) found Arizona's aquatic communities to
be particularly vulnerable to crayfish because many endemic aquatic
species never evolved in the presence of crayfish. Fernandez and Rosen
(1996, p. 3) studied the effects of crayfish introductions on two
stream communities in Arizona, a low-elevation semi-desert stream and a
high mountain stream, and concluded that crayfish can noticeably reduce
species diversity and destabilize food chains in riparian and aquatic
ecosystems through their effect on vegetative structure, stream
substrate (stream bottom; i.e., silt, sand, cobble, boulder)
composition, and predation on eggs, larval, and adult forms of native
invertebrate and vertebrate species. Crayfish fed on embryos, tadpoles,
newly metamorphosed frogs, and adult leopard frogs, but they did not
feed on egg masses (Fernandez and Rosen 1996, p. 25). However, Gamradt
and Kats (1996, p. 1155) found that crayfish readily consumed the egg
masses of California newts (Taricha torosa). Crayfish are known to also
eat fish eggs and larva (Inman et al. 1998, p. 17), especially those
bound to the substrate (Dorn and Mittlebach 2004, p. 2135). Fernandez
and Rosen (1996, pp. 6-19, 52-56) and Rosen (1987, p. 5) discussed
observations of inverse relationships between crayfish abundance and
native reptile and amphibian populations, including narrow-headed
gartersnakes, northern leopard frogs, and Chiricahua leopard frogs.
Crayfish may also affect native fish populations. Carpenter (2005, pp.
338-340) documented that crayfish may reduce the growth rates of native
fish through competition for food and noted that the significance of
this impact may vary between species.
Crayfish alter the abundance and structure of aquatic vegetation by
grazing on aquatic and semiaquatic vegetation, which reduces the cover
needed by frogs and gartersnakes, as well as the food supply for prey
species such as tadpoles (Fernandez and Rosen 1996, pp. 10-12).
Fernandez and Rosen (1996, pp. 10-12) found that crayfish frequently
burrow into stream banks, leading to increased bank erosion, stream
turbidity, and siltation of stream bottoms. Creed (1994, p. 2098) found
that filamentous alga (Cladophora glomerata) was at least 10-fold
greater in aquatic habitats that lacked crayfish. Filamentous algae is
an important component of aquatic vegetation that provides cover for
foraging gartersnakes, as well as microhabitat for prey species, in
situations where predation risk is high.
Crayfish have recently been found to also act as a host for the
amphibian disease-causing fungus, Bd (McMahon et al. 2013, pp. 210-
213). This could have serious implications for northern Mexican
gartersnakes because crayfish can now be considered a source of disease
in habitat that is devoid of amphibians but otherwise potentially
suitable habitat for immigrating amphibians, such as leopard frogs,
which could serve as a prey base. Because crayfish are so widespread
throughout Arizona, New Mexico, and portions of Mexico, the scope of
this threat is significant for native amphibian populations and,
therefore, to northern Mexican gartersnake populations.
Inman et al. (1998, p. 3) documented crayfish as widely distributed
and locally abundant in a broad array of natural and artificial free-
flowing and still-water habitats throughout Arizona, many of which
overlap the historical and current distribution of northern Mexican and
narrow-headed gartersnakes. Hyatt (undated, p. 71) concluded that the
majority of waters in Arizona contained at least one species of
crayfish. In surveying for northern Mexican and narrow-headed
gartersnakes, Holycross et al. (2006, p. 14) found crayfish in 64
percent of the sample sites in the Agua Fria subbasin; in 85 percent of
the sites in the Verde River subbasin; in 46 percent of the sites in
the Salt River subbasin; and in 67 percent of the sites in the Gila
River subbasin. In total, crayfish were observed at 35 (61 percent) of
the 57 sites surveyed across the Mogollon Rim (Holycross et al. 2006,
p. 14), most of which were sites historically or currently occupied by
northern Mexican or narrow-headed gartersnakes, or sites the
investigators believed possessed suitable habitat and may be occupied
by these gartersnakes based upon their known historical distributions.
A number of authors have documented the presence of crayfish
through their survey efforts throughout Arizona and New Mexico in
specific regional areas, drainages, and lentic wetlands within or
adjacent to the historical distribution of the northern Mexican or
narrow-headed gartersnake, including northern Arizona (Sredl et al.
1995a, p. 7; 1995c, p. 7), central Arizona and along the Mogollon Rim
of Arizona and New Mexico (Sredl et al. 1995b, p. 9; Fernandez and
Rosen 1996, pp. 54-55, 71; Inman et al. 1998, Appendix B; Nowak and
Spille 2001, p. 33; Holycross et al. 2006, pp. 15-51; Brennan 2007, p.
7; Burger 2008, p. 4; Wallace et al. 2008; pp. 243-244; Brennan and
Rosen 2009, p. 9; Karam et al. 2009; pp. 2-3; Hellekson 2012a, pers.
comm.), southern Arizona (Rosen and Schwalbe 1988, Appendix I; Inman et
al. 1998,
[[Page 38696]]
Appendix B; Sredl et al. 2000, p. 10; Rosen et al. 2001, Appendix I),
and along the Colorado River (Ohmart et al. 1988, p. 150; Inman et al.
1998, Appendix B). Specific localities within the distribution of
northern Mexican and narrow-headed gartersnakes where crayfish have
been detected are presented in Appendix A (available at https://www.regulations.gov, Docket No. FWS-R2-ES-2013-0071). Like bullfrogs,
crayfish can be very difficult, if not impossible, to eradicate once
they have become established in an area, depending on the complexity of
the habitat (Rosen and Schwalbe 1996a, pp. 5-8; 2002a, p. 7; Hyatt
undated, pp. 63-71).
It is likely that crayfish populations, where they overlap with
northern Mexican or narrow-headed gartersnakes, could have a varied
influence on gartersnake populations. The size of crayfish can
influence their predatory influence on gartersnakes or their prey
species; small crayfish are unlikely to pose a significant threat to
gartersnakes themselves but may still consume fish eggs or fry, whereas
larger crayfish can prey on neonatal gartersnakes directly. The
presence of adequate numbers of favorable fish prey for narrow-headed
gartersnakes may counter the effects of resident crayfish to some
degree. Crayfish densities may also be affected by periodic flooding,
which is thought to reduce crayfish population densities temporarily
until recolonization occurs from the dispersal of individuals from
downstream populations. More field research is needed to fully
understand the ecological relationship between crayfish and these
gartersnakes, at least at any particular site. However, the best
available scientific and commercial information strongly suggests that
crayfish in larger size classes or in high densities are a cause for
concern for gartersnakes and their prey species, especially with other
threats simultaneously affecting gartersnake populations.
Effects of Predation-Related Injuries to Gartersnakes (Northern Mexican
and Narrow-Headed Gartersnakes) (Factor C)
The tails of gartersnakes are often broken off during predation
attempts by bullfrogs, crayfish, or other predators, and do not
regenerate. The incidence of tail breaks in gartersnakes can often be
used to assess predation pressure within gartersnake populations.
Attempted predation occurs on both sexes and all ages of gartersnakes
within a population, although some general trends have been detected.
For example, female gartersnakes may be more susceptible to predation
as evidenced by the incidence of tail damage (Willis et al. 1982, pp.
100-101; Rosen and Schwalbe 1988, p. 22; Mushinsky and Miller 1993, pp.
662-664; Fitch 2003, p. 212). This can be explained by higher basking
rates associated with pregnant females that increase their visibility
to predators. Fitch (2003, p. 212) found that tail injuries in the
common gartersnake occurred more frequently in adults than in
juveniles. Predation on juvenile snakes likely results in complete
consumption of the animal, which would limit observations of tail
injury in their age class.
Tail injuries can have negative effects on the health, longevity,
and overall success of individual gartersnakes from infection, slower
swimming and crawling speeds, or impeding reproduction. Mushinsky and
Miller (1993, pp. 662-664) commented that, while tail breakage in
gartersnakes can save the life of an individual snake, it also leads to
permanent handicapping of the snake, resulting in slower swimming and
crawling speeds, which could leave the snake more vulnerable to
predation or affect its foraging ability. Willis et al. (1982, p. 98)
discussed the incidence of tail injury in three species in the genus
Thamnophis (common gartersnake, Butler's gartersnake (T. butleri), and
the eastern ribbon snake (T. sauritus)) and concluded that individuals
that suffered nonfatal injuries prior to reaching a length of 12 in (30
cm) are not likely to survive and that physiological stress during
post-injury hibernation may play an important role in subsequent
fatality. While northern Mexican or narrow-headed gartersnakes may
survive an individual predation attempt from a bullfrog or crayfish
with tail damage, secondary effects from infection of the wound may
significantly contribute to fatality of individuals. Perry-Richardson
et al. (1990, p. 77) described the importance of tail-tip alignment in
the successful courtship and mating in Thamnophiine snakes and found
that missing or shortened tails adversely affected these activities
and, therefore, mating success. In researching the role of tail length
in mating success in the red-sided gartersnake (Thamnophis sirtalis
parietalis), Shine et al. (1999, p. 2150) found that males that
experienced injuries or the partial or whole loss of the tail
experienced a three-fold decrease in mating success.
The frequency of tail injuries can be quite high in a given
gartersnake population; for example at the SBNWR (Rosen and Schwalbe
1988, pp. 28-31), 78 percent of northern Mexican gartersnakes had
broken tails with a ``soft and club-like'' terminus, which suggests
repeated injury from multiple predation attempts by bullfrogs. While
medically examining pregnant female northern Mexican gartersnakes,
Rosen and Schwalbe (1988, p. 28) noted bleeding from the posterior
region, which suggested to the investigators the snakes suffered from
``squeeze-type'' injuries inflicted by adult bullfrogs. In another
example, Holm and Lowe (1995, pp. 33-34) observed tail injuries in 89
percent of northern Mexican gartersnakes during the early 1990s in
Scotia Canyon in the Huachuca Mountains, as well as a skewed age class
ratio that favored adults over sub-adults, which is consistent with
data collected by Willis et al. (1982, pp. 100-101) on other
gartersnake species. Bullfrogs are largely thought to be responsible
for the significant decline of northern Mexican gartersnake and its
prey base at this locality, although the latter has improved through
recovery actions. In the Black River, crayfish are very abundant and
have been identified as the likely cause for a high-frequency of tail
injuries to narrow-headed gartersnakes (Brennan 2007, p. 7; Brennan and
Rosen 2009, p. 9). Brennan (2007, p. 5) found that, in the Black River,
14 of 15 narrow-headed gartersnakes captured showed evidence of damaged
or missing tails (Brennan 2007, p. 5). In 2009, 16 of 19 narrow-headed
gartersnakes captured in the Black River showed evidence of damaged or
missing tails (Brennan and Rosen 2009, p. 8). In the middle Verde River
region, Emmons and Nowak (2013, p. 5) reported that 18 of 49 (37
percent) northern Mexican gartersnakes captured had scars (n = 17) and/
or missing tails tips (n = 7).
Vegetation or other forms of protective cover may be particularly
important for gartersnakes to reduce the effects of harmful nonnative
species on populations. For example, the population of northern Mexican
gartersnakes at the Page Springs and Bubbling Ponds State Fish
Hatcheries occurs with harmful nonnative species (Boyarski 2008b, pp.
3-4, 8). Yet, only 11 percent of northern Mexican gartersnakes captured
in 2007 were observed as having some level of tail damage (Boyarski
2008b, pp. 5, 8). The relatively low occurrence of tail damage, as
compared to 78 percent of snakes with tail damage found by Rosen and
Schwalbe (1988, pp. 28-31), may indicate: (1) Adequate vegetation
density was used by gartersnakes to avoid harmful nonnative species
predation attempts; (2) a relatively small population of harmful
nonnative species may be at a comparatively lower density than sites
sampled by previous studies
[[Page 38697]]
(harmful nonnative species population density data were not collected
by Boyarski (2008b)); (3) gartersnakes may not have needed to move
significant distances at this locality to achieve foraging success,
which might reduce the potential for encounters with harmful nonnative
species; or (4) gartersnakes infrequently escaped predation attempts by
harmful nonnative species, were removed from the population, and were
consequently not detected by surveys.
Expansion of the American Bullfrog and Crayfish in Mexico (Northern
Mexican Gartersnake) (Factors A, C, and E)
Bullfrogs are a significant threat to native aquatic and riparian
species throughout Mexico. Luja and Rodr[iacute]guez-Estrella (2008,
pp. 17-22) examined the invasion of the bullfrog in Mexico. The
earliest records of bullfrogs in Mexico were Nuevo Leon (1853),
Tamaulipas (1898), Morelos (1968), and Sinaloa (1969) (Luja and
Rodr[iacute]guez-Estrella 2008, p 20). By 1976, the bullfrog was
documented in seven more states: Aguacalientes, Baja California Sur,
Chihuahua, Distrito Federal, Puebla, San Luis Potosi, and Sonora (Luja
and Rodr[iacute]guez-Estrella 2008, p. 20). The bullfrog was recently
verified from the state of Hidalgo, Mexico, at an elevation of 8,970
feet (2,734 m), which indicates the species continues to spread in that
country and can exist even at the uppermost elevations inhabited by
northern Mexican gartersnakes (Duifhuis Rivera et al. 2008, p. 479). As
of 2008, Luja and Rodr[iacute]guez-Estrella (2008, p. 20) have recorded
bullfrogs in 20 of the 31 Mexican States (65 percent of the states in
Mexico) and suspect that they have invaded other States, but were
unable to find documentation.
Bullfrogs have been commercially produced for food in Mexico in
Yucatan, Nayarit, Morelos, Estado de Mexico, Michoac[aacute]n,
Guadalajara, San Luis Potosi, Tamaulipas, and Sonora, and their use for
food was endorsed by the Mexican Secretary of Aquaculture Support (Luja
and Rodr[iacute]guez-Estrella 2008, p. 20). However, frog legs
ultimately never gained popularity in Mexican culinary culture (Conant
1974, pp. 487-489), and Luja and Rodr[iacute]guez-Estrella (2008, p.
22) point out that only 10 percent of these farms remain in production.
Luja and Rodr[iacute]guez-Estrella (2008, pp. 20, 22) document
instances where bullfrogs have escaped production farms and suspect the
majority of the frogs that were produced commercially in farms that
have since ceased operation have assimilated into surrounding habitat.
Luja and Rodr[iacute]guez-Estrella (2008, p. 20) also state that
Mexican people deliberately introduce bullfrogs for ornamental
purposes, or ``for the simple pleasure of having them in ponds.'' The
act of deliberately releasing bullfrogs into the wild in Mexico was
cited by Luja and Rodr[iacute]guez-Estrella (2008, p. 21) as being
``more common than we can imagine.'' Bullfrogs are available for
purchase at some Mexican pet stores (Luja and Rodr[iacute]guez-Estrella
2008, p. 22). Luja and Rodr[iacute]guez-Estrella (2008, p. 21) state
that bullfrog eradication efforts in Mexico are often thwarted by their
popularity in rural communities (presumably as a food source).
Currently, no regulation exists in Mexico to address the threat of
bullfrog invasions or prevent their release into the wild (Luja and
Rodr[iacute]guez-Estrella 2008, p. 22). As a result, the bullfrogs'
distribution continues to increase in Mexico, beyond what it would
through natural dispersal mechanisms.
Rosen and Melendez (2006, p. 54) report bullfrog invasions to be
prevalent in northwestern Chihuahua and northwestern Sonora, where the
northern Mexican gartersnake is thought to occur. In many areas, native
leopard frogs were completely displaced where bullfrogs were observed.
Rosen and Melendez (2006, p. 54) also demonstrated the relationship
between fish and amphibian communities in Sonora and western Chihuahua.
Native leopard frogs, a primary prey item for the northern Mexican
gartersnake, only occurred in the absence of nonnative fish, and were
absent from waters containing nonnative species, which included several
major waters. In Sonora, Rorabaugh (2008a, p. 25) also considers the
bullfrog to be a significant threat to the northern Mexican gartersnake
and its prey base, substantiated by field observations made during
surveys conducted in Chihuahua and Sonora in 2006 (Rorabaugh 2008b, p.
1).
Few data were found on the presence or distribution of nonnative
crayfish species in Mexico. However, in a 2-week gartersnake survey
effort in 2006 in northern Mexico, crayfish were observed as ``widely
distributed'' in the valleys of western Chihuahua (Rorabaugh 2008b, p.
1). Based on the invasive nature of crayfish ecology and their
distribution in the United States along the Border region, it is
reasonable to assume that, at a minimum, crayfish are likely
distributed along the entire Border region of northern Mexico, adjacent
to where they occur in the United States, and act in a similar fashion
on affected northern Mexican gartersnake populations.
Risks to Gartersnakes From Fisheries Management Activities (Northern
Mexican and Narrow-Headed Gartersnakes) (Factors A and E)
The decline in native fish communities from the effects of harmful
nonnative fish species has spurred resource managers to take action to
help recover native fish species. While we fully support activities
designed to help recover native fish, recovery actions for native fish,
in the absence of thorough planning, can have negative effects on
resident gartersnake populations.
Piscicides--Piscicide is a term that refers to a ``fish poison.''
The use of piscicides, such as rotenone or antimycin A, for the removal
of harmful nonnative fish species has widely been considered invaluable
for the conservation and recovery of imperiled native fish species
throughout the United States, and in particular the Gila River basin of
Arizona and New Mexico (Dawson and Kolar 2003, entire). Antimycin A is
rarely used anymore due to limited production and has been largely
replaced by rotenone in field applications. Experimentation with
ammonia as a piscicide has shown promising results and may ultimately
replace rotenone in the future as a desired control method if legally
registered for such use (Ward et al. 2013, pp. 402-404). Currently,
rotenone is the most commonly used piscicide. The active ingredient in
rotenone is a natural chemical compound extracted from the stems and
roots of tropical plants in the family Leguminosae that interrupts
oxygen absorption in gill-breathing animals (Fontenot et al. 1994, pp.
150-151). In the greater Gila River subbasin alone, 57 streams or water
bodies have been treated with piscicide, some on several occasions
spanning many years (Carpenter and Terrell 2005; Table 6). However,
this practice has been the source of recent controversy due to a
perceived link between rotenone and Parkinson's disease in humans, as
well as potential effects to livestock.
Speculation of the potential role of rotenone in Parkinson's
disease was fueled by Tanner et al. (2011, entire), which correlated
the incidence of the disease with lifetime exposure to certain
pesticides, including rotenone. As a result, in 2012, the Arizona State
Legislature proposed two bills that called for the development of an
environmental impact statement prior to the application of rotenone or
antimycin A (S.B. 1453, see State of Arizona Senate (2012b)) and urged
the U.S. Environmental Protection Agency to deregister rotenone from
use in the
[[Page 38698]]
United States (S.B. 1009, see State of Arizona Senate (2012b)). Public
safety considerations were fully evaluated by a multidisciplined
technical team of specialists that found no correlation between
rotenone applications performed, according to product label
instructions, and Parkinson's disease (Rotenone Review Advisory
Committee 2012, pp. 24-25). Nonetheless, continued anxiety regarding
the use of piscicides for conservation and management of fish
communities leaves an uncertain future for this important management
tool. Should circumstances result in the discontinued practice of using
piscicides for fish recovery and management, the likelihood of recovery
for listed or sensitive aquatic vertebrates in Arizona, such as
northern Mexican and narrow-headed gartersnakes, would be substantially
reduced, if not eliminated outright.
The use of piscicides is a vital and scientifically sound tool, the
only tool, in most circumstances, for reestablishing native fish
communities and removing threats related to nonnative aquatic species
in occupied northern Mexican and narrow-headed gartersnake habitat. By
extension, the use of piscicides is also invaluable in the recovery and
conservation of northern Mexican and narrow-headed gartersnakes.
However, without proper planning the amount of time a treated water
body remains fishless post-treatment can affect gartersnakes by
removing fish, their primary food source. The time period between
rotenone applications and the subsequent restocking of native fish is
contingent on two basic variables, the time it takes for piscicide
levels to reach nontoxic levels and the level of certainty required to
ensure that renovation goals and objectives have been met prior to
restocking. Implementation of the latter consideration may vary from to
a year or longer, depending on the level of certainty required by
project proponents. Carpenter and Terrell (2005, p. 14) reported that
standard protocols used by the AGFD for Apache trout renovations at
that time required two applications of piscicide before repatriating
native fish to a stream, waiting a season to see if the renovation was
successful, and then continuing to renovate if necessary. Past
protocols have included goals for the renovated water body to remain
fishless for extended periods, sometimes up to an entire year before
restocking (Carpenter and Terrell 2005, p. 14). At a minimum and
according to our files, reaches of Big Bonito Creek, the West Fork
Black River, West Fork Gila River, Little Creek, and O'Donnell Creek
have all been subject to fish renovations using these or similarly
accepted protocols (Carpenter and Terrell 2005; Table 6; Paroz and
Propst 2009, p. 4; Hellekson 2012a, pers. comm.). Therefore, northern
Mexican or narrow-headed gartersnake populations in these streams have
likely been negatively affected, due to the eradication of a portion
of, or their entire, prey base in these systems for varying periods of
time. Big Bonito Creek was restocked with salvaged native fish shortly
after renovation occurred. However, we are uncertain how long other
stream reaches remained fishless post-treatment, but it was likely to
be a minimum of weeks in each instance, and possibly a year or longer
in some instances.
Although significant efforts are generally made to salvage as many
native fish as possible prior to treatment, logistics of holding fish
for several weeks prior to restocking limit the number of individuals
that can be held safely. Therefore, not every individual fish is
salvaged, and native fish remaining in the stream are subsequently lost
during the treatment. The number of fish subsequently restocked is,
therefore, smaller than the number of fish that were present prior to
the treatment. The full restoration of native fish populations to pre-
treatment levels may take several years, depending on the size of the
treated area and the size and maturity of the founding populations.
Restocking salvaged fish in the fall may allow natural spawning and
recruitment to begin in the spring, which would provide a more
immediate benefit to resident gartersnake populations.
Several streams within the distribution of narrow-headed
gartersnakes in New Mexico have been identified for potential future
fish barrier construction, for which piscicide applications are likely
necessary. These streams include Little Creek, West Fork Gila River,
Middle Fork Gila River, Turkey Creek, Saliz Creek, Dry Blue Creek, Iron
Creek, and the San Francisco River (Riley and Clarkson 2005, pp. 4-5,
7, 9, 12; Clarkson and Marsh 2012, p. 8; 2013, pp. 1, 4, 6; Hellekson
2013, pers. comm.). Of these, the Middle Fork Gila River and Turkey
Creek appear to the most likely chosen for renovation (Clarkson and
Marsh 2013, p. 8). Mule Creek and Cienega Creek, both occupied by
northern Mexican gartersnakes, as well as Whitewater Creek (occupied by
narrow-headed gartersnakes), are under consideration but ultimately may
not be chosen (Clarkson and Marsh 2013, pp. 8-9). Haigler Creek
(occupied by narrow-headed gartersnakes) is planned for renovation in
2015 (Burger and Jeager 2013, p. 2) and barrier development.
The current standard operating procedures for piscicide
application, as adopted nationally and provided in Finlayson et al.
(2010, p. 23), provide guidance for assuring that nontarget, baseline
environmental conditions (the biotic community) are accounted for in
assessing whether mitigation measures are necessary. This procedural
protocol states, ``Survival and recovery of the aquatic community may
be demonstrated by sampling plankton, macroinvertebrates (aquatic
insects, crustacea, leeches, and mollusks), and amphibians (frogs,
tadpoles, and larval and adult salamanders)'' (Finlayson et al. 2010,
p. 23). This protocol, adopted by the AGFD (see AGFD 2012a), does not
in itself consider the effects of leaving a treated water body without
a prey base for a sensitive species much less for a fish-specialist,
such as the narrow-headed gartersnake, for extended periods of time.
However, the AGFDs' internal Environmental Assessment Checklist (EAC)
addresses considerations for nontarget aquatic reptiles. Thus, we
believe that concerns for potential effects of piscicide treatments on
these gartersnake species within Arizona should not be substantial in
the future.
As of 2012, a new policy was finalized by the AGFD that includes an
early and widespread public notification and planning process that
involves the approval of several decision-makers within four major
stages: (1) Piscicide project internal review and approval; (2)
preliminary planning and public involvement; (3) intermediate planning
and public involvement; and (4) project implementation and evaluation
(AGFD 2012a, p. 3). Within the Internal Review and Approval stage of
the process, sensitive, endemic, and listed species potentially
impacted by the project must be identified (AGFD 2012a, p. 13), such as
northern Mexican or narrow-headed gartersnakes. This change ensures
that an analysis of potential effects to nontarget wildlife by
fisheries management activities occurs within the same planning
document, versus a separate process. In addition, the AGFD's
Conservation and Mitigation Program has specifically committed to
quickly restocking renovated streams that are occupied by either
northern Mexican or narrow-headed gartersnakes (USFWS 2011, Appendix
C).
Piscicide application protocols used by the New Mexico Department
of Game and Fish are provided in Pierce (2014,
[[Page 38699]]
entire) and specify that effects to amphibian species are reviewed
prior to application; however, the protocol does not provide for an
assessment of potential gartersnake effects from treatment. No specific
timeframe, post-treatment, was recommended by the protocol for when
native fish are recommended for stocking into treated waters (Pierce
2014, pers. comm.). We intend to coordinate with the New Mexico
Department of Game and Fish as active partners in wildlife conservation
to ensure potential effects, from piscicide treatments, to either
gartersnake are avoided or minimized. However, if proper protocols are
not incorporated into future fish restoration projects, these
activities will continue to threaten local gartersnake populations.
Mechanical Methods--In addition to chemical renovation techniques,
mechanical methods using electroshocking equipment are often used in
fisheries management, both for nonnative aquatic species removal and
fisheries survey and monitoring activities that often occur in
conjunction with piscicide treatments. Northern Mexican and narrow-
headed gartersnakes often flee into the water as a first line of
defense when startled. In occupied habitat, gartersnakes present in the
water and within the affected radius of electroshockers are often
temporarily paralyzed from electrical impulses intended for fish, and
are, therefore, readily detected by surveyors (Hellekson 2012a, pers.
comm.). We are not aware of any research that has investigated
potential short- or long-term consequences to gartersnakes from these
events, and so we do not consider electroshock surveys as a substantial
threat to either gartersnake.
Trapping methods are also used in fisheries surveys, for other
applications in aquatic species management, and for the collection of
live baitfish in recreational fishing. One such common method to study
aquatic or semi-aquatic wildlife (including populations of aquatic
snakes such as gartersnakes) is through the use of wire minnow traps.
When used to monitor gartersnake populations, wire minnow traps are
anchored to vegetation, logs, etc., along the shoreline (in most
applications) and positioned so that half to one-third of the trap,
along its lateral line, is above the water surface to allow snakes to
surface for air. These traps often attract prey species, such as small
fishes and amphibian larvae (when present), and, therefore, become
self-baiting. They are then checked according to a predetermined
schedule. Because the wire, twine, etc., used to anchor these traps is
fixed in length, these traps may become fully submerged if there is a
sudden, unanticipated rise in water levels (e.g., storm event). During
the monsoon in Arizona and New Mexico, these types of storm events are
common, and river hydrographs respond accordingly with rapid and
dynamic increases in flow.
We are aware of examples where northern Mexican gartersnakes,
intentionally captured in minnow traps, have drowned as a direct result
of a rapid, unexpected rise in water levels. Some examples include an
adult female northern Mexican gartersnake along lower Tonto Creek in
2004, an adult and two neonates at the Bubbling Ponds State Fish
Hatchery in 2009 and 2010, respectively, and an individual of
undisclosed age in the upper Santa Cruz River (Holycross et al. 2006,
p. 41, Boyarski 2011, pp. 2-3; Lashway 2012, p. 5). In another example,
involving an underwater funnel trap used to survey for lowland leopard
frogs (but which are not used for fishery surveys), a large adult
female northern Mexican gartersnake was discovered deceased in the trap
(Jones 2012a, pers. comm.). Death of that individual was likely due to
drowning or predation by numerous crayfish that were also confined in
the funnel trap with the gartersnake (Jones 2012a, pers. comm.).
Depending on the mesh size of traps, neonatal gartersnakes can become
stuck in the mesh of traps (Lashway 2012, p. 5), which could result in
injury or death of the individual. There are likely additional cases
where northern Mexican or narrow-headed gartersnake fatality from
trapping has not been reported, particularly where trapping has
occurred in occupied habitat prone to flash flooding.
Minnow traps are often deployed for monitoring fully aquatic
species, such as fish, and are, therefore, intentionally positioned in
the water column where they are fully under water. Traps used for this
purpose may be checked less frequently, because risks to gill-breathing
aquatic species are less if held in the trap for longer periods of
time. As fish collectively become trapped, the trap becomes
incidentally self-baited for gartersnakes and, if deployed in habitat
occupied by either northern Mexican or narrow-headed gartersnakes,
these traps may accidentally attract, capture, and drown gartersnakes
that are actively foraging under water and are lured to the traps
because of captured prey species. Neonatal northern Mexican and narrow-
headed gartersnakes can also wriggle through the mesh of some wire
minnow traps and become lodged halfway through, depending on the pore
size of the wire mesh (Jaeger 2012, pers. comm.). If not found in time,
this situation would likely result in their death from drowning,
predation, or exposure.
The use of minnow traps is also allowed in recreational fishing in
Arizona and New Mexico (AGFD 2013a, p. 57; New Mexico Department of
Game and Fish (NMDGF) 2013, p. 17). In Arizona and New Mexico, it is
lawful to set minnow traps for the collection of live baitfish (AGFD
2013a, pp. 56-57; NMDGF 2013, p. 17). In Arizona, minnow traps used for
collecting live baitfish must be checked once daily and the trapping
activity must occur where captured bait will be used (AGFD 2013a, pp.
56-57); in New Mexico, there is no stipulation on time intervals in the
regulations to check minnow traps (NMDGF 2013, p. 17). In either
scenario in either state, these minnow traps are likely to be fully
submerged when in use and pose a drowning hazard to resident
gartersnakes while foraging underwater, as they can be lured into the
traps by fish already caught.
We do not have adequate information to assess the frequency and
geographical extent to which accidental drownings of gartersnakes in
minnow traps may be occurring. This is mainly because it happens
incidentally as a result of trapping efforts for other species, and so
it historically did not get reported by researchers. Without additional
information, we cannot conclude at this time that deaths from
accidental minnow trapping are likely having population-level effects
on either gartersnake. However, if even a few adult females are lost
from populations that already have low densities and low rates of
recruitment, these losses would contribute to population extirpations
and the continued decline in the status of the gartersnakes. Working
with researchers in the future to minimize the chances of snake
drownings and to report any incidental collections of gartersnakes will
be important for future conservation of both species.
Intentional Dewatering--Lastly, dewatering or water fluctuation
techniques are sometimes considered for eliminating undesirable fish
species from water bodies (Finlayson et al. 2010, p. 4). Dewatering of
occupied northern Mexican or narrow-headed gartersnake habitat would
have deleterious effects to affected populations by removing a primary
habitat feature and eliminating the prey base. Because northern Mexican
gartersnakes often occupy lentic water bodies or intermittently watered
canyon bottoms, where this practice is most feasible, effects of
dewatering activities may disproportionately affect that
[[Page 38700]]
species. This technique is being considered by the AGFD for pools
within Redrock Canyon where northern Mexican gartersnakes could be
adversely affected. We have been made aware that northern Mexican
gartersnakes are being considered by the AGFD in their implementation
planning process. Depending on the availability of suitable habitat
regionally and the length of time water is absent, these activities may
ultimately cause local extirpations of gartersnake populations.
Summary
In our review of the scientific and commercial literature, we have
found that over time, native aquatic communities, specifically the
native prey bases for northern Mexican and narrow-headed gartersnakes,
have been substantially weakened as a result of the cumulative effects
of disease and harmful nonnative species. Harmful nonnative species
have been intentionally introduced or have naturally dispersed into
virtually every subbasin throughout the distribution of northern
Mexican and narrow-headed gartersnakes in the United States and Mexico.
According to Geographic Information System (GIS) analyses, nonnative,
predatory fish are known to occur in 90 percent of the historical
distribution of the northern Mexican gartersnake and 85 percent of the
historical distribution of the narrow-headed gartersnake in the United
States. Bullfrogs are known to occur in 85 percent of the historical
distribution of the northern Mexican gartersnake and 53 percent of the
historical distribution of the narrow-headed gartersnake in the United
States. Crayfish are known to occur in 77 percent of the historical
distribution of the northern Mexican gartersnake and 75 percent of the
historical distribution of the narrow-headed gartersnake in the United
States. Nonnative, predatory fish, bullfrogs, and crayfish are known to
occur simultaneously in 65 percent of the historical distribution of
the northern Mexican gartersnake and 44 percent of the historical
distribution of the narrow-headed gartersnake in the United States.
Native fish are important prey for northern Mexican gartersnakes
but much more so for narrow-headed gartersnakes. Predation by and
competition with primarily nonnative, predatory fish species, and
secondarily with brown trout and crayfish, are widely considered to be
the primary reason for major declines in native fish communities
throughout the range of both gartersnakes. In Arizona, 19 of 31 (61
percent) of all native fish species are listed under the Act.
Consequently, Arizona ranks the highest of all 50 States in the
percentage of native fish species with declining trends (85.7 percent).
Similar trends in the loss of native fish biodiversity have been
described in New Mexico and Mexico. Native amphibians such as the
Chiricahua leopard frog, an important component of the northern Mexican
gartersnake prey base, have declined significantly and may face future
declines as a result of Bd and harmful nonnative species. Historical
native frog populations have been wholly replaced by harmful nonnative
species, both on local and regional scales. These declines have
directly contributed to subsequent northern Mexican gartersnake
population declines or extirpations in these areas. An adequate native
prey base is essential to the conservation and recovery of northern
Mexican gartersnakes, and this native ranid frog prey base faces an
uncertain future if harmful nonnative species continue to persist and
expand their distributions in occupied habitat.
The best available commercial and scientific information confirms
that harmful nonnative species are the most important threat to
northern Mexican and narrow-headed gartersnakes and their prey bases,
and they have had a profound role in their decline. A large body of
literature documents that northern Mexican and narrow-headed
gartersnakes are uniquely susceptible to the influence of harmful
nonnative species in their biotic communities. This sensitivity is
largely the result of complex ecological interactions that result in
direct predation on gartersnakes; shifts in biotic community structure
from largely native to largely nonnative; and competition for a
diminished prey base that can ultimately result in the injury,
starvation, or death of northern Mexican or narrow-headed gartersnakes
followed by reduced recruitment, population declines, and extirpations.
Lastly, fisheries management activities can have negative effects
on gartersnake populations when gartersnakes are not considered in
project planning and implementation. The use of rotenone and other
fisheries management techniques are important in the conservation and
recovery of native fish. However, significant threats can occur if
streams are left without an intact fish community for extended periods
of time. New policies and mitigation measures have been developed in
Arizona that will reduce the likelihood of these activities having
negative effects on either northern Mexican or narrow-headed
gartersnake populations in the future. However, some level of effect is
still expected based on logistical complications and complexities of
restoring fish populations to pre-treatment levels. We expect to
coordinate with resource managers in New Mexico as we do in Arizona, to
ensure gartersnake populations are not significantly affected by these
activities. However, if proper protocols are not incorporated into
future fish restoration projects, these activities will continue to
threaten local gartersnake populations. Other mechanisms or activities
used in fisheries management, such as electroshocking, trapping, or
dewatering, can result in the injury or death of northern Mexican or
narrow-headed gartersnakes, where these activities coincide with extant
populations, and if they have not been considered in the planning or
implementation processes. The significance of these losses depends on
the status of the gartersnake population affected and whether or not
either gartersnake, as appropriate, was considered in project planning.
If similar fisheries management techniques are used in Mexico, we
conclude that the northern Mexican gartersnake populations in Mexico
are threatened by the same mechanisms described above.
The presence of harmful nonnative species ultimately affects where
northern Mexican and narrow-headed gartersnakes can live as viable
populations. Collectively, the ubiquitous presence of harmful nonnative
species across the landscape has appreciably reduced the quantity of
suitable gartersnake habitat and changed its spatial orientation on the
landscape. Most northern Mexican and narrow-headed gartersnake
populations, even some considered viable today, live in the presence of
harmful nonnative species. While they continue to persist, they do so
under constant threat from unnatural levels of predation and
competition associated with harmful nonnative species. This weakens
their resistance to other threats, including those that affect the
physical suitability of their habitat (discussed below). This
ultimately renders populations much less resilient to stochastic,
natural, or anthropogenic stressors that could otherwise be withstood.
Over time and space, subsequent population declines have threatened the
genetic representation of each species because many populations have
become disconnected and isolated from neighboring populations.
Expanding distances between extant populations coupled with increasing
populations of
[[Page 38701]]
harmful nonnative species prevents normal colonizing mechanisms that
would otherwise reestablish populations where they have become
extirpated. This subsequently leads to a reduction in species
redundancy when isolated, small populations are at increased
vulnerability to the effects of stochastic events, without a means for
natural recolonization. Ultimately, the effect of scattered, small, and
disjunct populations, without the means to naturally recolonize, is
weakened species resiliency as a whole, which ultimately enhances the
risk of either or both species becoming endangered.
Therefore, based on the best available scientific and commercial
information, we conclude that harmful nonnative species are the most
significant threat to both the northern Mexican and narrow-headed
gartersnake, rangewide. We expect the impacts from harmful nonnative
species to only increase in the foreseeable future. The effects of
these threats on both gartersnakes have resulted in the extirpation of
a few populations already and the decline in abundance in the vast
majority of populations, so we expect the results of continuing decline
of the gartersnakes, in terms of additional population losses and
increased risk of extinction in the foreseeable future, which we
consider as the next several decades.
Main Factors That Destroy or Modify the Physical Habitat of Northern
Mexican and Narrow-Headed Gartersnakes (Factor A)
Relationship Between Harmful Nonnative Species and Adverse Effects to
Physical Habitat (Northern Mexican and Narrow-headed Gartersnakes)
The presence or absence of harmful nonnative species in occupied
gartersnake habitat affects the tolerance, or sensitivity, of
gartersnake populations to factors or activities that threaten to
modify or destroy components of their physical habitat. When we use the
term ``physical habitat,'' we refer to the structural integrity of
aquatic and terrestrial components to habitat, such as plant species
richness and density, available water, stream banks and substrates, and
any habitat feature that does not pertain to the animal community,
which we also define as a habitat component. The animal community (the
prey and predator species that co-occur within habitat) is not
considered in our usage of ``physical habitat,'' for reasons described
immediately below. In the presence of harmful nonnative species,
gartersnake populations are more sensitive to alterations in their
physical habitat. In the absence of harmful nonnative species,
gartersnake populations have shown resiliency, or tolerance, to changes
in their physical habitat.
As discussed above, we found harmful nonnative species to be a
significant and widespread factor that continues to drive further
declines in and extirpations of gartersnake populations. Furthermore,
we found various activities have affected, and continue to affect,
primary components of the physical habitat required by northern Mexican
and narrow-headed gartersnakes, even when the potential impact of
harmful nonnatives is absent. These activities, such as dams, water
diversions, groundwater pumping, and residential and commercial
development, result in the loss of stream flow. The period from 1850 to
1940 marked the greatest loss and degradation of riparian and aquatic
communities in Arizona, many of which were caused by anthropogenic
(human-caused) land uses (Stromberg et al. 1996, p. 114; Webb and Leake
2005, pp. 305-310). An estimated one-third of Arizona's wetlands has
dried or is no longer suitable (Yuhas 1996, entire). However, not all
aquatic and riparian habitats in the United States that support
northern Mexican or narrow-headed gartersnakes have been degraded or
lost. Despite the loss or modification of aquatic and riparian habitat,
large reaches of the Verde, Salt, San Pedro, and Gila Rivers, as well
as several of their tributaries, remain functionally suitable as
physical habitat for either gartersnake species.
Our treatment of how the loss or modification of physical habitat
may affect the northern Mexican or narrow-headed gartersnake is based,
in part, on recent observations made in Mexico that illustrate the
relationship of gartersnakes' physical habitat suitability to the
presence of native prey species and the lack of harmful nonnative
species, and the presence, or lack thereof, of attributes associated
with these gartersnakes' physical habitat. In 2007, two groups
consisting of agency biologists (including U.S. Fish and Wildlife
Service staff), species experts, and field technicians conducted
numerous gartersnake surveys in Durango and Chihuahua, Mexico (Burger
2007, p. 1; Burger et al. 2010, entire).
While considerable gartersnake habitat in Mexico is affected by the
presence of harmful nonnative species (Conant 1974, pp. 471, 487-489;
Contreras Balderas and Lozano 1994, pp. 383-384; Unmack and Fagan 2004,
p. 233; Miller et al. 2005, pp. 60-61; Rosen and Melendez 2006, p. 54;
Luja and Rodr[iacute]guez-Estrella 2008, pp. 17-22), Burger (2007, pp.
1-72) surveyed several sites in remote areas that appeared to be free
of nonnative species. In some sites, the physical habitat for northern
Mexican gartersnakes and similar species of gartersnakes appeared to be
in largely good condition, but few or no gartersnakes were detected. At
other sites, the physical habitat was drastically affected by
overgrazing, rural development, or road crossings; however,
gartersnakes were relatively easily detected, indicating seemingly
adequate population densities, but we do not have the necessary data to
calculate population trends at sampled localities. Inversely,
gartersnake habitat in Arizona and New Mexico is in relatively better
physical condition compared to observations of these habitats made in
Durango and Chihuahua, Mexico. However, harmful nonnative species are
essentially ubiquitous in the southwestern United States, based on our
literature review and GIS modeling. Several sites visited by Burger
(2007, pp. 1-72) in Durango and Chihuahua, Mexico, had physical habitat
in poor to very poor condition, but were largely free of nonnative
species. These situations are rarely encountered in Arizona and New
Mexico and, therefore, provided Burger (2007, entire) a unique
opportunity to examine differences in gartersnake population densities
based on condition of the physical habitat, without the confounding
effect of harmful nonnative species on resident gartersnake
populations.
Our observations of gartersnake populations in Mexico provide
evidence for the relative importance of native prey species and the
lack of nonnative species in comparison to the physical attributes of
gartersnake habitat. For example, Burger (2007, pp. 6, 12, 36, 41, 58,
63) detected moderate to high densities of gartersnakes at six sites
where their physical habitat was moderately to highly impacted by land
uses but were largely free of nonnatives. Burger (2007, pp. 18, 26, 32,
61, 64, 66, 67, 69, 72) also detected either low densities or no
gartersnakes at nine sites where the physical habitat was in moderate
to good condition but where nonnative species were detected. Eight
streams surveyed by Burger (2007, pp. 15, 22, 46, 49, 51-52, 54, 62)
had little to no surface flow, were without fish detections and had few
to no gartersnake observations. As a result, we have formulated three
general hypotheses: (1) Northern Mexican and narrow-headed gartersnakes
may be
[[Page 38702]]
more resilient to adverse effects to physical habitat in the absence of
harmful nonnative species and, therefore, more sensitive to negative
effects to physical habitat in the presence of harmful nonnative
species; (2) the presence of an adequate prey base is important for
persistence of gartersnake populations regardless of whether or not
harmful nonnative species are present; and (3) detections and effects
from harmful nonnative species appear to decrease from north to south
in the Mexican states of Chihuahua and Durango (from the United States-
Mexico International Border), as discussed in Unmack and Fagan (2004,
pp. 233-243).
Based on field data collected by Burger (2007, entire), Burger et
al. (2010, entire), and on the above hypotheses, we evaluated effects
to physical habitat in the context of the presence or absence of
nonnative species. Effects to the physical habitat of gartersnakes can
have varying effects on the gartersnakes themselves depending on the
composition of their biotic community. In the presence of harmful
nonnative species, effects to physical habitat, especially those that
diminish or weaken the gartersnake prey base, are believed to be
comparatively more significant than those that do not. As previously
discussed, harmful nonnative species are essentially ubiquitous in
Arizona and New Mexico where the northern Mexican and narrow-headed
gartersnakes occur and, therefore, exacerbate the effects from
activities or factors that modify or destroy their physical habitat.
Altering or Dewatering Aquatic Habitat (Northern Mexican and Narrow-
headed Gartersnakes)
Dams and Diversions (Northern Mexican and Narrow-headed
Gartersnakes)--The presence of water is critical for northern Mexican
and narrow-headed gartersnakes, as well as their prey base. Activities
that reduce flows or dewater habitat, such as dams, diversions, flood-
control projects, and groundwater pumping, seriously threaten the
physical habitat of the gartersnakes, because both fish and amphibians
must have water to survive and reproduce and without this prey base,
gartersnakes cannot persist. Such activities are widespread in Arizona.
For example, municipal water use in central Arizona increased by 39
percent from 1998 to 2006 (American Rivers 2006), and at least 35
percent of Arizona's perennial rivers have been dewatered, assisted by
approximately 95 dams that are in operation in Arizona today (Turner
and List 2007, pp. 3, 9). Larger dams may prevent movement of fish
between populations (which affects prey availability for northern
Mexican and narrow-headed gartersnakes) and dramatically alter the flow
regime of streams through the impoundment of water (Ligon et al. 1995,
pp. 184-189). These diversions also require periodic maintenance and
reconstruction, resulting in potential habitat damages and inputs of
sediment into the active stream.
Flow regimes within stream systems are a primary factor that shape
fish community assemblages. The timing, duration, intensity, and
frequency of flood events has been altered to varying degrees by the
presence of dams, which has an effect on fish communities (Rinne et al.
1998, pp. 8-10; 2005, p. 2). Specifically, Haney et al. (2008, p. 61)
suggested that flood pulses may help to reduce populations of nonnative
species, and efforts to increase the baseflows may assist in sustaining
native prey species for northern Mexican and narrow-headed
gartersnakes. However, the investigators in this study also suggest
that, because the northern Mexican gartersnake preys on both fish and
frogs, it may be less affected by reductions in baseflow of streams
(Haney et al. 2008, pp. 82, 93). The effect of regulated flow regimes
on the fish community in the Bill Williams River was studied by Pool
and Olden (2014 In press, p. 5), who found the presence of Alamo Dam
having a negative effect on native fish, while benefitting harmful
nonnative species, which now account for the majority of the fish
fauna, in terms of species composition and relative biomass, in the
Bill Williams River.
Other streams that are not dammed in the same watershed still
reflect a largely native fish community due to the presence of a
natural flow regime (Pool and Olden 2014 In press, pp. 5-6). Collier et
al. (1996, p. 16) mentions that water development projects are one of
two main causes for the decline of native fish in the Salt and Gila
rivers of Arizona. Unregulated flows with elevated discharge events
favor native species, and regulated flows, absent significant discharge
events, favor nonnative species (Propst et al. 2008, p. 1246).
Interactions among native fish, nonnative fish, and flow regimes were
observed in the upper reaches of the East Fork of the Gila River. Prior
to the 1983 and 1984 floods in the Gila River system, native fish
occurrence was limited, while nonnative fish were moderately common.
Following the 1983 flood event, adult nonnative predators were
generally absent, and native fish were subsequently collected in
moderate numbers in 1985 (Propst et al. 1986, p. 83). These
relationships are most readily observed in canyon-bound streams, where
shelter sought by nonnative species during large-scale floods is
minimal (Propst et al. 2008, p. 1249). Propst et al. (2008, p. 1246)
also suggested the effect of nonnative fish species on native fish
communities may be most significant during periods of natural drought
(simulated by artificial dewatering).
Effects from flood control projects threaten riparian and aquatic
habitat, as well as threaten the northern Mexican gartersnake directly
in lower Tonto Creek. Kimmell (2008, pers. comm.), Gila County Board of
Supervisors (2008, pers. comm.), Trammell (2008, pers. comm.), and
Sanchez (2008, pers. comm.) all discuss a growing concern of residents
that live within or adjacent to the floodplain of Tonto Creek in Gila
County, Arizona, both upstream and downstream of the town of Gisela,
Arizona. Specifically, there is growing concern to address threats to
private property and associated infrastructure posed by flooding of
Tonto Creek (Sanchez 2008, pers. comm.). An important remaining
population of northern Mexican gartersnakes within the Salt River
subbasin occurs on Tonto Creek. In Resolution No. 08-06-02, the Gila
County Board of Supervisors proactively declared a state of emergency
within Gila County as a result of the expectation for heavy rain and
snowfall causing repetitive flooding conditions (Gila County Board of
Supervisors 2008, pers. comm.). In response, the Arizona Division of
Emergency Management called meetings and initiated discussions among
stakeholders in an attempt to mitigate these flooding concerns (Kimmell
2008, pers. comm., Trammell 2008, pers. comm.).
Mitigation measures that have been discussed include removal of
riparian vegetation, removal of debris piles, potential channelization
of Tonto Creek, improvements to existing flood control structures or
addition of new structures, and the construction of new bridges.
Adverse effects from these types of activities to aquatic and riparian
habitat, and to the northern Mexican gartersnake or its prey species,
will result from the physical alteration or destruction of habitat,
significant increases to flow velocity, and removal of key foraging
habitat and areas to hibernate, such as debris jams. Specifically,
flood control projects permanently alter stream flow characteristics
and have the potential to make the stream unsuitable as habitat for the
northern Mexican gartersnake by reducing or eliminating stream
sinuosity
[[Page 38703]]
and associated pool and backwater habitats that are critical to
northern Mexican gartersnakes and their prey species. Threats presented
by these flood control planning efforts are considered imminent within
the next decade because high flows associated with the monsoon are
expected to increase in both intensity and frequency according to
climate change predictions, as discussed below in the section ``Climate
Change and Drought.''
Many streams in New Mexico, currently or formerly occupied by
northern Mexican or narrow-headed gartersnakes, have been or could be
affected by water withdrawals. Approximately 9.5 river mi (15.3 km) of
the Gila River mainstem in New Mexico, from Little Creek to the Gila
Bird Area, are in private ownership and have been channelized, and the
water is largely used for agricultural purposes (Hellekson 2012a, pers.
comm.). Below the Highway 180 crossing of the mainstem Gila River,
several water diversions have reduced stream flow (Hellekson 2012a,
pers. comm.). Channelization has also affected a privately owned reach
of Whitewater Creek from the Catwalk downstream to Glenwood, New Mexico
(Hellekson 2012a, pers. comm.). The Gila River downstream of the town
of Cliff, New Mexico, flows through a broad valley where irrigated
agriculture and livestock grazing are the predominant uses. Human
settlement has increased since 1988 (Propst et al. 2008, pp. 1237-
1238). Agricultural practices have led to dewatering of the river in
the Cliff-Gila valley at times during the dry season (Soles 2003, p.
71). For those portions of the Gila River downstream of the Arizona-New
Mexico border, agricultural diversions and groundwater pumping have
caused declines in the water table, and surface flows in the central
portion of the river basin are diverted for agriculture (Leopold 1997,
pp. 63-64; Tellman et al. 1997, pp. 101-104).
The San Francisco River in New Mexico has undergone sedimentation,
riparian habitat degradation, and extensive water diversion, and at
present has an undependable water supply throughout portions of its
length (Hellekson 2012a, pers. comm.; 2013, pers. comm.). The San
Francisco River is seasonally dry in the Alma Valley, and two diversion
structures fragment habitat in the upper Alma Valley and at Pleasanton
(NMDGF 2006, p. 302). An approximate 2-stream-mi (3.2-km) reach of the
lower San Francisco River between the Glenwood Diversion and Alma
Bridge, which would otherwise be good narrow-headed gartersnake
habitat, has been completely dewatered by upstream diversions
(Hellekson 2012a, pers. comm.).
Additional withdrawals of water from the Gila and San Francisco
Rivers may occur in the next several decades as the effects of drought
and human population levels increase. Implementation of Title II of the
Arizona Water Settlements Act (AWSA) (Public Law 108-451) would
facilitate the exchange of Central Arizona Project water within and
between southwestern river basins in Arizona and New Mexico, and may
result in the construction of new water development projects. Section
212 of the AWSA pertains to the New Mexico Unit of the Central Arizona
Project. The AWSA provides for New Mexico water users to deplete 14,000
acre-feet of additional water from the Gila Basin in any 10-year
period. The settlement also provides the ability to divert that water
without complaint from downstream pre-1968 water rights in Arizona. New
Mexico will receive $66 million to $128 million in non-reimbursable
Federal funding. The Interstate Stream Commission (ISC) funds may be
used to cover costs of an actual water supply project, planning,
environmental mitigation, or restoration activities associated with or
necessary for the project, and may be used on one or more of 15
alternative projects ranging from Gila National Forest San Francisco
River Diversion/Ditch improvements to a regional water supply project
(the Deming Diversion Project). Currently, 3 of the 15 projects under
consideration include elements of diversion or storage. At this time,
it is not known how the funds will be spent or which potential
alternatives may be chosen. While multiple potential project proposals
have been accepted by the New Mexico Office of the State Engineer
(NMOSE) (NMOSE 2011a, p. 1), implementation of the AWSA is still in the
planning stages on these streams, and final notice is expected by the
end of 2014. Should water be diverted from the Gila or San Francisco
Rivers, flows would be diminished and direct and indirect losses and
degradation of habitat for the narrow-headed gartersnake and its prey
species would result.
In addition to affecting the natural behavior of streams and rivers
through changes in timing, intensity, and duration of flood events,
dams create reservoirs that alter resident fish communities (Paradzick
et al. 2006, entire). Water level fluctuation can affect the degree of
benefit to harmful nonnative fish species. Reservoirs that experience
limited or slow fluctuations in water levels are especially beneficial
to harmful nonnative species whereas reservoirs that experience greater
fluctuations in water levels provide less benefit for harmful nonnative
species (Paradzick et al. 2006, entire). The timing of fluctuating
water levels contributes to their effect; a precipitous drop in water
levels during harmful nonnative fish reproduction is most deleterious
to their recruitment (Paradzick et al. 2006, entire). A drop in water
levels outside of the reproductive season of harmful nonnative species
has less effect on overall population dynamics (Paradzick et al. 2006,
entire). Large dams can also act as fish barriers, which prevent
upstream migration of harmful nonnative fish that occur downstream of
these structures.
The cross-sectional profile of any given reservoir also contributes
to its benefit for harmful nonnative fish species (Paradzick et al.
2006, entire). Shallow reservoir profiles generally provide maximum
space and elevated water temperatures favorable to reproduction of
harmful nonnative species, while deep reservoir profiles, with limited
shallow areas, provide commensurately less benefit (Paradzick et al.
2006, entire). Examples of reservoirs that benefit harmful nonnative
species, and therefore adversely affect northern Mexican and narrow-
headed gartersnakes (presently or historically), include Horseshoe and
Bartlett Reservoirs on the Verde River, and Roosevelt, Saguaro, Canyon,
and Apache Lakes on the Salt River. The Salt River Project (SRP)
operates the previously mentioned reservoirs on the Verde and Salt
Rivers and, in the case of Horseshoe and Bartlett Reservoirs, received
section 10(a)(1)(B) take authorization under the Act for adverse
effects to several avian and aquatic species (including northern
Mexican and narrow-headed gartersnakes) through a comprehensive threat
minimization and mitigation program found in SRP's habitat conservation
plan (SRP 2008, entire). There is no such minimization and mitigation
program developed for the operation of Lake Roosevelt, where
comparatively limited fluctuation in reservoir levels benefit harmful
nonnative species and negatively affect northern Mexican or narrow-
headed gartersnakes and their prey bases in Tonto Creek. A detailed
analysis of the effects of reservoir operations on aquatic communities
is provided in our intra-Service biological and conference opinion
provided in USFWS (2008, pp. 112-131).
The Effect of Human Population Growth and Development on Water
Demands and Gartersnake Habitat (Northern Mexican and Narrow-headed
[[Page 38704]]
Gartersnakes)--Arizona's population is expected to double from 5
million to 10 million people by the year 2030, which will put
increasing pressure on water demands (Overpeck 2008, entire). Arizona
increased its population by 474 percent from 1960 to 2006 (Gammage
2008, p. 15) and is second only to Nevada as the fastest growing State
in terms of human population (Social Science Data Analysis Network
(SSDAR) (2000, p. 1). Over approximately the same time period,
population growth rates in Arizona counties where northern Mexican or
narrow-headed gartersnake habitat exists have varied by county but are
no less remarkable, and all are increasing: Maricopa (463 percent);
Pima (318 percent); Santa Cruz (355 percent); Cochise (214 percent);
Yavapai (579 percent); Gila (199 percent); Graham (238 percent); Apache
(228 percent); Navajo (257 percent); Yuma (346 percent); LaPaz (142
percent); and Mohave (2,004 percent) (SSDAR 2000, entire). From 1960 to
2006, the Phoenix metropolitan area alone grew by 608 percent, and the
Tucson metropolitan area grew by 356 percent (Gammage 2008, p. 15).
Population growth in Arizona is expected to be focused along wide
swaths of land from the international border in Nogales, through
Tucson, Phoenix, and north into Yavapai County (called the Sun Corridor
``Megapolitan'') and is predicted to have 8 million people by 2030, an
82.5 percent increase from 2000 (Gammage et al. 2008, pp. 15, 22-23).
If build-out occurs as expected, it could indirectly affect (through
increased recreation pressure and demand for water) currently occupied
habitat for the northern Mexican or narrow-headed gartersnake,
particularly regional populations in lower Cienega Creek near Vail,
Arizona, and the Verde Valley, and, to a lesser extent, Red Rock Canyon
in extreme south-central Arizona.
The effect of the increased water withdrawals may be exacerbated by
the current, long-term drought facing the arid southwestern United
States, which is predicted to continue. The effect of long-term drought
has already been observed in the Southwest. Philips and Thomas (2005,
pp. 1-4) provided stream flow records that indicate that the drought
Arizona experienced between 1999 and 2004 was the worst drought since
the early 1940s and possibly earlier. The Arizona Drought Preparedness
Plan Monitoring Technical Committee (ADPPMTC) (2012) determined the
drought status within the Arizona distributions of northern Mexican and
narrow-headed gartersnakes, through June 2012, to be in ``severe
drought.'' Ongoing drought conditions have depleted recharge of
aquifers and decreased base flows in the region. While drought periods
have been relatively numerous in the arid Southwest from the mid-1800s
to the present, the effects of human-caused impacts on riparian and
aquatic communities have compromised the ability of these communities
to function under the additional stress of prolonged drought
conditions. Below we further discuss the effect of climate change-
induced drought in the future.
The Arizona Department of Water Resources (ADWR) manages water
supplies in Arizona and has established five Active Management Areas
(AMAs) across the State (ADWR 2006, entire). An AMA is established by
ADWR when an area's water demand has exceeded the groundwater supply
and an overdraft has occurred. In these areas, groundwater use has
exceeded the rate where precipitation can recharge the aquifer, and
these areas are subject to regulation pursuant to Arizona's Groundwater
Code with a goal of balancing groundwater use with recharge (reaching
safe yield) by the year 2025. Geographically, these five AMAs overlap
the historical distribution of the northern Mexican or narrow-headed
gartersnake, or both, in Arizona. The establishment of these AMAs
further illustrates the condition of limited water availability for
riparian habitat in these areas both currently and into the future, and
they indicate a cause of concern for the long-term maintenance of
northern Mexican and narrow-headed gartersnake habitat. These areas are
already vulnerable to declines in surface and groundwater availability,
and surface water may not be sustainable to support the gartersnakes'
prey base. An overdraft of groundwater withdrawal creates what is
referred to as a cone of depression within the groundwater. Reduced or
eliminated surface flow can result in areas where these cones of
depression intersect with stream alluvium (deposits in a valley a
stream flows through).
The presence of surface water is a primary habitat component for
northern Mexican and narrow-headed gartersnakes. Existing water laws in
Arizona and New Mexico may not be fully adequate to protect gartersnake
habitat from the dewatering effects of groundwater withdrawals. New
Mexico water law now includes provisions for instream water rights to
protect fish and wildlife and their habitats. Arizona water law also
recognizes such provisions; however, because this change is relatively
recent, instream water rights have low priority, and are often never
fulfilled because more senior diversion rights have priority. Existing
water laws are considered outdated and reflect a legislative
interpretation of water resources that is not consistent with current
scientific understanding of the hydrologic connection between
groundwater and surface water (Gelt 2008, pp. 1-12).
Water for development and urbanization is often supplied by
groundwater pumping and surface water diversions from sources that
include reservoirs and Central Arizona Project's allocations from the
Colorado River. As stated previously, groundwater pumping creates a
cone of depression within the affected aquifer that slowly radiates
outward from the well site. When the cone of depression intersects the
hyporheic zone of a stream (the active transition zone between two
adjacent ecological communities under or beside a stream channel or
floodplain between the surface water and groundwater that contributes
water to the stream itself), the surface water flow may decrease, and
the subsequent drying of riparian and wetland vegetative communities
can follow. Continued groundwater pumping at such levels draws down the
aquifer sufficiently to create a water-level gradient away from the
stream and floodplain (Webb and Leake 2005, p. 309). Complete
disconnection of the aquifer and the stream results in strong negative
effects to riparian vegetation (Webb and Leake 2005, p. 309) that
result in a reduction or loss in surface water and riparian vegetation
that can reduce or eliminate the local prey base that gartersnakes
depend on for survival.
The arid southwestern United States is characterized by limited
annual precipitation, which means limited annual recharge of
groundwater aquifers; even modest changes in groundwater levels from
groundwater pumping can affect above-ground stream flow as evidenced by
depleted flows in the Santa Cruz, Verde, San Pedro, Blue, and lower
Gila rivers as a result of regional groundwater demands (Stromberg et
al. 1996, pp. 113, 124-128; Rinne et al. 1998, p. 9; Voeltz 2002, pp.
45-47, 69-71; Haney et al. 2009 p. 1). Groundwater demands are expected
to reduce surface water flow in Arivaca Creek, Babocomari River, lower
Cienega Creek, San Pedro River, upper Verde River, and Agua Fria River
over the next several decades (Haney et al. 2009 p. 3, Table 2), which
historically or currently support northern Mexican or narrow-headed
gartersnake populations. If
[[Page 38705]]
surface flow is lost entirely from additional stress caused by drought
induced by projected climate change in the Southwest, local or regional
extirpations of both gartersnake species are likely to occur.
Water depletion is a concern for the Verde River (Garner et al.
2013, entire). For example, the City of Prescott, Arizona, experienced
a 22 percent increase in population between 2000 and 2005 (U.S. Census
Bureau 2010, p. 1), averaging around 4 percent growth per year (City of
Prescott 2010, p. 1). In addition, the towns of Prescott Valley and
Chino Valley experienced growth rates of 66 and 67 percent,
respectively (Arizona Department of Commerce 2009a, p. 1; 2009b, p. 1).
This growth is facilitated by groundwater pumping in the Verde River
basin. In 2004, the cities of Prescott and Prescott Valley purchased a
ranch in the Big Chino basin in the headwaters of the Verde River, with
the intent of drilling new wells to supply up to approximately 5
million cubic meters (4,000 acre-feet (AF)) of groundwater per year.
Barnett and Hawkins (2002, Table 4) reported population census data
from 1970, as well as projections for 2030, for communities situated
along the middle Verde River or within the Verde River subbasin as a
whole, such as Clarkdale, Cottonwood, Jerome, and Sedona. From 1970-
2000, population growth was recorded as Clarkdale (384 percent),
Cottonwood (352 percent), Jerome (113 percent), and Sedona (504
percent) (Barnett and Hawkins 2002, Table 4). Projected growth in these
same communities from 1970-2030 was tabulated at Clarkdale (620
percent), Cottonwood (730 percent), Jerome (292 percent), and Sedona
(818 percent) (Barnett and Hawkins 2002, Table 4).
Garner et al. (2013, p. 5) found that the Verde Valley population
grew 13 percent in 10 years from 63,000 in 2000 to 71,000 in 2010.
These examples of documented and projected population growth within the
Verde River subbasin indicate ever-increasing water demands that have
impacted base flow in the Verde River and are expected to continue. The
middle and lower Verde River has limited or no flow during portions of
the year due to agricultural diversion and upstream impoundments, and
it has several impoundments in its middle reaches, which could expand
the area of impacted northern Mexican and narrow-headed gartersnake
habitat. Blasch et al. (2006, p. 2) suggests that groundwater storage
in the Verde River subbasin has already declined due to groundwater
pumping and reductions in natural channel recharge resulting from
stream flow diversions.
Scientific studies have shown a link between the Big Chino aquifer
and spring flows that form the headwaters of the Verde River. It is
estimated that 80 to 86 percent of baseflow in the upper Verde River
comes from the Big Chino aquifer (Wirt 2005, p. G8). An in-depth
discussion of the potential effects to the Verde River from pumping of
the Big Chino Aquifer is available in Marder (2009, pp. 183-189).
However, while these withdrawals could potentially dewater the upper 26
mi (42 km) of the Verde River (Wirt and Hjalmarson 2000, p. 4; Marder
2009, pp. 188-189), it is uncertain that this project will occur given
the cost and administrative challenges it faces. An agreement in
principle was signed among the Salt River Project, the City of
Prescott, and Town of Prescott Valley to work toward resolution of
water rights in the Verde watershed, and, in 2012, Comprehensive
Agreement No. 1, which established monitoring and modeling plans, was
entered into. Within the Verde River subbasin, and particularly within
the Verde Valley, where the northern Mexican and narrow-headed
gartersnakes could occur, several other activities continue to threaten
surface flows (Rinne et al. 1998, p. 9; Paradzick et al. 2006, pp. 104-
110).
Portions of the Verde River or its tributaries are permanently or
seasonally dewatered by water diversions for agriculture (Paradzick et
al. 2006, pp. 104-110). The demands for surface water allocations from
rapidly growing communities and agricultural and mining interests have
altered flows or dewatered significant reaches during the spring and
summer months in some of the Verde River's larger, formerly perennial
tributaries such as Wet Beaver Creek, West Clear Creek, and the East
Verde River (Girmendonk and Young 1993, pp. 45-47; Sullivan and
Richardson 1993, pp. 38-39; Paradzick et al. 2006, pp. 104-110), which
may have supported either the northern Mexican or narrow-headed
gartersnake, or both. Groundwater pumping in the Tonto Creek drainage
regularly eliminates surface flows during parts of the year (Abarca and
Weedman 1993, p. 2).
Further south in Arizona, portions of the once-perennial San Pedro
River are now ephemeral, and water withdrawals are a concern for the
San Pedro River (USGS 2013, p. 3). The Cananea Mine in Sonora, Mexico,
owns the land surrounding the headwaters of the San Pedro. There is
disagreement on the exact amount of water withdrawn by the mine,
Mexicana de Cananea, which is one of the largest open-pit copper mines
in the world. However, there is agreement that it is the largest water
user in the basin (Harris et al. 2001, p. 213; Varady et al. 2000, p.
232). Along the upper San Pedro River, Stromberg et al. (1996, pp. 124-
127) found that wetland herbaceous species, important as cover for
northern Mexican gartersnakes, are the most sensitive to the effects of
a declining groundwater level. Webb and Leake (2005, pp. 302, 318-320)
described a correlative trend regarding vegetation along southwestern
streams from historically being dominated by marshy grasslands
preferable to northern Mexican gartersnakes, to currently being
dominated by woody species that are more tolerant of declining water
tables due to their deeper rooting depths. The cone of depression
associated with regional groundwater pumping is expected to continue
expanding its influence on surface flow in the San Pedro River over the
next several decades, which is expected to further reduce surface flow
in the river and negatively affect riparian vegetation (Stromberg et
al. 1996, pp. 124-128).
Another primary groundwater user in the San Pedro subbasin is Fort
Huachuca. Fort Huachuca is a U.S. Army installation located near Sierra
Vista, Arizona. Initially established in 1877 as a camp for the
military, the Fort has some of the earliest priority dates for water
rights in the state (Varady et al. 2000, p. 230). Fort Huachuca has
pursued a rigorous water use reduction plan, working over the past
decade to reduce groundwater consumption in the Sierra Vista subbasin.
Their efforts have focused primarily on reductions in groundwater
demand both on-post and off-post and increased artificial and enhanced
recharge of the groundwater system. Annual pumping from Fort Huachuca
production wells has decreased from a high of approximately 3,200 AF in
1989, to a low of approximately 1,400 AF in 2005. In addition, Fort
Huachuca and the City of Sierra Vista have increased the amount of
water recharged to the regional aquifer through construction of
effluent recharge facilities and detention basins that not only
increase stormwater recharge but mitigate the negative effects of
increased runoff from urbanization. The amount of effluent that was
recharged by Fort Huachuca and the City of Sierra Vista in 2005 was 426
AF and 1,868 AF, respectively. During this same year, enhanced
stormwater recharge at detention basins was estimated to be 129 AF. The
total net effect of all the combined efforts initiated by Fort Huachuca
has been to reduce the net groundwater
[[Page 38706]]
consumption by approximately 2,272 AF (71 percent) since 1989 (USFWS
2007b, pp. 41-42). Additional water conservation and recharge efforts
have since been implemented by Fort Huachuca and have reduced the
Fort's effect on baseflow in the upper San Pedro River to near zero, as
analyzed in a recent section 7 consultation (see https://www.fws.gov/southwest/es/arizona/Documents/Biol_Opin/120173_Fort%20HuachucaFINALBO_3.31.2014.pdf).
Groundwater withdrawal in Eagle Creek, primarily for water
supplying the large open-pit copper mine at Morenci, Arizona, dries
portions of the stream (Sublette et al. 1990, p. 19; USFWS 2005; Propst
et al. 1986, p. 7) that otherwise supports habitat for narrow-headed
gartersnakes. Mining is the largest industrial water user in
southeastern Arizona (ADWR Undated (accessed 2014), p. 62). The Morenci
mine on Chase Creek is North America's largest producer of copper,
covering approximately 24,281 hectares (ha) (60,000 acres (ac)). Water
for the Morenci mine is pumped from the Black River as an inter-basin
transfer via pipeline and open channel to Willow Creek, an east-flowing
tributary to Eagle Creek, then downstream more than 30 stream miles (50
km) to a facility where water is withdrawn and pumped uphill to the
mine in the adjacent Chase Creek drainage (Arizona Department of Water
Resources 2009, p. 1; Marsh 2013, pers. comm.). We are not aware of
plans for the closure of the Morenci Mine over the next several years,
and as the price for copper increases, the demand for copper mining
will increase into the future.
The Rosemont Copper Mine proposed to be constructed in the
northeastern area of the Santa Rita Mountains in Santa Cruz County,
Arizona, will include a mine pit that will be excavated to a depth
greater than that of the regional aquifer. Water will thus drain from
storage in the aquifer into the pit. The need to dewater the pit during
mining operations will thus result in ongoing removal of aquifer water
storage. Upon cessation of mining, a pit lake will form, and
evaporation from this water body will continue to remove water from
storage in the regional aquifer. This aquifer also supplies baseflow to
Cienega Creek, immediately east of the proposed project site. Several
groundwater models have been developed to analyze potential effects of
expected groundwater withdrawals. The latest independent models
indicate that a potentially significant reduction to baseflows in
Cienega Creek and Emprire Gulch are expected within 50 years post-
closure of the Rosemont Copper Mine, should it be permitted for
development (see https://www.rosemonteis.us/final-eis).
The best available scientific and commercial information indicates
that any reduction in the presence or availability of water is a
significant threat to northern Mexican and narrow-headed gartersnakes,
their prey base, and their habitat. This is because water is a
fundamental need that supports the necessary aquatic and riparian
habitats and prey species needed by both species of gartersnake.
Through GIS analyses, we found that approximately 32 percent of
formerly perennial streams have been dewatered within the historical
distribution of the northern Mexican gartersnake. Within the historical
distribution of the narrow-headed gartersnake, approximately 13 percent
of formerly perennial streams have been dewatered. With continued human
population growth and corresponding water use throughout the range of
both gartersnakes, we expect the loss of habitat due to reduction in
stream flows to increase in the foreseeable future and result in
additional declines and extirpations of gartersnake populations.
Climate Change and Drought (Northern Mexican and Narrow-headed
gartersnake)--Our analyses under the Act include consideration of
ongoing and projected changes in climate. The terms ``climate'' and
``climate change'' are defined by the Intergovernmental Panel on
Climate Change (IPCC). ``Climate'' refers to the mean and variability
of different types of weather conditions over time, with 30 years being
a typical period for such measurements, although shorter or longer
periods also may be used (IPCC 2007, p. 78). The term ``climate
change'' thus refers to a change in the mean or variability of one or
more measures of climate (e.g., temperature or precipitation) that
persists for an extended period, typically decades or longer, whether
the change is due to natural variability, human activity, or both (IPCC
2007, p. 78). Various types of changes in climate can have direct or
indirect effects on species. These effects may be positive, neutral, or
negative and they may change over time, depending on the species and
other relevant considerations, such as the effects of interactions of
climate with other variables (e.g., habitat fragmentation) (IPCC 2007,
pp. 8-14, 18-19). In our analyses, we use our expert judgment to weigh
relevant information, including uncertainty, in our consideration of
various aspects of climate change and their predicted effects on
northern Mexican and narrow-headed gartersnakes.
The ecology and natural histories of northern Mexican and narrow-
headed gartersnakes are strongly linked to water. As discussed above,
the northern Mexican gartersnake is a highly aquatic species and relies
largely upon other aquatic species, such as ranid frogs and native and
nonnative, soft-rayed fish as prey. The narrow-headed gartersnake is
the most aquatic of the southwestern gartersnakes and is a specialized
predator on native and nonnative, soft-rayed fish found primarily in
clear, rocky, higher elevation streams. Because of their aquatic
nature, they may be uniquely susceptible to environmental change,
especially factors associated with climate change (Wood et al. 2011, p.
3). Together, these factors are likely to make northern Mexican and
narrow-headed gartersnakes vulnerable to effects of climate change and
drought discussed below.
Several climate-related trends have been detected since the 1970s
in the southwestern United States, including increases in surface
temperatures, rainfall intensity, drought, heat waves, extreme high
temperatures, and average low temperatures (Overpeck 2008, entire).
Annual precipitation amounts in the southwestern United States may
decrease by 10 percent by the year 2100 (Overpeck 2008, entire). Seager
et al. (2007, pp. 1181-1184) analyzed 19 different computer models of
differing variables to estimate the future climatology of the
southwestern United States and northern Mexico in response to
predictions of changing climatic patterns. All but 1 of the 19 models
predicted a drying trend within the Southwest; one predicted a trend
toward a wetter climate (Seager et al. 2007, p. 1181). A total of 49
projections were created using the 19 models, and all but 3 predicted a
shift to increasing aridity (dryness) in the Southwest as early as
2021-2040 (Seager et al. 2007, p. 1181). Northern Mexican and
particularly narrow-headed gartersnakes, and their prey bases, depend
on permanent or nearly permanent water for survival. A large percentage
of habitats within the current distribution of northern Mexican and
narrow-headed gartersnakes are predicted to be at risk of becoming more
arid with reductions in snow pack levels by 2021-2040 (Seager et al.
2007, pp. 1183-1184). This has severe implications for the integrity of
aquatic and riparian ecosystems and the water that supports them.
In assessing potential effects of predicted climate change to river
systems in New Mexico, Molles (2007,
[[Page 38707]]
entire) found that: (1) Variation in stream flow will likely be higher
than variation in precipitation; (2) predicted effects such as warming
and drying are expected to result in higher variability in stream
flows; and (3) high-elevation fish and non-flying invertebrates (which
are prey for gartersnake prey species) are at greatest risk from
effects of predicted climate change. Enquist and Gori (2008, p. iii)
found that most of New Mexico's mid- to high-elevation forests and
woodlands have experienced either consistently warmer and drier
conditions or greater variability in temperature and precipitation from
1991 to 2005. However, Enquist et al. (2008, p. v) found the upper Gila
and San Francisco subbasins, which support narrow-headed gartersnake
populations, have experienced very little change in moisture stress
during the same period.
Cavazos and Arriaga (2010, entire) found that average temperatures
along the Mexican Plateau in Mexico could rise in the range of
1.8[emsp14][deg]F (1 [deg]C) to 9[emsp14][deg]F (5 [deg]C) in the next
20 years, according to their models. Cavazos and Arriaga (2010, entire)
also found that precipitation may decrease up to 12 percent over the
next 20 years in the same region, with pronounced decreases in winter
and spring precipitation.
Potential drought associated with changing climatic patterns may
adversely affect the amphibian prey base for the northern Mexican
gartersnake. Amphibians may be among the first vertebrates to exhibit
broad-scale changes in response to changes in global climatic patterns
due to their sensitivity to changes in moisture and temperature (Reaser
and Blaustein 2005, p. 61). Changes in temperature and moisture,
combined with the ongoing threat to amphibians from the persistence of
disease-causing bacteria such as Batrachochytrium dendrobatidis (Bd)
may cause prey species to experience increased physiological stress and
decreased immune system function, possibly leading to disease outbreaks
(Carey and Alexander 2003, pp. 111-121; Pounds et al. 2006, pp. 161-
167). Of the 30 different vertebrate species in the Sky Island region
of southeastern Arizona, the northern Mexican gartersnake was found to
be the fifth most vulnerable (total combined score) to predicted
climate change; one of its primary prey species, the Chiricahua leopard
frog, was determined to be the fourth most vulnerable (Coe et al. 2012,
p. 16). Both the northern Mexican gartersnake and the Chiricahua
leopard frog ranked the highest of all species assessed for
vulnerability of their habitat to predicted climate change, and the
Chiricahua leopard frog was also found to be the most vulnerable in
terms of its physiology (Coe et al. 2012, p. 18). Relative uncertainty
for the vulnerability assessment provided by Coe et al. (2012, Table
2.2) ranged from 0 to 8 (higher score means greater uncertainty), and
the northern Mexican gartersnake score was 3, meaning that the
vulnerability assessment was more certain than not. Coe et al. (2012,
entire) focused their assessment of species vulnerability to climate
change on those occurring on the Coronado National Forest in
southeastern Arizona. However, it is not unreasonable to hypothesize
that results might be applicable in a larger, regional context as
applied in most climate models.
The bullfrog, also assessed by Coe et al. (2012, pp. 16, 18, Table
2.2), was shown to be significantly less vulnerable to predicted
climate change than either northern Mexican gartersnakes or Chiricahua
leopard frogs with an uncertainty score of 1 (very certain). We suspect
bullfrogs were found to be less vulnerable by Coe et al. (2012) to
predicted climate change in southeastern Arizona due to their dispersal
and colonization capabilities, capacity for self-sustaining
cannibalistic populations, and ecological dominance where they occur.
Based upon climate change models, nonnative species biology, and
ecological observations, Rahel et al. (2008, p. 551) concluded that
climate change could foster the expansion of nonnative aquatic species
into new areas, magnify the effects of existing aquatic nonnative
species where they currently occur, increase nonnative predation rates,
and heighten the virulence of disease outbreaks in North America.
Rahel and Olden (2008, p. 526) expect that increases in water
temperatures in drier climates such as the southwestern United States
will result in periods of prolonged low flows and stream drying. These
effects from changing climatic conditions may have profound effects on
the amount, permanency, and quality of habitat for northern Mexican and
narrow-headed gartersnakes as well as their prey base. Changes in
amount or type of winter precipitation may affect snowpack levels as
well as the timing of their discharge into high-elevation streams. Low
or no snowpack levels would jeopardize the amount and reliability of
stream flow during the arid spring and early summer months, which would
increase water temperatures to unsuitable levels or eliminate flow
altogether. Harmful nonnative species such as largemouth bass are
expected to benefit from prolonged periods of low flow (Rahel and Olden
2008, p. 527). These nonnative predatory species evolved in river
systems with hydrographs that were largely stable, not punctuated by
flood pulses in which native species evolved and benefit from. Propst
et al. (2008, p. 1246) also suggested that nonnative fish species may
benefit from drought.
Changes to climatic patterns may warm water temperatures, alter
stream flow events, and increase demand for water storage and
conveyance systems (Rahel and Olden 2008, pp. 521-522). Warmer water
temperatures across temperate regions are predicted to expand the
distribution of existing harmful nonnative species, which evolved in
warmer water temperatures, by providing 31 percent more suitable
habitat. This conclusion is based upon studies that compared the
thermal tolerances of 57 fish species with predictions made from
climate change temperature models (Mohseni et al. 2003, p. 389). Eaton
and Scheller (1996, p. 1,111) reported that, while several cold-water
fish species (such as trout, a prey species for narrow-headed
gartersnakes) in North America are expected to have reductions in their
distribution from effects of climate change, several harmful nonnative
species are expected to increase their distribution. In the
southwestern United States, this situation may occur where the quantity
of water is sufficient to sustain effects of potential prolonged
drought conditions but where water temperature may warm to a level
found suitable to harmful nonnative species that were previously
physiologically precluded from occupation of these areas. Species that
are particularly harmful to northern Mexican and narrow-headed
gartersnake populations, such as the green sunfish, channel catfish,
largemouth bass, and bluegill, are expected to increase their
distribution by 7.4 percent, 25.2 percent, 30.4 percent, and 33.3
percent, respectively (Eaton and Scheller 1996, p. 1,111).
Vanishing Cienegas (Northern Mexican Gartersnake)--Cienegas are
particularly important habitat for the northern Mexican gartersnake
because these areas present ideal habitat characteristics for the
species and its prey base and have been shown to support robust
populations of both (Rosen and Schwalbe 1988, p. 14). Hendrickson and
Minckley (1984, p. 131) defined cienegas as ``mid-elevation (3,281-
6,562 ft (1,000-2000 m)) wetlands characterized by permanently
saturated, highly organic, reducing (lowering of oxygen level) soils.''
Many of these unique communities of the southwestern United States,
Arizona in
[[Page 38708]]
particular, and Mexico have been lost in the past century to streambed
modification, intensive livestock grazing, woodcutting, artificial
drainage structures, stream flow stabilization by upstream dams,
channelization, and stream flow reduction from groundwater pumping and
water diversions (Hendrickson and Minckley 1984, p. 161). Stromberg et
al. (1996, p. 114) state that cienegas were formerly extensive along
streams of the Southwest; however, most were destroyed during the late
1800s, when groundwater tables declined several meters and stream
channels became incised. Drying trends are expected to continue into
the next several decades and likely beyond.
Development and Recreation Within Riparian Corridors (Northern
Mexican and Narrow-headed Gartersnake)--Development within and adjacent
to riparian areas has proven to be a significant threat to riparian
biological communities and their suitability for native species (Medina
1990, p. 351; Nowak and Santana-Bendix 2002, p. 37). Riparian
communities are sensitive to even low levels (less than 10 percent) of
urban development within a subbasin (Wheeler et al. 2005, p. 142).
Development along or within proximity to riparian zones can alter the
nature of stream flow dramatically, changing once-perennial streams
into ephemeral streams, which has direct consequences on the riparian
community (Medina 1990, pp. 358-359). Medina (1990, pp. 358-359)
correlated tree density and age class representation to stream flow in
a high-elevation system with a narrow alluvium basin, finding that
decreased flow reduced tree densities and generally resulted in few to
no small-diameter trees. Small-diameter trees assist northern Mexican
and narrow-headed gartersnakes by providing additional habitat
complexity, thermoregulatory opportunities, and cover needed to reduce
predation risk and enhance the usefulness of areas for maintaining
optimal body temperature. Development along lower elevation streams
with broad alluvial basins may have different effects on stream flow
and riparian vegetation, as compared to high-elevation streams. The
presence of small shrubs and trees may be particularly important for
the narrow-headed gartersnake (Deganhardt et al. 1996, p. 327).
Development within occupied riparian habitat also likely increases the
number of human-gartersnake encounters and, therefore, the frequency of
adverse human interaction, described below.
Obvious examples of the influence of urbanization and development
can be observed within the areas of greater Tucson and Phoenix,
Arizona, where impacts have modified riparian vegetation, structurally
altered stream channels, facilitated nonnative species introductions,
and dewatered large reaches of formerly perennial rivers where the
northern Mexican gartersnake historically occurred (Santa Cruz, lower
Gila, and lower Salt Rivers, respectively). Urbanization and
development of these areas, along with the introduction of nonnative
species, are largely responsible for the likely extirpation of the
northern Mexican gartersnake from these regions.
Development near riparian areas usually leads to increased
recreation. Riparian areas located near urban areas are vulnerable to
the effects of increased recreation. An example of such an area within
the existing distribution of both the northern Mexican and narrow-
headed gartersnake is the Verde Valley. The reach of the Verde River
that winds through the Verde Valley receives a high amount of
recreational use from people living in central Arizona (Paradzick et
al. 2006, pp. 107-108). Increased human use results in the trampling of
near-shore vegetation, which reduces cover for gartersnakes, especially
newborns. Increased human visitation in occupied habitat also increases
the potential for adverse human interactions with gartersnakes, which
frequently leads to the capture, injury, or death of the snake (Rosen
and Schwalbe 1988, p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp.
285-286; Nowak and Santana-Bendix 2002, pp. 37-39).
Oak Creek Canyon, which represents an important source population
for narrow-headed gartersnakes, is also a well-known example of an area
with very high recreation levels (Nowak and Santana-Bendix 2002, p.
37). In 1995, 1.3 million people visited the Red Rock Ranger District,
which includes Oak Creek Canyon and the Sedona, Arizona area; that
figure climbed to six million visitors by 1999 (Nowak and Santana-
Bendix 2002, p. 37). Recreational activities in the Southwest are often
heavily tied to water bodies and riparian areas, due to the general
lack of surface water on the landscape. Increased recreational impacts
on the quantity and quality of water, as well as the adjacent
vegetation, negatively affect northern Mexican and narrow-headed
gartersnakes. The impacts to riparian habitat from recreation can
include movement of people or livestock, such as horses or mules, along
stream banks, trampling, loss of vegetation, and increased danger of
fire starts (Northern Arizona University 2005, p. 136; Monz et al.
2010, pp. 553-554).
High stream-side recreation levels can result in increased
siltation of streams, which can result in lower recruitment rates of
native fish and, therefore, negatively affect the prey base for narrow-
headed gartersnakes (Nowak and Santana-Bendix 2002, pp. 37-38). In the
arid Gila River Basin, recreational impacts are disproportionately
distributed along streams as a primary focus for recreation (Briggs
1996, p. 36). Within the range of the northern Mexican and narrow-
headed gartersnakes in the United States, the majority of the occupied
areas occur on Federal lands, which are managed for recreation and
other purposes. On the Gila National Forest, and associated private,
state, or non-Forest Service inholdings in the area, heavy recreation
use can affect gartersnakes within occupied narrow-headed gartersnake
habitat along the Middle Fork Gila River, the West Fork Gila River
between Cliff Dwellings and Little Creek, and Whitewater Creek from the
Catwalk to Glenwood (Hellekson 2012a, pers. comm.). Much of the
recreation use in these areas is related to hiking and backpacking,
which are not a threat to gartersnakes except when increased human
visitation leads to more gartersnake encounters and potentially more
killing of gartersnakes where the foot trail is near the canyon bottom
(see ``Adverse Human Interactions with Gartersnakes'' below).
Urbanization on smaller scales can also impact habitat suitability
and the prey base for the northern Mexican or narrow-headed
gartersnakes, such as along Tonto Creek, within the Verde Valley, and
the vicinity of Rock Springs along the Agua Fria River (Girmendonk and
Young 1997, pp. 45-52; Voeltz 2002, pp. 58-59, 69-71; Holycross et al.
2006, pp. 53, 56; Paradzick et al. 2006, pp. 89-90). One of the more
stable populations of the northern Mexican gartersnake in the United
States, at the Page Springs and Bubbling Ponds fish hatcheries along
Oak Creek, is likely to be affected by future small-scale development
over the next decade. As mitigation for effects to species covered
under their habitat conservation plan for the operation of Horseshoe
and Bartlett Reservoirs on the Verde River, the Salt River Project will
be funding development improvements and capacity expansion at these
State-owned and operated hatcheries for the purpose of creating a
native fish hatchery. Construction is likely to include the replacement
of earthen ponds currently used by the gartersnakes, with modernized
non-earthen units. However, the AGFD is committed to
[[Page 38709]]
maintaining the healthy population of northern Mexican gartersnakes at
these hatcheries, and is investigating land use options to improve
gartersnake habitat. A variety of activities associated with ongoing
and future operation of the hatchery is likely to contribute to some
level of fatality in resident gartersnakes, but that level might be
offset by a mitigation strategy when adopted.
Diminishing Water Quantity and Quality in Mexico (Northern Mexican
Gartersnake)--While effects to riparian and aquatic communities affect
both the northern Mexican gartersnake and the narrow-headed gartersnake
in the United States, Mexico provides habitat only for the northern
Mexican gartersnake. Threats to northern Mexican gartersnake habitat in
Mexico include intensive livestock grazing, urbanization and
development, water diversions and groundwater pumping, loss of
vegetation cover and deforestation, and erosion, as well as
impoundments and dams that have modified or destroyed riparian and
aquatic communities in areas of Mexico where the species occurred
historically. Rorabaugh (2008, pp. 25-26) noted threats to northern
Mexican gartersnakes and their native amphibian prey base in Sonora,
which included disease, pollution, intensive livestock grazing,
conversion of land for agriculture, nonnative plant invasions, and
logging.
Illegal or under-regulated logging in the Sierra Madre of Mexico,
and particularly within Chihuahua (Sierra Tarahumara), has been
identified as a significant environmental concern (Gingrich 1993,
entire). Gingrich (1993, p. 6) described the risk to streams from
excessive logging in the Sierra Madre as including increased flooding,
increased sedimentation, and lower baseflows. In an attempt to reverse
disturbing trends in logging practices, the World Wildlife Fund-Mexico
(2004, entire) has begun implementing a conservation plan for the
Sierra Tarahumara region. Ramirez Bautista and Arizmendi (2004, p. 3)
stated that the principal threats to northern Mexican gartersnake
habitat in Mexico include the drying of temporary ponds, livestock
grazing, deforestation, wildfires, and human settlements. In addition,
nonnative species, such as bullfrogs and nonnative, predatory fish,
have been introduced throughout Mexico and continue to disperse
naturally, broadening their distributions (Conant 1974, pp. 487-489;
Miller et al. 2005, pp. 60-61; Luja and Rodr[iacute]guez-Estrella 2008,
pp. 17-22).
Mexico's water needs for urban and agricultural development, as
well as impacts to aquatic habitat from these uses, are linked to
significant human population growth over the past century in Mexico.
Mexico's human population grew 700 percent from 1910 to 2000 (Miller et
al. 2005, p. 60). Mexico's population increased by 245 percent from
1950 to 2002 and is projected to grow by another 28 percent by 2025
(EarthTrends 2005, p. 1). Growth is concentrated in Mexico's northern
states (Stoleson et al. 2005, Table 3.1) and is now skewed towards
urban areas (Miller et al. 2005, p. 60). The human population of
Sonora, Mexico, doubled in size from 1970 (1.1 million) to 2000 (2.2
million) (Stoleson et al. 2005, p. 54). The population of Sonora is
expected to increase by 23 percent, to 2.7 million people, in 2020
(Stoleson et al. 2005, p. 54). Increasing trends in Mexico's human
population will continue to place additional stress on the country's
freshwater resources and continue to be the catalyst for the
elimination of northern Mexican gartersnake habitat and prey species.
Much knowledge of the status of aquatic ecosystems in Mexico has
come from fisheries research, which is particularly applicable to
assessing the status of northern Mexican gartersnakes because of the
gartersnakes' ecology and relationship to other aquatic and riparian
vertebrates. Fisheries research is particularly applicable because of
the role fishes serve as indicators of the status of the aquatic
community as a whole. Miller et al. (2005) reported information on
threats to freshwater fishes and riparian and aquatic communities in
specific water bodies from several regions throughout Mexico within the
range of the northern Mexican gartersnake: headwaters of the R[iacute]o
Lerma (extirpation of freshwater fish species, nonnative species,
pollution, dewatering, pp. 60, 105, 197); medium-sized streams
throughout the Sierra Madre Occidental (localized extirpations,
logging, dewatering, pp. 109, 177, 247); the R[iacute]o Conchos
(extirpations of freshwater fish species, p. 112); the r[iacute]os
Casas Grandes, Santa Mar[iacute]a, del Carmen, and Laguna Bustillos
(water diversions, groundwater pumping, channelization, flood control
practices, pollution, and introduction of nonnative species, pp. 124,
197); the R[iacute]o Santa Cruz (extirpations, p. 140); the R[iacute]o
Yaqui (dewatering, nonnative species, p. 148, Plate 61, p. 247); the
R[iacute]o Colorado (nonnative species, p. 153); the r[iacute]os Fuerte
and Culiac[aacute]n (logging, p. 177); canals, ponds, lakes in the
Valle de M[eacute]xico (nonnative species, extirpations, pollution, pp.
197, 281); the R[iacute]o Verde Basin (dewatering, nonnative species,
extirpations, Plate 88); the R[iacute]o Mayo (dewatering, nonnative
species, p. 247); the R[iacute]o Papaloapan (pollution, p. 252); and
the R[iacute]o P[aacute]nuco Basin (nonnative species, p. 295). These
examples should not be construed as to suggest that all native fishes
are threatened and all aquatic habitat or ecosystems are in peril.
Rather, these examples suggest that threats may be localized in some
examples and wider-ranging in others, but collectively several types of
threats are acting in various degrees across numerous drainages in
Mexico, throughout the range of the northern Mexican gartersnake. This
provides some level of insight into the status of native aquatic
ecosystems within its range.
Excessive sedimentation also appears to be a significant problem
for aquatic habitat in Mexico. Recent estimates indicate that 80
percent of Mexico is affected by soil erosion caused by vegetation
removal related to grazing, fires, agriculture, deforestation, etc. The
most serious erosion is occurring in the states of Guanajuato (43
percent of the state's land area), Jalisco (25 percent of the state's
land area), and M[eacute]xico (25 percent of the state's land area)
(Landa et al. 1997, p. 317), all of which occur within the distribution
of the northern Mexican gartersnake. Miller et al. (2005, p. 60) stated
that ``During the time we have collectively studied fishes in
M[eacute]xico and southwestern United States, the entire biotas of long
reaches of major streams such as the R[iacute]o Grande de Santiago
below Guadalajara (Jalisco) and R[iacute]o Colorado (lower Colorado
River in Mexico) downstream of Hoover (Boulder) Dam (in the United
States), have simply been destroyed by pollution and river
alteration.'' These streams are within the distribution of the northern
Mexican gartersnake. The geographic extent of threats reported by
Miller et al. (2005) across the distribution of the northern Mexican
gartersnake in Mexico is evidence that they are widespread through the
country, and encompass a large proportion of the distribution of the
northern Mexican gartersnake in Mexico.
In northern Mexico, effects of development, which is expected to
continue at similar rates, if not increase, over the next several
decades, such as agriculture and irrigation practices on streams and
rivers in Sonora have been documented at least as far back as the
1960s. Branson et al. (1960, p. 218) found that the perennial rivers
that drain the ``mountains'' (Sierra Madre) are ``silt-laden and
extremely turbid, mainly because of irrigation practices.'' Specific
rivers were not identified where Branson et al. (1960, p. 218)
[[Page 38710]]
describes the effects of irrigation practices, but the Sierra Madre in
Sonora is within the known distribution of the northern Mexican
gartersnake in Mexico and, therefore, suggests that at least some
portion of occupied habitat has been adversely impacted by these
practices. Smaller mountain streams, such as the Rio Nacozari in Sonora
were found to be ``biological deserts'' from the effects of numerous
local mining practices (Branson et al. 1960, p. 218). The perennial
rivers and their mountain tributaries that may have been historically
occupied by northern Mexican gartersnakes (as well as their prey
species) have since been adversely affected, which likely contributed
to declines in these areas.
Minckley et al. (2002, pp. 687-705) provided a summary of threats
(p. 696) to two newly described (at the time) species of pupfish and
their habitat in Chihuahua, Mexico, which occur with the northern
Mexican gartersnake and comprise part of its prey base. Initial
settlement and agricultural development of the area resulted in
significant channel cutting through soil layers protecting the alluvial
plain above them, which resulted in reductions in the base level of
each basin in succession (Minckley et al. 2002, p. 696). Related to
these activities, the building of dams and diversion structures dried
entire reaches of some regional streams and altered flow patterns of
others (Minckley et al. 2002, p. 696). This was followed by groundwater
pumping (enhanced by the invention of the electric pump), which lowered
groundwater levels and dried up springs and small channels and reduced
the reliability of baseflow in ``essentially all systems'' (Minckley et
al. 2002, p. 696). Subsequently, the introduction and expansion of
nonnative species in the area successfully displaced or extirpated many
native species (Minckley et al. 2002, p. 696). Conant (1974, pp. 486-
489) described significant threats to northern Mexican gartersnake
habitat within its distribution in western Chihuahua, Mexico, and
within the Rio Concho system where it occurs. These threats included
impoundments, water diversions, and purposeful introductions of
largemouth bass, common carp, and bullfrogs.
In the central portions of the northern Mexican gartersnakes' range
in Mexico, such as in Durango, Mexico, population growth since the
1960s has led to regional effects such as reduced stream flow,
increased water pollution, and largemouth bass introductions, which
``have seriously affected native biota'' (Miller et al. 1989, p. 26).
McCranie and Wilson (1987, p. 2) discuss threats to the pine-oak
communities of higher elevation habitats (within the distribution of
the northern Mexican gartersnake) in the Sierra Madre Occidental in
Mexico, specifically noting that ``. . . the relative pristine
character of the pine-oak woodlands is threatened . . . every time a
new road is bulldozed up the slopes in search of new madera or
pasturage. Once the road is built, further development follows; pueblos
begin to pop up along its length. . . .'' Several drainages that
possess suitable habitat for the northern Mexican gartersnake occur in
the area referenced above by McCranie and Wilson (1987, p. 2),
including the Rio de la Cuidad, Rio Quebrada El Salto, Rio Chico, Rio
Las Bayas, Rio El Cigarrero, Rio Galindo, Rio Santa Barbara, and the
Rio Chavaria.
In the southern portion of the northern Mexican gartersnake's range
in Mexico, growth and development around Mexico City resulted in
agricultural practices and groundwater demands that dewatered aquatic
habitat and led to declines, and in some cases, extinctions of local
native fish species (Miller et al. 1989, p. 25). Considerable research
has been focused in the central and west-central regions of Mexico,
within the southern portion of the northern Mexican gartersnake's
range, where native fish endemism (unique, narrowly distributed suite
of species) is high, as are threats to their populations and habitat.
Since the 1970s in central Mexico, significant human population growth
has resulted in the overexploitation of local fisheries and water
pollution; these factors have accelerated the degradation of stream and
riverine habitats and led to fish communities becoming reduced or
undergoing significant changes in structure and composition (Mercado-
Silva et al. 2002, p. 180).
These shifts in fish community composition, population density, and
shrinking distributions have adversely affected the northern Mexican
gartersnake prey base in the southern portion of its range in Mexico.
The Lerma River basin is the largest in west-central Mexico and is
within the distribution of the northern Mexican gartersnake in the
states of Jalisco, Guanajuato, and Quer[eacute]taro in the southern
portion of its range. Lyons et al. (1995, p. 572) reported that many
fish communities in large perennial rivers, isolated spring-fed
streams, or spring sources themselves of this region have been
``radically restructured'' and are now dominated by a few nonnative,
generalist species. Lowland streams and rivers in this region are used
heavily for irrigation and are polluted by industrial, municipal, and
agricultural discharges (Lyons and Navarro-Perez 1990, p. 37; Lyons et
al. 1995, p. 572).
Native fish communities of west-central Mexico have been found to
be in serious decline as a result of habitat degradation at an
``unprecedented'' rate due to water withdrawals (diversions for
irrigation), as well as untreated municipal, industrial, and
agricultural discharges (Lyons et al. 1998, pp. 10-11). Numerous dams
have been built along the Lerma River and along its major tributaries
to support one of Mexico's most densely populated regions during the
annual dry period; the water is used for irrigation, industry, and
human consumption (Lyons et al. 1998, p. 11). From 1985 to 1993, Lyons
et al. (1998, p. 12) found that 29 of 116 (25 percent) fish sampling
locations visited within the Lerma River watershed were completely dry
and another 30 were too polluted to support a fish community. These
figures indicate that over half of the localities visited by Lyons et
al. (1998, p. 12) that maintained fish populations prior to 1985 no
longer support fish, which has likely adversely affected local northern
Mexican gartersnake populations, and perhaps led to population declines
or extirpations.
Soto-Galera et al. (1999, p. 137) reported fish and water quality
sampling results from within the Rio Grande de Morelia-Lago de Cuitzeo
Basin of Michoac[aacute]n and Guanajuato, Mexico. The easternmost
portion of this basin occurs at the periphery of the known northern
Mexican gartersnake range in Mexico. Soto-Galera et al. (1999, p. 137)
found that over the past several decades, diminishing water quantity
and worsening water quality have resulted in the elimination of 26
percent of native fish species from the basin, the extinction of two
species of native fish, and declining distributions of the remaining 14
species. These figures suggest significant concern for aquatic
ecosystems of this region. Some conservation value, however, is
realized when headwaters, springs, and small streams are protected as
parks or municipal water supplies (Lyons et al. 1998, p. 15), but these
efforts do little to protect larger perennial rivers that represent
valuable habitat for northern Mexican gartersnakes.
Mercado-Silva et al. (2002, Appendix 2) reported results from fish
community sampling and habitat assessments along 63 sites across
central Mexico; the easternmost of these sites include most of the
northern Mexican gartersnake's southern range. Specifically, sampling
locations in the Balsas, Lerma, Morelia, P[aacute]nuco Moctezuma, and
P[aacute]nuco
[[Page 38711]]
Tampa[oacute]n basins each occurred within the range of the northern
Mexican gartersnake in the states of Guanajuato, Queretaro, Mexico, and
Puebla; approximately 30 locations in total. The purpose of this
sampling effort was to score each site in terms of its index of biotic
integrity (IBI) and environmental quality (EQ), with a score of 100
representing the optimum score for each category. The IBI scoring
method has been verified as a valid means to quantitatively assess
ecosystem integrity at each site (Lyons et al. 1995, pp. 576-581;
Mercado-Silva et al. 2002, p. 184). The range in IBI scores in these
sampling locations was 85 to 35, and the range in EQ scores was 90 to
50 (Mercado-Silva et al. 2002, Appendix 2). The average IBI score was
57, and the average EQ score was 74, across all 30 sites and all 4
basins (Mercado-Silva et al. 2002, Appendix 2). According to the
qualitative equivalencies assigned to scores (Mercado-Silva et al.
2002, p. 184), these values indicate that the environmental quality
score averaged across all 30 sites was ``good'' and the biotic
integrity scores were ``fair.'' It should be noted that 14 of the 30
sites sampled had IBI scores equal to or less than 50, and 5 of those
ranked as ``poor.'' Of all the basins throughout central Mexico that
were scored in this exercise, the two P[aacute]nuco basins represented
20 of the 30 sites sampled and scored the worst of all basins (Mercado-
Silva et al. 2002, p. 186). This indicates that threats to the northern
Mexican gartersnake, its prey base, and its habitat pose the greatest
risk in this portion of its range in Mexico.
Near Torre[oacute]n, Coahuila, where the northern Mexican
gartersnake occurs, groundwater pumping has resulted in flow reversal,
which has dried up many local springs, drawn arsenic-laden water to the
surface, and resulted in adverse human health effects in that area
(Miller et al. 2005, p. 61). Severe water pollution from untreated
domestic waste is evident downstream of large Mexican cities, such as
Mexico City, and inorganic pollution from nearby industrialized areas
and agricultural irrigation return flow has dramatically affected
aquatic communities through contamination (Miller et al. 2005, p. 60).
Miller et al. (2005, p. 61) provide an excerpt from Soto Galera et al.
(1999) addressing the threats to the R[iacute]o Lerma, Mexico's longest
river, which is occupied by the northern Mexican gartersnake: ``The
basin has experienced a staggering amount of degradation during the
20th Century. By 1985-1993, over half of our study sites had
disappeared or become so polluted that they could no longer support
fishes. Only 15 percent of the sites were still capable of supporting
sensitive species. Forty percent (17 different species) of the native
fishes of the basin had suffered major declines in distribution, and
three species may be extinct. The extent and magnitude of degradation
in the R[iacute]o Lerma basin matches or exceeds the worst cases
reported for comparably sized basins elsewhere in the world.''
In the Transvolcanic Belt Region of the states of Jalisco, Mexico,
and Veracruz in southern Mexico, Conant (2003, p. 4) noted that water
diversions, pollution (e.g., discharge of raw sewage), sedimentation of
aquatic habitats, and increased dissolved nutrients were resulting in
decreased dissolved oxygen in suitable northern Mexican gartersnake
habitat. Conant (2003, p. 4) stated that many of these threats were
evident during his field work in the 1960s, and that they are
``continuing with increased velocity.''
High-Intensity Wildfires and Sedimentation of Aquatic Habitat (Narrow-
Headed Gartersnake)
High-intensity wildfires lead to excessive sedimentation and ash
flows in streams, which can, in turn, result in sharp declines, and
even complete elimination, in fish communities downstream. According to
the Apache-Sitgreaves National Forest forested vegetation types,
historic fire-return intervals varied from frequent, low-intensity
surface fires in ponderosa pine types (every 2-17 years), to mixed-
severity fires in wet mixed-conifer forests (every 35-50 years), to
high-severity, stand-replacement fires of the spruce-fir ecosystems
(every 150-400 years) (U.S. Forest Service (USFS) 2013). Low-intensity
fire has been a common, natural disturbance factor in forested
landscapes for centuries prior to European settlement (Rinne and Neary
1996, pp. 135-136). Rinne and Neary (1996, p. 143) concluded that
existing wildfire suppression policies intended to protect the
expanding number of human structures on forested public lands have
altered the fuel loads in these ecosystems and increased the
probability of high-intensity wildfires.
Climate change-driven drought cycles are also likely contributing
to a changing fire regime in the west (Westerling et al. (2006, pp.
941-943). Westerling et al. (2006, p. 940) showed that ``large wildfire
activity (in the western United States) increased suddenly and markedly
in the mid-1980s, with higher large-wildfire frequency, longer wildfire
durations, and longer wildfire seasons.'' The effects of these high-
intensity wildfires include the removal of vegetation, the degradation
of subbasin condition, altered stream behavior, and increased
sedimentation of streams. These effects can harm fish communities, as
observed in the 1990 Dude Fire, when corresponding ash flows resulted
in fish kills in Dude Creek and the East Verde River (Voeltz 2002, p.
77). Fish kills, also discussed below, can drastically affect the
suitability of habitat for northern Mexican and narrow-headed
gartersnakes due to the removal of a portion or the entire prey base.
The Chiricahua leopard frog recovery plan cites altered fire regimes as
a serious threat to Chiricahua leopard frogs, a prey species for
northern Mexican gartersnakes (USFWS 2007a, pp. 38-39).
The nature and occurrence of wildfires in the Southwest is expected
to also be affected by climate change and ongoing and predicted future
drought. Current predictions of drought and/or higher winter low
temperatures may stress ponderosa pine forests in which the narrow-
headed gartersnake principally occurs, and may increase the frequency
and magnitude of wildfire. Ganey and Vojta (2010, entire) studied tree
mortality in mixed-conifer and ponderosa pine forests in Arizona from
1997-2007, a period of extreme drought. They found the mortality of
trees to be severe; the number of trees dying over a 5[hyphen]year
period increased by more than 200 percent in mixed[hyphen]conifer
forest and by 74 percent in ponderosa pine forest during this
timeframe. Ganey and Vojta (2010) attributed drought and subsequent
insect (bark beetle) infestation to the die-offs in trees. Drought
stress and a subsequent high degree of tree mortality from bark beetles
make high-elevation forests more susceptible to high-intensity
wildfires.
Climate is a top-down factor that synchronizes with fuel loads, a
bottom-up factor. Combined with a predicted reduction in snowpack and
an earlier snowmelt, these factors suggest wildfires will be larger,
more frequent, and more severe in the southwestern United States
(Ful[eacute] 2010, entire). Wildfires are expected to reduce vegetative
cover and result in greater soil erosion, subsequently resulting in
increased sediment flows in streams (Ful[eacute] 2010, entire).
Increased sedimentation in streams reduces the visibility of
gartersnakes in the water column, hampering their hunting ability as
well as resulting in fish kills (which is also caused by the disruption
in the nitrogen cycle post-wildfire), which reduce the amount of prey
available to gartersnake populations. Additionally, unnaturally high
amounts of sediment fill in pools in intermittent streams,
[[Page 38712]]
which reduces the amount and availability of habitat for fish and
amphibian prey.
In 2011 and 2012, both Arizona (2011 Wallow Fire) and New Mexico
(2012 Whitewater-Baldy Complex Fire) experienced the largest wildfires
in their respective State histories; indicative of the last decade that
has been punctuated by wildfires of massive proportion. The 2011 Wallow
Fire affected (to various degrees) approximately 540,000 acres (218,530
ha) of Apache-Sitgreaves National Forest, White Mountain Apache Indian
Tribe, and San Carlos Apache Indian Reservation lands in Apache,
Navajo, Graham, and Greenlee counties in Arizona as well as Catron
County, New Mexico (InciWeb 2011). The 2011 Wallow Fire impacted 97
percent of perennial streams in the Black River subbasin, 70 percent of
perennial streams in the Gila River subbasin, and 78 percent of the San
Francisco River subbasin and resulted in confirmed fish kills in each
subbasin (Meyer 2011, p. 3, Table 1); each of these streams is known to
support populations of either northern Mexican or narrow-headed
gartersnakes.
Although the Black River drainage received no moderate or high-
severity burns as a result of the 2011 Wallow Fire, the Fish and Snake
Creek subbasins (tributaries to the Black River) were severely burned
(Coleman 2011, p. 2). Post-fire fisheries surveys above Wildcat Point
in the Black River found no fish in a reach extending up to the
confluence with the West Fork of the Black River. This was likely due
to subsequent ash and sediment flows that had occurred there (Coleman
2011, p. 2). Fisheries surveys of the Black River in 2012 also
reflected a largely absent prey base for narrow-headed gartersnakes
(narrow-headed gartersnakes observed appeared to be in starving
condition), but young-of-the-year native fish were detected, which may
signal the beginning of fish recruitment (Lopez et al. 2012, entire).
Post-fire fisheries surveys at ``the Box,'' in the Blue River, detected
only a single native fish. This was also likely due to ash and sediment
flows and the associated subsequent fish kills that had occurred there,
extending down to the Gila River Box in Safford, Arizona (Coleman 2011,
pp. 2-3). The East Fork Black River subbasin experienced moderate to
high-severity burns in 23 percent of its total acreage that resulted in
declines in Apache trout and native sucker populations, but speckled
dace and brown trout remained prevalent as of 2011 (Coleman 2011, p.
3). These fire data suggest that the persistence of the prey base for
northern Mexican and narrow-headed gartersnakes in the Black River, and
narrow-headed gartersnakes in the lower Blue River, will be precarious
into the near- to mid-term future, as will likely be the stability of
gartersnake populations there. Immediate post-fire fish sampling in
Eagle Creek confirmed that fish populations had been severely depleted,
but that some level of population rebound had occurred by 2 years post-
fire (Marsh 2013, pers. comm.).
Several large wildfires have occurred historically on the Gila
National Forest. These fires have resulted in excessive sedimentation
of streams and affected resident fish populations that serve as prey
for narrow-headed gartersnakes. From 1989-2004, numerous wildfires
cumulatively burned much of the uplands within the Gila National
Forest, which resulted in most perennial streams in the area
experiencing ash flows and elevated sedimentation (Paroz et al. 2006,
p. 55). More recently, the 2012 Whitewater-Baldy Complex Fire in the
Gila National Forest in New Mexico is the largest wildfire in that
State's history. This wildfire was active for more than 5 weeks and
consumed approximately 300,000 acres (121,406 ha) of ponderosa, mixed-
conifer, pinyon-juniper, and grassland habitat (InciWeb 2012). Over 25
percent of the burn area experienced high-moderate burn severity
(InciWeb 2012) and included several subbasins occupied by narrow-headed
gartersnakes such as the Middle Fork Gila River, West Fork Gila River,
Iron Creek, the San Francisco River, Whitewater Creek, Turkey Creek,
and Mineral Creek (Brooks 2012, Table 1; Hellekson 2013, pers. comm.).
Other extant populations of the narrow-headed gartersnake in Gilita and
South Fork Negrito Creeks are also expected to be impacted from the
2012 Whitewater-Baldy Complex Fire. Narrow-headed gartersnake
populations in the Middle Fork Gila River and Whitewater Creek formerly
represented two of the four most robust populations known from New
Mexico, and two of the five known rangewide, and are expected to have
been severely jeopardized by post-fire effects to their prey base.
Thus, we now consider them currently as likely not viable, at least
until the watershed stabilizes and again supports a fish community, or
perhaps the next 5-10 years. In reference to Gila trout populations,
Brooks (2012, p. 3) stated that fish populations are expected to be
severely impacted in the West Fork Gila River and Whitewater Creek. The
loss of fish communities in affected streams is likely to lead to
associated declines, or potential extirpations, in affected narrow-
headed gartersnake populations as a result of the collapse in their
prey base.
Since 2000, several wildfires have affected occupied narrow-headed
gartersnake habitat on the Gila National Forest. The West Fork Gila
subbasin was affected by the 2002 Cub Fire, the 2003 Dry Lakes Fire,
and the 2011 Miller Fire; each resulted in post-fire ash and sediment
flows, which adversely affected fish populations used by narrow-headed
gartersnakes (Hellekson 2012a, pers. comm.). In 2011, the Miller Fire
significantly affected the Little Creek subbasin and has resulted in
substantive declines in abundance of the fish community (Hellekson
2012a, pers. comm.). Dry Blue and Campbell Blue creeks were affected by
the 2011 Wallow Fire (Hellekson 2012a, pers. comm.). Saliz Creek was
highly affected by the 2006 Martinez Fire (Hellekson 2012a, pers.
comm.). Turkey Creek was heavily impacted by the Dry Lakes Fire in
2003, which resulted in an extensive fish kill, but the fish community
has since rebounded (Hellekson 2012a, pers. comm.). It is not certain
how long the fish community was depleted or absent from Turkey Creek,
but it is suspected that the narrow-headed gartersnake population there
may have suffered declines from the loss of their prey base, as
evidenced by the current low population numbers. Black Canyon was
affected by large ash and debris flows from the 2013 Silver Fire (USFS
2013, entire). Prior to the 2002 Dry Lakes Fire, Turkey Creek was
largely populated by nonnative, predatory fish species, in its lower
reaches. Upper reaches were largely dominated by native fish species,
which have since rebounded in numbers (Hellekson 2012a, pers. comm.),
and may provide high-quality habitat for narrow-headed gartersnakes,
once the subbasin has adequately stabilized.
Effects to northern Mexican and narrow-headed gartersnake habitat
from wildfire should be considered in light of effects to the
structural habitat and effects to the prey base. Post-fire effects vary
with burn severity, percent of area burned within each severity
category, and the intensity and duration of precipitation events that
follow (Coleman 2011, p. 4). Low-severity burns within riparian habitat
can actually have a rejuvenating effect by removing decadent ground
cover and providing nutrients to remaining vegetation. As a result,
riparian vegetative communities may be more resilient to wildfire,
given that water is present (Coleman 2011, p. 4). Willows, an important
component to narrow-headed gartersnake habitat, can be
[[Page 38713]]
positively affected by low-severity burns, as long as the root crowns
are not damaged (Coleman 2011, p. 4). High-severity burns that occur
within the floodplain of occupied habitat are expected to have some
level of shorter term effect on resident gartersnake populations
through effects to the vegetative structure and abundance, which may
include a reduction of basking sites and a loss of cover, which could
increase the risk of predation. These potential effects need further
study. Post-fire ash flows, flooding, and impacts to native prey
populations are longer term effects and can occur for many years after
a large wildfire (Coleman 2011, p. 2).
Post-fire flooding with significant ash and sediment loads can
result in significant declines, or even the collapse, of resident fish
communities, which poses significant concern for the persistence of
resident gartersnake populations in affected areas. Sedimentation can
adversely affect fish populations used as prey by northern Mexican or
narrow-headed gartersnakes by: (1) Interfering with respiration; (2)
reducing the effectiveness of fish's visually based hunting behaviors;
and (3) filling in interstitial spaces (spaces between cobbles, etc.,
on the stream floor) of the substrate, which reduces reproduction and
foraging success of fish (Wheeler et al. 2005, p. 145). Excessive
sediment also fills in intermittent pools required for amphibian prey
reproduction and foraging. Siltation of the rocky interstitial spaces
along stream bottoms decreases the dissolved oxygen content where fish
lay their eggs, resulting in depressed recruitment of fish and a
subsequent reduction in prey abundance for northern Mexican and narrow-
headed gartersnakes through the loss of prey microhabitat (Nowak and
Santana-Bendix 2002, pp. 37-38). As stated above, sediment can lead to
several effects in resident fish species used by northern Mexican or
narrow-headed gartersnakes as prey, which can ultimately cause
increased direct fatalities, reduced reproductive success, lower
overall abundance, and reductions in prey species composition as
documented by Wheeler et al. (2005, p. 145). The underwater foraging
ability of narrow-headed gartersnakes (de Queiroz 2003, p. 381) and
likely northern Mexican gartersnakes is largely based on vision and is
also directly compromised by excessive turbidity caused by
sedimentation of water bodies. Suspended sediment in the water column
may reduce the narrow-headed gartersnake's visual hunting efficiency
from effects to water clarity, based on research conducted by de
Queiroz (2003, p. 381) that concluded the species relied heavily on
visual cues during underwater striking behaviors.
The presence of adequate interstitial spaces along stream floors
may be particularly important for narrow-headed gartersnakes. Hibbitts
et al. (2009, p. 464) reported the precipitous decline of narrow-headed
gartersnakes in a formerly robust population in the San Francisco River
at San Francisco Hot Springs from 1996 to 2004. The exact cause for
this decline is uncertain, but the investigators suspected that a
reduction in interstitial spaces along the stream floor from an
apparent conglomerate, cementation process may have affected the
narrow-headed gartersnake's ability to successfully anchor themselves
to the stream bottom when seeking refuge or foraging for fish (Hibbitts
et al. 2009, p. 464). These circumstances would likely result in low
predation success and eventually starvation. Other areas where
sedimentation has affected either northern Mexican or narrow-headed
gartersnake habitat are Cibecue Creek in Arizona, and the San Francisco
River and South Fork Negrito Creek in New Mexico (Rosen and Schwalbe
1988, p. 46; Arizona Department of Water Resources 2011, p. 1;
Hellekson 2012a, pers. comm.). The San Francisco River in Arizona was
classified as impaired due to excessive sediment from its headwaters
downstream to the Arizona-New Mexico border (Arizona Department of
Water Resources 2011, p. 1). South Fork Negrito Creek is also listed as
impaired due to excessive turbidity (Hellekson 2012a, pers. comm.).
Potential mechanisms exist that can ameliorate the effects of
wildfires, such as prescribed fire, use of wildland fire, fuels
management, and timber harvest, and can sustain desired conditions for
fire-adapted ecosystems and provide habitat for threatened and
endangered species, but will only be effective at a landscape scale.
The Guidance for Implementation of Federal Wildland Fire Management
Policy is the Department of Agriculture's single cohesive Federal fire
policy, and it was updated in February 2009. The intent of this policy
is to solidify that the full range of strategic and tactical options
are available and considered in the response to every wildland fire
(USFS 2013, entire). Benefits are considered to include the movement of
vegetation toward desired conditions, a greater contribution to
landscape restoration, control of invasive species, a reduction in
uncharacteristic wildfire across the broader landscape, and the
resiliency of potential natural vegetation types to adapt to climate
change (USFS 2013, entire). We are uncertain whether such projects can
be completed with the scope and urgency required to reverse the current
trend of massive, high-intensity wildfires in the southwest but intend
to facilitate their implementation as project cooperators. We conclude
that effects of high-intensity wildfires are threatening narrow-headed
gartersnakes with increasing likelihood of future impacts as a result
of climate change.
Summary
The presence of water is critical to both northern Mexican and
narrow-headed gartersnakes and their primary prey species because their
ecology and natural histories are strongly linked to water. Several
factors, both natural and manmade, contribute to the continued
degradation and dewatering of aquatic habitat throughout the range of
northern Mexican and narrow-headed gartersnakes. Increasing human
population growth is driving higher and higher demands for water in
both the United States and Mexico. Water is subsequently secured
through dams, diversions, flood-control projects, and groundwater
pumping, which affects gartersnake habitat through reductions in flow
and complete dewatering of stream reaches. Entire reaches of the Gila,
Salt, Santa Cruz, and San Francisco Rivers, as well as numerous other
rivers throughout the Mexican Plateau in Mexico that were historically
occupied by either or both northern Mexican or narrow-headed
gartersnakes, are now completely dry due to diversions, dams, and
groundwater pumping. Several groundwater basins within the range of
northern Mexican and narrow-headed gartersnakes in the United States
are considered active management areas where pumping exceeds recharge,
which is a constant threat to surface flow in streams and rivers
connected to these aquifers. Reduced flows concentrate northern Mexican
and narrow-headed gartersnakes and their prey with harmful nonnative
species, which accelerate and amplify adverse effects of native-
nonnative community interactions. Where surface water persists,
increasing land development and recreation use adjacent to and within
riparian habitat has led to further reductions in stream flow, removal
or alteration of vegetation, and increased frequency of adverse human
interactions with gartersnakes.
Exacerbating the effects of increasing human populations and higher
water demands, climate change predictions
[[Page 38714]]
include increased aridity, lower annual precipitation totals, lower
snow pack levels, higher variability in flows (lower low-flows and
higher high-flows), and enhanced stress on ponderosa pine communities
in the southwestern United States and northern Mexico. Increased stress
to ponderosa pine forests places them at higher risk of high-intensity
wildfires, the effects of which are discussed below. Climate change has
also been predicted to enhance the abundance and distribution of
harmful nonnative species, which adversely affect northern Mexican and
narrow-headed gartersnakes.
Cienegas, a unique and important habitat for northern Mexican
gartersnakes, have been adversely affected or eliminated by a variety
of historical and current land uses in the United States and Mexico,
including streambed modification, intensive livestock grazing,
woodcutting, artificial drainage structures, stream flow stabilization
by upstream dams, channelization, and stream flow reduction from
groundwater pumping and water diversions. The historical loss of the
cienega habitat of the northern Mexican gartersnake has resulted in
local population declines or extirpations, negatively affecting its
status and contributing to its decline rangewide.
Wildfire has historically been a natural and important disturbance
factor within the range of northern Mexican and narrow-headed
gartersnakes. However, in recent decades, forest management policies in
the United States have favored fire suppression, the result of which
has led to wildfires of unusual proportions, particularly along the
Mogollon Rim of Arizona and New Mexico. These policies are generally
not in place in Mexico, and consequently, wildfire is not viewed as a
significant threat to the northern Mexican gartersnake in Mexico.
However, in the last 2 years, both Arizona (2011 Wallow Fire) and New
Mexico (2012 Whitewater-Baldy Complex Fire) have experienced the
largest wildfires in their respective State histories, which is
indicative of the last decade having been punctuated by wildfires of
significant magnitude. High-intensity wildfire has been shown to result
in significant ash and sediment flows into habitat occupied by northern
Mexican or narrow-headed gartersnakes, resulting in significant
reductions of their fish prey base and, in some instances, total fish
kills. The interstitial spaces between rocks located along the stream
floor are important habitat for the narrow-headed gartersnake because
of its specialized foraging strategy and specialized diet. These spaces
are also important spawning and egg deposition habitat for native fish
species used as prey by narrow-headed gartersnakes. When these spaces
fill in with sediment, the narrow-headed gartersnake may be unable to
forage successfully and may succumb to stress created by a depressed
prey base.
A significant reduction or absence of a prey base results in stress
of resident gartersnake populations and can result in local population
extirpations. Also, narrow-headed gartersnakes are believed to rely
heavily on visual cues while foraging underwater; increased turbidity
from suspended fine sediment in the water column is likely to impede
their ability to use visual cues at some level. Factors that result in
depressed foraging ability from excessive sedimentation are likely to
be enhanced when effects from harmful nonnative species are also acting
on resident northern Mexican and narrow-headed gartersnake populations.
We consider the narrow-headed gartersnake to be particularly threatened
by the effects of wildfires as described because they occur throughout
its range, the species is a fish-eating specialist that is unusually
vulnerable to localized fish kills, and wildfire has already
significantly affected two of the last remaining five populations that
were formerly considered viable, pre-fire. We have demonstrated that
high-intensity wildfires have the potential to eliminate gartersnake
populations through a reduction or loss of their prey base. Since 1970,
wildfires have adversely impacted the native fish prey base in 6
percent of the historical distribution of northern Mexican gartersnakes
in the United States and 21 percent of that for narrow-headed
gartersnakes rangewide, according to GIS analysis. These percentages
represent only stream miles within fire perimeters, not downstream
effects of ash flows within drainages, which would undoubtedly increase
the percentage of habitat impacted, at least for narrow-headed
gartersnakes, whose distribution overlaps more concisely with more and
larger wildfires over recent decades.
All of these conditions affect the primary drivers of gartersnake
habitat suitability (the presence of water and prey) and exist in
various degrees throughout the range of both gartersnake species.
Collectively, they reduce the amount and arrangement of physically
suitable habitat for northern Mexican and narrow-headed gartersnakes
over their regional landscapes. The genetic representation of each
species is threatened when populations become disconnected and isolated
from neighboring populations because the length or area of dewatered
zones is too great for dispersing individuals to overcome. Therefore,
normal colonizing mechanisms that would otherwise reestablish
populations where they have become extirpated are no longer viable.
This subsequently leads to a reduction in species redundancy when
isolated, small populations are at increased vulnerability to the
effects of stochastic events, without a means for natural
recolonization. Ultimately, the effects of scattered, small, and
disjunct populations, without the means to naturally recolonize, is
weakened species resiliency as a whole, which ultimately enhances the
risk of either or both species becoming endangered or going extinct.
Therefore, based on the best available scientific and commercial
information, we conclude that land uses or conditions described above
that alter or dewater northern Mexican and narrow-headed gartersnake
habitat are threats rangewide, now and in the foreseeable future.
Other Cumulative and Synergistic Effect of Threats on Low-Density
Populations (Northern Mexican and Narrow-Headed Gartersnakes)
In most locations where northern Mexican or narrow-headed
gartersnakes historically occurred or still occur currently, two or
more threats are likely acting in combination with regard to their
influence on the suitability of those habitats or on the species
themselves. Many threats could be considered minor in isolation, but
when they affect gartersnake populations in combination with other
threats, become more serious. We have concluded that in as many as 24
of 29 known localities in the United States (83 percent), the northern
Mexican gartersnake population is likely not viable and may exist at
low population densities that could be threatened with extirpation or
may already be extirpated. We also determined that in as many as 29 of
38 known localities (76 percent), the narrow-headed gartersnake
population is likely not viable and may exist at low population
densities that could be threatened with extirpation or may already be
extirpated, but survey data are lacking in areas where access is
restricted. We have also discussed how harmful nonnative species have
affected recruitment of gartersnakes across their range. In viable
populations, gartersnakes are resilient to the loss of individuals
through ongoing recruitment into the reproductive age class. However,
when northern Mexican or narrow-headed gartersnakes occur at low
population densities in the absence
[[Page 38715]]
of appropriate recruitment, the loss of even a few adults could
substantially increase the risk of extirpation of local populations.
Below, we discuss threats that, when considered in combination, can
appreciably threaten low-density populations of these species with
extirpation.
Historical and Unmanaged Livestock Grazing and Agricultural Land Uses
(Northern Mexican and Narrow-Headed Gartersnake) (Factor A)
Currently in the United States, livestock grazing is a largely
managed activity, but in Mexico, livestock grazing is much less managed
or unmanaged altogether. Several examples of extant gartersnake
populations (in some cases, apparently robust populations) in Mexico
were found in habitat that was heavily grazed with no riparian
vegetation development; these sites were coincidently free or largely
free of harmful nonnative species (Burger 2007, entire). Historical
livestock grazing has damaged approximately 80 percent of stream,
cienega, and riparian ecosystems in the western United States (Kauffman
and Krueger 1984, pp. 433-435; Weltz and Wood 1986, pp. 367-368; Cheney
et al. 1990, pp. 5, 10; Waters 1995, pp. 22-24; Pearce et al. 1998, p.
307; Belsky et al. 1999, p. 1). Fleischner (1994, p. 629) found that
``Because livestock congregate in riparian ecosystems, which are among
the most biologically rich habitats in arid and semiarid regions, the
ecological costs of grazing are magnified at these sites.'' Stromberg
and Chew (2002, p. 198) and Trimble and Mendel (1995, p. 243) also
discussed the propensity for cattle to remain within or adjacent to
riparian communities. Expectedly, this behavior is more pronounced in
more arid regions (Trimble and Mendel 1995, p. 243). Effects from
historical or unmanaged grazing include: (1) Declines in the structural
richness of the vegetative community; (2) losses or reductions of the
prey base; (3) increased aridity of habitat; (4) loss of thermal cover
and protection from predators; (5) a rise in water temperatures to
levels lethal to larval stages of amphibian and fish development; and
(6) desertification (Szaro et al. 1985, p. 362; Schulz and Leininger
1990, p. 295; Schlesinger et al. 1990, p. 1043; Belsky et al. 1999, pp.
8-11; Zwartjes et al. 2008, pp. 21-23). In one rangeland study, it was
concluded that 81 percent of the vegetation that was consumed,
trampled, or otherwise removed was from a riparian area, which amounted
to only 2 percent of the total grazing space, and that these actions
were 5 to 30 times higher in riparian areas than on the uplands
(Trimble and Mendel 1995, pp. 243-244). However, according to one study
along the Agua Fria River, herbaceous ground cover can recover quickly
from heavy grazing pressure (Szaro and Pase 1983, p. 384). Additional
information on the effects of historical livestock grazing can be found
in Sartz and Tolsted (1974, p. 354); Rosen and Schwalbe (1988, pp. 32-
33, 47); Clary and Webster (1989, p. 1); Clary and Medin (1990, p. 1);
Orodho et al. (1990, p. 9); and Krueper et al. (2003, pp. 607, 613-
614).
Szaro et al. (1985, p. 360) assessed the effects of historical
livestock management on a related taxon and found that western
(terrestrial) gartersnake (Thamnophis elegans vagrans) populations were
significantly higher (versus controls) in terms of abundance and
biomass in areas that were excluded from grazing, where the streamside
vegetation remained lush, than where uncontrolled access to grazing was
permitted. This effect was complemented by higher amounts of cover from
organic debris from ungrazed shrubs that accumulate as the debris moves
downstream during flood events. Specifically, results indicated that
snake abundance and biomass were significantly higher in ungrazed
habitat, with a five-fold difference in number of snakes captured,
despite the difficulty of making observations in areas of increased
habitat complexity (Szaro et al. 1985, p. 360). Szaro et al. (1985, p.
362) also noted the importance of riparian vegetation for the
maintenance of an adequate prey base and as cover in thermoregulation
and predation avoidance behaviors, as well as for foraging success.
Direct fatalities of amphibian species, in all life stages, from being
trampled by livestock has been documented (Bartelt 1998, p. 96; Ross et
al. 1999, p. 163). Gartersnakes may, on occasion, be trampled by
livestock. A black-necked gartersnake (Thamnophis cyrtopsis cyrtopsis)
had apparently been killed by livestock trampling along the shore of a
stock tank in the Apache-Sitgreaves National Forest, within an actively
grazed allotment (Chapman 2005).
Subbasins where historical grazing has been documented as a
suspected contributing factor for either northern Mexican or narrow-
headed gartersnake declines include the Verde, Salt, Agua Fria, San
Pedro, Gila, and Santa Cruz (Hendrickson and Minckley 1984, pp. 140,
152, 160-162; Rosen and Schwalbe 1988, pp. 32-33; Girmendonk and Young
1997, p. 47; Hale 2001, pp. 32-34, 50, 56; Voeltz 2002, pp. 45-81;
Krueper et al. 2003, pp. 607, 613-614; Forest Guardians 2004, pp. 8-10;
Holycross et al. 2006, pp. 52-61; Paradzick et al. 2006, pp. 90-92;
USFS 2008). Livestock grazing still occurs in these subbasins but is a
largely managed land use and is not likely to pose significant threats
to either northern Mexican or narrow-headed gartersnakes where closely
managed. In cases where poor livestock management results in fence
lines in persistent disrepair, providing unmanaged livestock access to
occupied habitat, adverse effects from loss of vegetative cover may
result, most likely in the presence of harmful nonnative species. As we
described above, however, we strongly suspect that northern Mexican and
narrow-headed gartersnakes are somewhat resilient to physical habitat
disturbance where harmful nonnative species are absent.
The creation and maintenance of stock tanks is an important
component to livestock grazing in the southwestern United States. Stock
tanks associated with livestock grazing may facilitate the spread of
harmful nonnative species when they are intentionally or
unintentionally stocked by anglers and private landowners (Rosen et al.
2001, p. 24). The management of stock tanks is an important
consideration for northern Mexican gartersnakes in particular. Stock
tanks associated with livestock grazing can be intermediary ``stepping
stones'' in the dispersal of nonnative species from larger source
populations to new areas (Rosen et al. 2001, p. 24). The effects of
livestock grazing at stock tanks on northern Mexican gartersnakes
depend on how they are managed. Dense bank and aquatic vegetation is an
important habitat characteristic for the northern Mexican gartersnake
in the presence of harmful nonnative species. This vegetation can be
affected if the impoundment is poorly managed. When harmful nonnative
species are absent, the presence of bank line vegetation is less
important. Well-managed stock tanks provide important habitat for
northern Mexican gartersnakes and their prey base, especially when the
tank: (1) Remains devoid of harmful nonnative species while supporting
native prey species; (2) provides adequate vegetation cover; and (3)
provides reliable water sources in periods of prolonged drought. Given
these benefits of well-managed stock tanks, we believe well-managed
stock tanks are an important, even vital at this time, component to
northern Mexican gartersnake conservation and recovery.
[[Page 38716]]
Road Construction, Use, and Maintenance (Northern Mexican and Narrow-
Headed Gartersnake) (Factor A)
Roads can pose unique threats to herpetofauna, and specifically to
species like the northern Mexican gartersnake, its prey base, and the
habitat where it occurs. The narrow-headed gartersnake, alternatively,
is probably less affected by roads due to its more aquatic nature.
Roads fragment occupied habitat and can result in diminished genetic
variability in populations from increased fatality from vehicle strikes
and adverse human encounters as supported by current research on
eastern indigo snakes (Breininger et al. 2012, pp. 364-366). Roads
often track along streams and present a fatality risk to gartersnakes
seeking more upland, terrestrial habitat for brumation and gestation.
Roads may cumulatively impact both species through the following
mechanisms: (1) Fragmentation, modification, and destruction of
habitat; (2) increase in genetic isolation; (3) alteration of movement
patterns and behaviors; (4) facilitation of the spread of nonnative
species via human vectors; (5) an increase in recreational access and
the likelihood of subsequent, decentralized urbanization; (6)
interference with or inhibition of reproduction; (7) contributions of
pollutants to riparian and aquatic communities; (8) reduction of prey
communities; and (9) acting as population sinks (when population death
rates from vehicle strikes exceed birth rates in a given area) (Rosen
and Lowe 1994, pp. 146-148; Waters 1995, p. 42; Foreman and Alexander
1998, p. 220; Trombulak and Frissell 2000, pp. 19-26; Carr and Fahrig
2001, pp. 1074-1076; Hels and Buchwald 2001, p. 331; Smith and Dodd
2003, pp. 134-138; Angermeier et al. 2004, pp. 19-24; Shine et al.
2004, pp. 9, 17-19; Andrews and Gibbons 2005, pp. 777-781; Wheeler et
al. 2005, pp. 145, 148-149; Roe et al. 2006, p. 161; Sacco 2007, pers.
comm.; Ouren et al. 2007, pp. 6-7, 11, 16, 20-21; Jones et al. 2011,
pp. 65-66; Hellekson 2012a, pers. comm.).
Perhaps the most common factor in road fatality of snakes is the
propensity for drivers to unintentionally and intentionally run them
over, both because people often dislike snakes (Rosen and Schwalbe
1988, p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp. 285-286; Nowak
and Santana-Bendix 2002, p. 39) and because they can be difficult to
avoid when crossing roads at perpendicular angles (Klauber 1956, p.
1026; Langley et al. 1989, p. 47; Shine et al. 2004, p. 11). Fatality
data for northern Mexican gartersnakes have been collected at the
Bubbling Ponds Hatchery since 2006. Of the 15 dead specimens, 8 were
struck by vehicles on roads within or adjacent to the hatchery ponds,
perhaps while crossing between ponds to forage (Boyarski 2011, pp. 1-
3). Van Devender and Lowe (1977, p. 47), however, observed several
northern Mexican gartersnakes crossing the road at night after the
commencement of the summer monsoon (rainy season), which highlights the
seasonal variability in surface activity of this snake. Wallace et al.
(2008, pp. 243-244) documented a vehicle-related fatality of a northern
Mexican gartersnake on Arizona State Route 188 near Tonto Creek that
occurred in 1995.
Adverse Human Interactions With Gartersnakes (Northern Mexican and
Narrow-Headed Gartersnake) (Factor E)
A fear of snakes is generally and universally embedded in modern
culture and is prevalent in the United States (Rosen and Schwalbe 1988,
p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp. 285-286; Nowak and
Santana-Bendix 2002, p. 39). We use the phrase ``adverse human
interaction'' to refer to the act of humans directly injuring or
killing snakes out of a sense of fear or anxiety (ophidiophobia), or
for no apparent purpose. One reason the narrow-headed gartersnake is
vulnerable to adverse human interactions is because of its appearance.
The narrow-headed gartersnake is often confused for a venomous water
moccasin (cottonmouth, Agkistrodon piscivorus), because of its
triangular-shaped head and propensity to be found in or near water
(Nowak and Santana-Bendix 2002, p. 38). Although the nearest water
moccasin populations are located over 700 miles (1,127 km) to the east
in central Texas, these misidentifications prove fatal for narrow-
headed gartersnakes (Nowak and Santana-Bendix 2002, p. 38).
Adverse human interaction may be largely responsible for highly
localized extirpations in narrow-headed gartersnakes based on the
collection history of the species at Slide Rock State Park along Oak
Creek, where high recreation use is strongly suspected to result in
direct fatality of snakes by humans (Nowak and Santana-Bendix 2002, pp.
21, 38). Declines in narrow-headed gartersnake populations in the North
and East Forks of the White River have also been attributed to humans
killing snakes (Rosen and Schwalbe 1988, pp. 43-44). Locations in New
Mexico where this unnatural form of fatality has been observed include
Wall Lake (Fleharty 1967, p. 219) and Whitewater Creek (Hellekson
2012a, pers. comm.). Areas with high visitation and recreation levels,
where this type of fatality is most likely to be more common, include
the Middle Fork and mainstem of the Gila River within 1 mile of Cliff
Dwellings to Little Creek, from the confluence with the East Fork to
Little Creek and the reach from Turkey Creek to the Gila Bird Area
south of Highway 180 (Hellekson 2013, pers. comm.), in Whitewater Creek
from the Catwalk to Glenwood (Hellekson 2012a, pers. comm.), near San
Francisco Hot Springs along the San Francisco River (Hibbitts and
Fitzgerald 2009, p. 466), the San Francisco River ``Box'', Black Canyon
near the FR150 crossing, and the south Fork Negrito Creek (Hellekson
2013, pers. comm.).
Environmental Contaminants (Northern Mexican and Narrow-Headed
Gartersnake) (Factor A)
Environmental contaminants, such as heavy metals, may be common at
low background levels in soils and, as a result, concentrations are
known to bioaccumulate in food chains. A bioaccumulative substance
increases in concentration in an organism or in the food chain over
time. A mid- to higher-order predator, such as a gartersnake, may,
therefore, accumulate these types of contaminants over time in their
fatty tissues, which may lead to adverse health effects (Wylie et al.
2009, p. 583, Table 5). Campbell et al. (2005, pp. 241-243) found that
metal concentrations accumulated in the northern watersnake (Nerodia
sipedon) at levels six times that of their primary prey item, the
central stoneroller (a fish, Campostoma anomalum). Metals, in trace
amounts, can be sequestered in the skin of snakes (Burger 1992, p.
212), interfere with metabolic rates of snakes (Hopkins et al. 1999, p.
1261), affect the structure and function of their liver and kidneys,
and may also act as neurotoxins, affecting nervous system function
(Rainwater et al. 2005, p. 670). Burger (1992, p. 209) found higher
concentrations of mercury, lead, and chromium in the skin of snakes, as
opposed to whole body tissue, ``suggesting that frequent shedding of
skin can act as a method of toxic excretion by snakes.'' Drewett et al.
(2013, entire) studied mercury accumulation in 4 species of snakes
(including the common gartersnake) ranging from mostly aquatic to
mostly terrestrial in an attempt to ascertain if a snake's ecology
affected the risk of exposure and tissue accumulation levels. They
found that the more aquatic the species' ecology and prey base, the
higher risk for exposure and accumulation of mercury (Drewett et al.
2013, pp. 7-8).
[[Page 38717]]
Based on data collected in 2002-2010, mercury appears to be
bioaccumulating in fish found in the lower reaches of Tonto Creek,
where northern Mexican gartersnakes also occur (Rector 2010, pers.
comm.; Arizona Department of Environmental Quality (ADEQ) 2011, Table
1). In fact, the State record for the highest mercury concentrations in
fish tissue was reported in Tonto Creek from this investigation by
Rector (2010, pers. comm.). Mean mercury levels in fish were found to
range from 0.2-1.5 mg/kg. The mean mercury concentration for all fish
was 1.1 mg/kg (ADEQ 2011, p. 3). Due to the risks of adverse human
health effects, ADEQ (2011, p. 8) recommends that smallmouth bass,
green sunfish, and black bullheads caught from Tonto Creek not be
consumed, and common carp be consumed sparingly. Because gartersnakes
eat fish, mercury may be bioaccumulating in resident populations,
although no testing of gartersnakes has occurred.
Specific land uses such as mining and smelting, as well as road
construction and use, can be significant sources of contaminants in
air, water, or soil through point-source and non-point source
mechanisms. Copper mining has occurred in Arizona and adjacent Mexico
for centuries, and many of these sites have smelters (now
decommissioned), which are former sources of airborne contaminants.
Industrial mine sites occur in several counties in Arizona (Greenlee,
Pima, Pinal, Yavapai, and Gila), as well as in Grant County, New
Mexico. The current price of copper is high and is expected to continue
to increase into the next several decades, fueled by international
development and economic growth. Overall, 18 mines are either in
production or in the pre-production phases of development in Arizona
and New Mexico. The mining industry in Mexico is largely concentrated
in the northern tier of that country, with the State of Sonora being
the leading producer of copper, gold, graphite, molybdenum, and
wollastonite, as well as the leader among Mexican States with regard to
the amount of surface area dedicated to mining (Stoleson et al. 2005,
p. 56). The three largest mines in Mexico (all copper) are found in
Sonora (Stoleson et al. 2005, p. 57). One of these, the Cananea Copper
Mine adjacent to the Upper San Pedro River in northern Sonora, was
responsible for a massive spill event. For two consecutive years (1977-
1978), two leaching ponds overflowed into the San Pedro River resulting
in very acidic water conditions and high levels of heavy metals such as
copper, zinc, and manganese (Eberhardt 1981, pp. 1, 16). These releases
caused the death of all aquatic organisms in the San Pedro River for a
60-mile (97-km) reach downstream of the mine (Eberhardt 1981, pp. 1,
16).
The sizes of mines in Sonora vary considerably, as do the known
environmental effects from mining-related activities (from exploration
to long after closure), which include contamination and drawdown of
groundwater aquifers, erosion, acid mine drainage, fugitive dust,
pollution from smelter emissions, and landscape clearing (Stoleson et
al. 2005, p. 57). We are aware of no specific research on potential
effects of mining or environmental contaminants acting on northern
Mexican gartersnakes, but conclude, based on the best available
scientific and commercial information, that where this land use is
prevalent, contaminants may be a concern for resident gartersnakes or
their prey.
Northern Mexican Gartersnake Competition With Marcy's Checkered
Gartersnake (Northern Mexican Gartersnake) (Factor E)
Preliminary research suggests that Marcy's checkered gartersnake
(Thamnophis marcianus marcianus) may impact the future conservation of
the northern Mexican gartersnake in southern Arizona. Rosen and
Schwalbe (1988, p. 31) hypothesized that bullfrogs are more likely to
eliminate northern Mexican gartersnakes when Marcy's checkered
gartersnakes are also present. Marcy's checkered gartersnake is a semi-
terrestrial species that is able to co-exist to some degree with
harmful nonnative predators. This might be due to its apparent ability
to forage in more terrestrial habitats, specifically during the
vulnerable juvenile size classes (Rosen and Schwalbe 1988, p. 31; Rosen
et al. 2001, pp. 9-10). In every age class, the northern Mexican
gartersnake forages in aquatic habitats where nonnative predatory fish,
bullfrogs, and crayfish are present, which increases not only the
encounter rate between predator and prey, but also the juvenile
fatality rate of the northern Mexican gartersnake, which negatively
affects recruitment. As northern Mexican gartersnake numbers decline
within a population, space becomes available for occupation by Marcy's
checkered gartersnakes. If competitive pressure between these two
species has existed over time, it is reasonable to conclude that
northern Mexican gartersnakes were successfully out-competing Marcy's
checkered gartersnake prior to the invasion of harmful nonnative
species. Therefore, Marcy's checkered gartersnake may simply be filling
the ecological void left by the decline of the northern Mexican
gartersnake. At a minimum, more research is needed to determine the
relationship between these two gartersnake species.
Fatality From Entanglement Hazards (Northern Mexican and Narrow-Headed
Gartersnake) (Factor E)
In addressing the effects of soil erosion associated with road
construction projects or post-fire remedial subbasin management,
erosion control materials placed on the ground surface are often used.
Examples of products used in erosion or sediment control include mulch
control netting, erosion control blankets, fiber rolls (wattles), and
reinforced silt fences (California Coastal Commission 2012, p. 1).
Erosion control is considered a best management practice for most soil-
disturbing activities, and is broadly required as mitigation across the
United States, in particular to avoid excess sedimentation of streams
and rivers. Rolled erosion control products, such as temporary erosion
control blankets and permanent turf reinforcement mats, are two methods
commonly used for these purposes (Barton and Kinkead 2005, p. 34).
These products use stitching or net-like mesh products to hold
absorbent media together. At a restoration site in South Carolina, 19
snakes (15 dead) representing 5 different species were found entangled
in the netting and had received severe lacerations in the process of
attempting to escape their entanglement (Barton and Kinkead 2005, p.
34). Stuart et al. (2001, pp. 162-164) also reported the threats of
net-like debris to snake species. Kapfer and Paloski (2011, p. 4)
reported at least 31 instances involving 6 different species of snake
(including the common gartersnake) in Wisconsin that had become
entangled in the netting used for either erosion control or as a
wildlife exclusion product. In their review, Kapfer and Paloski (2011,
p. 6) noted that 0.5-in.-by-0.5-in. mesh has the greatest likelihood of
entangling snakes.
Similar snake fatalities have not been documented in Arizona or New
Mexico, according to our files. However, given the broad usage of these
materials across the distribution of the northern Mexican and narrow-
headed gartersnakes, it is not unlikely that fatalities occur, but go
unreported. The likelihood of either gartersnake species becoming
entangled depends on the distance these erosion control materials are
used from water in occupied habitat and the density of potentially
affected populations. Because erosion control products are
[[Page 38718]]
usually used to prevent sedimentation of streams, there is a higher
likelihood for gartersnakes to become entangled. We encourage those who
use these materials in or near gartersnake habitat to take necessary
precautions and monitor their use as gartersnake fatalities could
occur.
Discarded fishing nets have also been documented as a source of
fatalities for northern Mexican gartersnakes in the area of Lake
Chapala, Jalisco, Mexico (Barrag[aacute]n-Ram[iacute]rez and Ascencio-
Arrayga 2013, p. 159). Netting or seining is not an authorized form of
recreational fishing for sport fish in Arizona or New Mexico, but the
practice is allowed in either state for the collection of live baitfish
(AGFD 2013a, p. 57; NMDGF 2013, p. 17). Arizona fishing regulations
authorize seining for baitfish only where the baitfish will be used and
specify that seining is not allowed in Coconino, Apache, Pima, and
Cochise Counties. In other areas, it is suspected that most seinng
activity occurs at sites dominated by warmwater sportfish, where these
gartersnakes are less likely to occur. We are not certain of the
frequency at which these techniques are used for such purposes in
either state, but we do not suspect that discarded nets or seines are
commonly left on-site where they could ensnarl resident gartersnakes.
However, this practice is used in Mexico as a primary means of
obtaining freshwater fish as a food source and may be more of a threat
to local northern Mexican gartersnake populations where this practice
occurs.
Disease and Parasites (Northern Mexican and Narrow-Headed Gartersnake)
(Factor C)
Our review of the scientific literature did not find evidence that
disease is a current factor contributing to the decline in northern
Mexican or narrow-headed gartersnakes. However, a recent wildlife
health bulletin announced the emergence of snake fungal disease (SFD)
within the eastern and midwestern portions of the United States
(Sleemen 2013, p. 1). SFD has now been diagnosed in several terrestrial
and aquatic snake genera including Nerodia, Coluber, Pantherophis,
Crotalus, Sistrurus, and Lampropeltis. Clinical signs of SFD include
scabs or crusty scales, subcutaneous nodules, abnormal molting, white
opaque cloudiness of the eyes, localized thickening or crusting of the
skin, skin ulcers, swelling of the face, or nodules in the deeper
tissues (Sleemen 2013, p. 1). While fatalities have been documented as
a result of SFD, population-level impacts have not, due to the cryptic
and solitary nature of snakes and the lack of long-term monitoring data
(Sleemen 2013, p. 1). So far, no evidence of SFD has been found in the
genus Thamnophis, but the documented occurrence of SFD in ecologically
similar, aquatic colubrids such as Nerodia is cause for concern.
Parasites, such as the common plerocercoid larvae of a
pseudophyllidean tapeworm (possibly Spirometra spp.), have been
observed in northern Mexican gartersnakes (Boyarski (2008b, pp. 5-6),
which may not be detrimental to the snake's health (Boyarski 2008b, p.
8). However, G[uacute]zman (2008, p. 102) first documented a Mexican
gartersnake fatality from a larval Eustrongylides sp. (endoparasitic
nematode), which ``raises the possibility that infection of Mexican
gartersnakes by Eustrongylides sp. larvae might cause fatality in some
wild populations,'' especially if those populations are under stress as
a result of the presence of other threats. Nowak et al. (2014, pp. 148-
149) reported the first observation of what appears as maternal
transmission of endoparasites, specifically of the genus (Macdonaldius
sp.). We found no substantive evidence that parasites represent a
significant threat to either gartersnake species.
Summary
We found numerous effects of livestock grazing that have resulted
in the historical degradation of riparian and aquatic communities that
have likely affected northern Mexican and narrow-headed gartersnakes.
Mismanaged or unmanaged grazing can have disproportionate effects to
riparian communities in arid ecosystems due to the attraction of
livestock to water, forage, and shade. We found current livestock
grazing activities to be more of a concern in Mexico, at least when it
occurs in areas that also support harmful nonnative species. The most
profound impacts from livestock grazing in the southwestern United
States occurred nearly 100 years ago, were significant, and may still
be affecting some areas that have yet to fully recover. Unmanaged or
poorly managed livestock operations likely have more pronounced effects
in areas impacted by harmful nonnative species through a reduction in
cover. However, land managers in Arizona and New Mexico currently
emphasize the protection of riparian and aquatic habitat in allotment
management planning, usually through fencing, rotation, monitoring, and
range improvements such as developing remote water sources.
Collectively, these measures have reduced the likelihood of significant
adverse impacts on northern Mexican or narrow-headed gartersnakes,
their habitat, and their prey base. We also recognize that, while the
presence of stock tanks on the landscape can benefit nonnative species,
well-managed stock tanks are currently an invaluable tool in the
conservation and recovery of northern Mexican gartersnakes and their
prey.
Other activities, factors, or conditions that act in combination,
such as road construction, use, and management, adverse human
interactions, environmental contaminants, entanglement hazards, and
competitive pressures from sympatric species, occur within the
distribution of these gartersnakes and have the propensity to
contribute to further population declines or extirpations where
gartersnakes occur at low population densities. An emerging skin
disease, SFD, has not yet been documented in gartersnakes but has
affected snakes of many genera within the United States, including
ecologically similar species, and may pose a future threat to northern
Mexican and narrow-headed gartersnakes. Where low-density populations
are affected by these types of threats described above, even the loss
of a few reproductive adults, especially females, from a population can
have significant population-level effects, most notably in the presence
of harmful nonnative species. Continued population declines and
extirpations threaten the genetic representation of each species
because many populations have become disconnected and isolated from
neighboring populations. This subsequently leads to a reduction in
species redundancy and resiliency when isolated, small populations are
at increased vulnerability to the effects of stochastic events, without
a means for natural recolonization. Based on the best available
scientific and commercial information, we conclude that these threats
have the tendency to act synergistically and disproportionately on low-
density gartersnake populations rangewide, now and in the foreseeable
future.
Adequacy and Effectiveness at Reducing Identified Threats of Existing
Regulatory Mechanisms (Northern Mexican and Narrow-Headed Gartersnake)
(Factors D and E)
Below, we examine whether existing regulatory mechanisms are
adequate to address the threats to the northern Mexican and narrow-
headed gartersnakes discussed under other factors and whether these
regulations are acting to alleviate the threats identified to the
species. Section 4(b)(1)(A) of the Endangered Species Act requires the
Service to take into account ``those efforts, if any, being
[[Page 38719]]
made by any State or foreign nation, or any political subdivision of a
State or foreign nation, to protect such species.'' We interpret this
language to require us to consider relevant Federal, State, and Tribal
laws, regulations, and other such mechanisms that may minimize any of
the threats we describe in the threats analysis under the other four
factors, or otherwise influence conservation of the species. We give
strongest weight to statutes and their implementing regulations, and
management direction that stems from those laws and regulations. They
are nondiscretionary and enforceable, and are considered a regulatory
mechanism under this analysis. Having evaluated the significance of the
threat as mitigated by any such conservation efforts, we analyze under
Factor D the extent to which existing regulatory mechanisms are
inadequate to address the specific threats to the species. Regulatory
mechanisms, if they exist, may reduce or eliminate the impacts from one
or more identified threats. In this section, we review existing State
and Federal regulatory mechanisms to determine whether they effectively
reduce or remove threats to the species.
A number of Federal statutes potentially afford protection to
northern Mexican and narrow-headed gartersnakes or their prey species.
These include section 404 of the Clean Water Act (33 U.S.C. 1251 et
seq.), Federal Land Policy and Management Act (43 U.S.C. 1701 et seq.),
National Forest Management Act (16 U.S.C. 1600 et seq.), National
Environmental Policy Act (NEPA; 42 U.S.C. 4321 et seq.), and the Act.
However, in practice, these statutes have not been able to provide
sufficient protection to prevent the currently observed downward trend
in northern Mexican and narrow-headed gartersnakes or their prey
species, and the concurrent upward trend in threats.
Section 404 of the Clean Water Act regulates placement of fill into
waters of the United States, including the majority of northern Mexican
and narrow-headed gartersnake habitat. However, many actions with the
potential to be highly detrimental to both species, their prey base,
and their habitat, such as gravel mining and irrigation diversion
structure construction and maintenance, may be exempted from the Clean
Water Act. Other detrimental actions, such as bank stabilization and
road crossings, are covered under nationwide permits that receive
limited environmental review. A lack of thorough, site-specific
analyses for projects can allow substantial adverse effects to northern
Mexican or narrow-headed gartersnakes, their prey base, or their
habitat.
The majority of the extant populations of northern Mexican and
narrow-headed gartersnakes in the United States occur on lands managed
by the U.S. Bureau of Land Management (BLM) and U.S. Forest Service.
Both agencies have riparian protection goals that may provide habitat
benefits to both species; however, neither agency has specific
management plans for northern Mexican or narrow-headed gartersnakes. As
a result, some of the significant threats to these gartersnakes, for
example, those related to nonnative species, are not necessarily
addressed on these lands. The BLM considers the northern Mexican
gartersnake as a ``Sensitive Species'' by default, due to its status
under the Act (U.S. Bureau of Land Management (USBLM) 2010), and agency
biologists actively attempt to identify gartersnakes for their records
for snakes observed incidentally during fieldwork (Young 2005). BLM
policy (BLM Manual Section 6840) requires consideration of sensitive
species during planning of activities and projects and mitigation of
specific threats. The BLM's Resource Management Plans include
objectives and management actions to benefit riparian habitat and
native fish; with some addressing ``invasive wildlife species'' (USBLM
2013, p. 2). When the Agua Fria National Monument was created in
January 2000, lowland leopard frogs, native fish, northern Mexican
gartersnakes, and riparian habitat were designated as ``monument
objects'' under protection by the National Monument (USBLM 2013, p. 3).
Similar conservation provisions are in place on the BLM's National
Conservation Areas (NCAs), such as the Las Cienegas NCA, San Pedro
River NCA, and the Gila Box Riparian NCA. While these measures likely
minimize the effect of otherwise adverse regional land use activities
on the aquatic community, gartersnake populations in these areas remain
in a precarious status.
The U.S. Forest Service does not include northern Mexican or
narrow-headed gartersnakes on their Management Indicator Species List,
but both species are included on the Regional Forester's Sensitive
Species List (USFS 2007, pp. 38-39). This means they are considered in
land management decisions, and protective measures can be implemented
to minimize adverse effects of otherwise lawful activities. However we
found no examples of specific protective measures that have been
implemented for these species. Individual U.S. Forest Service
biologists who work within the range of either northern Mexican or
narrow-headed gartersnakes may opportunistically gather data for their
records on gartersnakes observed incidentally in the field or
coordinate with other collaborators on surveys, although it is not
required. The Gila National Forest mentions the narrow-headed
gartersnake in their land and resource management plan, which includes
standards relating to forest management for the benefit of endangered
and threatened species as identified through approved management and
recovery plans (Center for Biological Diversity (CBD) et al. 2011, p.
18). Neither species is mentioned in any other land and resource
management plan for the remaining national forests where they occur
(CBD et al. 2011, p. 18).
The New Mexico Department of Game and Fish lists the northern
Mexican gartersnake as State-endangered and the narrow-headed
gartersnake as State-threatened (NMDGF 2006, Appendix H). A species is
State-endangered if it is in jeopardy of extinction or extirpation
within the State; a species is State-threatened if it is likely to
become endangered within the foreseeable future throughout all or a
significant portion of its range in New Mexico (NMDGF 2006, p. 52).
``Take,'' defined as ``to harass, hunt, capture or kill any wildlife or
attempt to do so'' by New Mexico Statutes Annotated (NMSA) 17-2-38.L.,
is prohibited without a scientific collecting permit issued by the New
Mexico Department of Game and Fish as per NMSA 17-2-41.C and New Mexico
Administrative Code (NMAC) 19.33.6. However, while the New Mexico
Department of Game and Fish can issue monetary penalties for illegal
take of either northern Mexican gartersnakes or narrow-headed
gartersnakes, the same provisions are not in place for actions that
result in loss or modification of their habitats (NMSA 17-2-41.C and
NMAC 19.33.6) (Painter 2005).
Prior to 2005, the AGFD allowed for take of up to four northern
Mexican or narrow-headed gartersnakes per person per year as specified
in Commission Order 43. The AGFD defines ``take'' as ``pursuing,
shooting, hunting, fishing, trapping, killing, capturing, snaring, or
netting wildlife or the placing or using any net or other device or
trap in a manner that may result in the capturing or killing of
wildlife.'' The AGFD subsequently amended Commission Order 43,
effective January 2005. Take of northern Mexican and narrow-headed
gartersnakes is no longer permitted in Arizona without issuance of a
scientific
[[Page 38720]]
collecting permit (Ariz. Admin. Code R12-4-401 et seq.) or special
authorization. While the AGFD can seek criminal or civil penalties for
illegal take of these species, the same provisions are not in place for
actions that result in destruction or modification of the gartersnakes'
habitat. In addition to making the necessary regulatory changes to
promote the conservation of northern Mexican and narrow-headed
gartersnakes, the AGFD's Nongame Branch continues to be a strong
partner in research and survey efforts that further our understanding
of current populations, and assist with conservation efforts and the
establishment of long-term conservation partnerships.
Throughout Mexico, the Mexican gartersnake is listed at the species
level of its taxonomy as ``Amenazadas,'' or Threatened, by the
Secretaria de Medio Ambiente y Recursos Naturales (SEMARNAT) (SEDESOL
2010, p. 71). Threatened species are ``those species, or populations of
the same, likely to be in danger of disappearing in a short or medium
timeframe, if the factors that negatively impact their viability, cause
the deterioration or modification of their habitat or directly diminish
the size of their populations continue to operate'' (Secretar[iacute]a
de Desarrollo Social (SEDESOL) 2010, p. 5). This designation prohibits
taking of the species, unless specifically permitted, as well as
prohibits any activity that intentionally destroys or adversely
modifies its habitat. Additionally, in 1988, the Mexican Government
passed a regulation that is similar to the National Environmental
Policy Act of the United States. This Mexican regulation requires an
environmental assessment of private or government actions that may
affect wildlife or their habitat (SEDESOL 1988 Ley General del
Equilibrio Ecol[oacute]gico y la Protecci[oacute]n al Ambiente
(LGEEPA)).
The Mexican Federal agency known as the Instituto Nacional de
Ecolog[iacute]a (INE) is responsible for the analysis of the status and
threats that pertain to species that are proposed for listing in the
Norma Oficial Mexicana NOM-059 (the Mexican equivalent to an endangered
and threatened species list), and, if appropriate, the nomination of
species to the list. INE is generally considered the Mexican
counterpart to the United States' Fish and Wildlife Service. INE
developed the Method of Evaluation of the Risk of Extinction of the
Wild Species in Mexico (MER), which unifies the criteria of decisions
on the categories of risk and permits the use of specific information
fundamental to listing decisions. The MER is based on four independent,
quantitative criteria: (1) Size of the distribution of the taxon in
Mexico; (2) state (quality) of the habitat with respect to natural
development of the taxon; (3) intrinsic biological vulnerability of the
taxon; and (4) impacts of human activity on the taxon. INE began to use
the MER in 2006; therefore, all species previously listed in the NOM-
059 were based solely on expert review and opinion in many cases.
Specifically, until 2006, the listing process under INE consisted of a
panel of scientific experts who convened as necessary for the purpose
of defining and assessing the status and threats that affect Mexico's
native species that are considered to be at risk, and applying those
factors to the definitions of the various listing categories. In 1994,
when the Mexican gartersnake was placed on the NOM-059 (SEDESOL 1994
(NOM-059-ECOL-1994), p. 46) as a threatened species, the decision was
made by a panel of scientific experts.
Although the Mexican gartersnake is listed as a threatened species
in Mexico and based on our experience collaborating with Mexico on
trans-border conservation efforts, no recovery plan or other
conservation planning occurs because of this status, and enforcement of
the regulation protecting the gartersnake is sporadic, depending on
available resources and location. Based upon the best available
scientific and commercial information on the status of the species, and
the historic and continuing threats to its habitat in Mexico, our
analysis concludes that regulatory mechanisms enacted by the Mexican
Government to conserve the northern Mexican gartersnake are not
adequate to address threats to the species or its habitat.
In summary, we reviewed a number of existing regulations that
potentially address issues affecting the northern Mexican and narrow-
headed gartersnakes and their habitats. Mexican law prohibits take of
the northern Mexican gartersnake and the intentional destruction or
modification of northern Mexican gartersnake habitat. However that law
has not led to a reduction in threats such that they no longer meet the
definition of endangered or threatened under the Act. Furthermore, most
existing regulations in the United States within the range of northern
Mexican and narrow-headed gartersnakes were not specifically designed
to protect the gartersnakes or their habitats, which is the overarching
threat to the species. For example, Arizona and New Mexico both have
statutes designed for protection of state-listed species that prohibit
the direct collection of individuals. However neither state law is
designed to provide protection of habitat and ecosystems. Therefore,
these laws are not reducing threats to the species such that they no
longer meet the definition of endangered or threatened under the Act.
Current Conservation of Northern Mexican and Narrow-Headed Gartersnakes
(Factor E)
Several conservation measures implemented by land and resource
managers, private land owners, and other stakeholders can directly or
indirectly benefit populations of northern Mexican and narrow-headed
gartersnakes. For example, the AGFD's conservation and mitigation
program (CAMP; implemented under an existing section 7 incidental take
permit) has committed to either stocking (with captive-bred stock) or
securing two populations each of northern Mexican and narrow-headed
gartersnakes to help minimize adverse effects to these species from
their sport fish stocking program through 2021 (USFWS 2011, Appendix
C). Other CAMP commitments include: (1) Developing a gartersnake
monitoring, research, and restocking plan to guide CAMP activities to
establish or secure populations; (2) developing outreach material to
reduce the deliberate killing or injuring of gartersnakes (placed in
high angler access areas); (3) ensuring that chemically renovated
streams are quickly restocked with native fish as gartersnake prey; (4)
conducting a live bait assessment team to develop recommendations to
amend live bait management; (5) reviewing and updating outreach
programs on the risks to native aquatic species from the transport of
nonnative aquatic species; (6) developing and implementing a public
education program on gartersnakes; and (7) working with the New Mexico
Department of Game and Fish to examine the roll of escaped rainbow
trout from Luna Lake into tributaries to the San Francisco River in
supporting narrow-headed gartersnakes. The programs' management
strategy is encapsulated in AGFD (2014a, entire) and progress on
activities through June 2013 is reported in AGFD (2012c, pp. 26-30;
2013b, pp. 37-44).
Significant challenges will have to be met for creating or securing
two populations each of northern Mexican or narrow-headed gartersnakes.
Captive propagation, if used to create stock for reintroductions, has
only been possible for northern Mexican gartersnakes. Specifically,
after approximately 6 years of experimentation with captive propagation
at five institutions, using two colonies of northern Mexican
[[Page 38721]]
gartersnakes and three colonies of narrow-headed gartersnakes, success
has been limited (see Gartersnake Conservation Working Group (GCWG)
2007, 2008, 2009, 2010). In 2012 and 2013, approximately 60 northern
Mexican gartersnakes were produced at one institution, 40 of which were
subsequently marked and released along Cienega Creek. These were the
first gartersnakes of either species to be produced under this program,
but the current status of released individuals remains unknown. No
narrow-headed gartersnakes have been produced in captivity under this
program since its inception. Secondly, in order to have the greatest
chance for success, the process of ``securing'' a population of either
species will likely involve an aggressive nonnative removal strategy,
and will have to account for habitat connectivity to prevent reinvasion
of unwanted species. Therefore, securing a population of either species
may involve removal of harmful nonnatives from an entire subbasin or on
a landscape scale (Cotton et al. 2014, pp. 12-13). In situations where
harmful nonnatives do not pose a threat to a given population, other
types of recovery actions may suffice.
To protect habitat for candidate, threatened, and endangered
species, including northern Mexican gartersnakes in the Agua Fria
subbasin, the AGFD purchased the approximate 200-acre (81-ha) Horseshoe
Ranch along the Agua Fria River located near the Bloody Basin Road
crossing, east of Interstate 17 and southeast of Cordes Junction,
Arizona. The AGFD plans (presumably in the next 5-10 years) to
introduce northern Mexican gartersnakes, as well as lowland leopard
frogs and native fish species, into a large pond, protected by bullfrog
exclusion fencing, located adjacent to the Agua Fria River. The
bullfrog exclusion fencing around the pond will permit the dispersal of
northern Mexican gartersnakes and lowland leopard frogs from the pond,
allowing the pond to act as a source population to the Agua Fria River.
The AGFD's short- to mid-term conservation planning for Horseshoe Ranch
will help ensure the northern Mexican gartersnake persists in this
historical locality.
In 2007, the New Mexico Department of Game and Fish completed a
recovery plan for narrow-headed gartersnakes in New Mexico (Pierce
2007, pp. 13-15) that included the following management objectives: (1)
Researching the effect of known threats to, and natural history of, the
species; (2) acquiring funding sources for research, monitoring, and
management; (3) enhancing education and outreach; and (4) managing
against known threats to the species. Implementation of the recovery
plan was to occur between the second half of 2007 through 2011, and was
divided into three main categories: (1) Improve and maintain knowledge
of potential threats to the narrow-headed gartersnake; (2) improve and
maintain knowledge of the biology of the narrow-headed gartersnake; and
(3) develop and maintain high levels of cooperation and coordination
between stakeholders and interested parties (Pierce 2007, pp. 16-17).
Our review of the plan found that it lacked specific threat-mitigation
commitments on the landscape, as well as stakeholder accountability for
implementing activities prescribed in the plan. We also found that
actions calling for targeted nonnative species removal or management
were absent in the implementation schedule provided in Pierce (2007, p.
17). As we have discussed at length, harmful nonnative species are the
primary driver of continued declines in both gartersnake species. No
recovery plan, conservation plan, or conservation agreement currently
exists in New Mexico with regard to the northern Mexican gartersnake
(NMDGF 2006, Table 6-3).
In Arizona's State Wildlife Action Plan 2012-2022 (SWAP) (AGFD
2012b, Appendix E), both the northern Mexican and narrow-headed
gartersnake are Tier 1A Species of Greatest Conservation Need (SGCN).
SGCN include those ``species that each State identified as most in need
of conservation actions'' and Tier 1A species include ``those species
for which the Department has entered into an agreement or has legal or
other contractual obligations, or warrants the protection of a closed
season'' (AGFD 2012b, p. 16). The SWAP is not a regulatory document,
and does not provide any specific protections for either the
gartersnakes themselves, or their habitats. The AGFD does not have
specified or mandated recovery goals for either the northern Mexican or
narrow-headed gartersnake, nor has a conservation agreement or recovery
plan been developed for either species.
Indirect benefits for both gartersnake species occur through
recovery actions designed for their prey species. Since the Chiricahua
leopard frog was listed as threatened under the Act, significant
strides have been made in its recovery, and the mitigation of its known
threats. The northern Mexican gartersnake, in particular, has likely
benefitted from these actions, at least in some areas, such as at the
Las Cienegas Natural Conservation Area and in Scotia Canyon of the
Huachuca Mountains. However, much of the recovery of the Chiricahua
leopard frog has occurred in areas that have not directly benefitted
the northern Mexican gartersnake, either because these activities have
occurred outside the known distribution of the northern Mexican
gartersnake or because they have occurred in isolated lentic systems
that are far removed from large perennial streams that typically
provide source populations of northern Mexican gartersnakes. In recent
years, significant strides have been made in controlling bullfrogs on
local landscape levels in Arizona, such as in the Scotia Canyon area,
in the Las Cienegas National Conservation Area, on the BANWR, and in
the vicinity of Pena Blanca Lake in the Pajarito Mountains. Recent
efforts to return the Las Cienegas National Conservation Area to a
wholly native biological community have involved bullfrog eradication
efforts, as well as efforts to recover the Chiricahua leopard frog and
native fish species. These actions should assist in conserving the
northern Mexican gartersnake population in this area. Bullfrog control
has been shown to be most effective in simple, lentic systems such as
stock tanks. Therefore, we encourage livestock managers to work with
resource managers in the systematic eradication of bullfrogs from stock
tanks where they occur, or at a minimum, ensure they are never
introduced.
An emphasis on native fish recovery in fisheries management and
enhanced harmful nonnative species control to favor native communities
may be the single most efficient and effective manner to recover these
gartersnakes, in addition to appropriate management for all listed or
sensitive native fish and amphibian species upon which they prey.
Alternatively, resource management policies that are intended to
directly benefit or maintain harmful nonnative communities, and which
will likely exclude native species, will significantly reduce the
potential for the conservation and recovery of northern Mexican and
narrow-headed gartersnakes, in those areas where they overlap with
habitat occupied by either gartersnake.
Fisheries managers strive to balance the needs of the recreational
angling community against those required by native aquatic communities.
Fisheries management has direct implications for the conservation and
recovery of northern Mexican and narrow-headed gartersnakes in the
United States. Clarkson et al. (2005) discuss management conflicts as a
primary factor in the decline of native fish species in the
southwestern United States, and declare the entire native fish
[[Page 38722]]
fauna as imperiled. The investigators cite nonnative species as the
most consequential factor leading to rangewide declines of native fish,
and that such declines prevent or negate species' recovery efforts from
being implemented or being successful (Clarkson et al. 2005, p. 20).
Maintaining the status quo of current management of fisheries within
the southwestern United States will have serious adverse effects to
native fish species (Clarkson et al. 2005, p. 25), which will affect
the long-term viability of northern Mexican and narrow-headed
gartersnakes and their potential for recovery. Clarkson et al. (2005,
p. 20) also note that over 50 nonnative species have been introduced
into the Southwest as either sportfish or baitfish, and some are still
being actively stocked, managed for, and promoted by both Federal and
State agencies as nonnative recreational fisheries.
To help resolve the fundamental conflict of management between
native fish and recreational sport fisheries, Clarkson et al. (2005,
pp. 22-25) propose the designation of entire subbasins as having either
native or nonnative fisheries and manage for these goals aggressively.
The idea of watershed-segregated fisheries management is also supported
by Marsh and Pacey (2005, p. 62). As part of the AGFD's overall
wildlife conservation strategy, the AGFD has planned an integrated
fisheries management approach (AGFD 2012b, p. 106), which is apparently
designed to manage subbasins specifically for either nonnative or
native fish communities. This strategy is described in detail in AGFD
(2009, entire), but the AGFD has not yet initiated implementation of
this strategy or decided how fisheries will be managed in Arizona's
subbasins, and we are not aware of a specific implementation timeline.
However, the ``current fish assemblage,'' ``current recovery or
conservation category,'' and ``current angling category'' inform what
is referred to as Step 2c: Identification of Current Fishery Values''
(AGFD 2009, pp. 10-11). Factors such as angler access (which
contributes directly to angler use days (AUD)), existing fish
communities, and stream flow considerations are likely to inform such
broadly based decisions.
Due to the relative scarcity of perennial streams in arid regions
such as Arizona, several of Arizona's large perennial rivers present an
array of existing sport fishing opportunities and angler access points,
and already contain harmful nonnative fish species that are considered
sport fish. We anticipate that these rivers may be preferred as
nonnative fisheries under the watershed designation process. Another
significant and confounding factor is the AGFD's ``no net loss'' policy
that addresses sport fishery resources statewide. There is no official
written AGFD Commission guidance on ``no net loss'' according to AGFD
(2009, Appendix D), but ``Commission policy DOM [Arizona Game Fish
Department Operating Manual] A2.24, Wildlife Management Program Goal
and Objective 6 states, `provide and promote fishing
opportunities to sustain a minimum of 8,000,000 AUD per year by June
30, 1997.' Although this policy has yet to be revised by the
Commission, based on current data, we remain below 8,000,000 AUD's
statewide (AGFD 2009, Appendix D). As such, it was determined the
Department's goal to manage for no net loss is consistent with current
Commission policy (A2.24). The ``no net loss'' policy is a guiding
tenet, and its implementation is directed as follows (AGFD 2009,
Appendix D):
``When a sport fishery is valued less than a native aquatic
conservation value within a management unit, the loss of sport
fishing opportunity will be compensated for by gain of an equal
number of AUDs in another area or management unit. This opportunity
will be created within the same watershed when possible. For this
purpose, a watershed is defined as a six-digit-numbered area
referenced on the USGS's Hydrological Unit Map. If this is not
possible, the opportunity will be created within the same Department
regional boundaries. Again, if this is not possible, the opportunity
will be created somewhere within the State with extensive
coordination between regional staff. If a net loss cannot be
avoided, the Director will evaluate if the loss is acceptable by
gauging the input from the public process leading to the
recommendation and may take the information to the Commission at his
discretion. The replacement opportunity will be initiated no more
than two years following the loss to anglers.''
Extensive coordination between AGFD and the Service will be
required under the no net loss policy with regard to gartersnake
conservation and recovery because the amount of suitable riparian and
aquatic habitat is finite, yet, somehow, the existing opportunity for
AUD must be maintained. This increases the uncertainty for the
persistence of existing gartersnake populations in Arizona.
Large perennial rivers that serve as sport fisheries also currently
serve as important habitat for northern Mexican or narrow-headed
gartersnake. If designated for sportfishing, fisheries management of
these rivers would likely include the maintenance of predatory sport
fish species, which would likely diminish the recovery potential for
gartersnakes in these areas, and, perhaps, even result in the local
extirpations of populations of northern Mexican and narrow-headed
gartersnakes. Alternatively, subbasins that are targeted for wholly
native species assemblages would likely secure the persistence of
northern Mexican and narrow-headed gartersnakes that occur there, if
not result in their complete recovery in these areas. Specific
subbasins where targeted fisheries management is to occur were not
provided in AGFD (2012b), but depending on which areas are chosen for
each management emphasis, the potential for future conservation and
recovery of northern Mexican and narrow-headed gartersnakes could
either be significantly bolstered, or significantly hampered. Close
coordination with the AGFD on the delineation of fisheries management
priorities in Arizona's subbasins will be instrumental to ensuring that
conservation and recovery of northern Mexican and narrow-headed
gartersnakes can occur.
Conservation of these gartersnakes has been implemented in the
scientific and management communities as well. The AGFD recently
produced identification cards for distribution that provide information
to assist field professionals with the identification of each of
Arizona's five native gartersnake species, as well as guidance on
submitting photographic vouchers for university museum collections.
Arizona State University and the University of Arizona now accept
photographic vouchers in lieu of physical specimens, in their
respective museum collections. These measures appreciably reduce the
necessity for physical specimens (unless discovered postmortem) for
locality voucher purposes and, therefore, further reduce impacts to
vulnerable populations of northern Mexican or narrow-headed
gartersnakes.
Despite these collective conservation efforts we have described
above, northern Mexican and narrow-headed gartersnakes have continued
to decline throughout their ranges due to past, current, and future
threats that have not been addressed through conservation efforts.
Summary of Changes From the Proposed Rule
Based on information provided during the comment period by the
general public, tribes, states, and peer reviewers, we updated the
information contained in the proposed rule for incorporation into this
final rule. In addition, new references were obtained,
[[Page 38723]]
evaluated, and discussed in the deliberation of information in the
final rule that were either not available or not obtained during the
development of the proposed rule. For clarity, we also revised the
language used in our Findings for the listing rule and in the
background and regulatory language of the 4(d) rule. However, no
substantive changes were made to either the conclusion of the final
listing rule or the scope of the final 4(d) rule.
Summary of Comments and Recommendations
In the proposed rule published on July 10, 2013 (78 FR 41500), we
requested that all interested parties submit written comments on the
proposal by September 9, 2013. We also contacted appropriate Federal,
State, and Tribal agencies, scientific experts and organizations, and
other interested parties and invited them to comment on the proposal.
Newspaper notices inviting general public comment were published in the
Verde Valley Independent, Camp Verde Bugle, Arizona Daily Star, and the
Silver City Sun News. We received a request for a public hearing from
the Hereford Natural Resource Conservation District who later withdrew
their request.
Our summary responses to the substantive comments we received on
the proposed listing rules and proposed 4(d) rule are provided below.
Comments simply providing support for or opposition to the proposed
rule, without any supporting information, were not considered to be
substantive and we do not provide a response.
Peer Reviewer Comments
In accordance with our peer review policy published on July 1, 1994
(59 FR 34270), we solicited expert opinion from eight knowledgeable
individuals with scientific expertise that included familiarity with
northern Mexican and narrow-headed gartersnakes and their habitat,
biological needs, and threats. We received responses from five of the
peer reviewers.
We reviewed all comments received from the peer reviewers for
substantive issues and new information regarding the listing of
northern Mexican and narrow-headed gartersnakes. All peer reviewers
shared the opinion that a thorough examination of all available
information was conducted in support of listing these gartersnakes.
Peer reviewers also commented that the quality of the information
presented in the proposed rule was very high and the analyses were
thorough. There were concerns expressed regarding whether listing these
gartersnakes as threatened would interfere with ongoing recovery
actions for listed fish species where they co-occur. Another concern
was based on how threats affecting these gartersnakes were prioritized
in their scope and magnitude in the proposed rule. In general, peer
reviewers generally concurred with our methods and conclusions and
provided additional information, clarifications, and suggestions to
improve the final rule. Peer reviewer comments are addressed in the
following summary and incorporated into the final rule as appropriate.
Comment 1: The term ``spiny-rayed fish'' has a very specific
scientific meaning, which is not consistent with its use in the
proposed rule. While this group includes some of the nonnative species
of concern, such as sunfish and bass, it does not include others,
specifically the catfishes. Also, the term spiny-rayed fishes as used
here excludes a suite of nonnative fishes that are problematic for
native fish species and likely for northern Mexican gartersnake and
narrow-headed gartersnake, such as nonnative trouts (especially highly
predaceous brown trout (Salmo trutta), red shiner (Cyprinella
lutrensis), and mosquitofish (Gambusia affinis)). The term ``spiny-
rayed fishes'' should either be eliminated from the document and
replaced with accurate terminology or be defined specifically for its
intended use in the rule. The Service should dispense entirely with use
of ``spiny-rayed fishes'' and use only the term ``nonnative fishes.''
Our Response: In the proposed rule, we intended to identify those
species of nonnative fish that were both considered highly predatory on
gartersnakes and also highly competitive with gartersnakes in terms of
common prey resources. The nonnative fish species we view as most
harmful to gartersnake populations include bass (Micropterus sp.),
flathead catfish (Pylodictis sp.), channel catfish (Ictalurus sp.),
sunfish, bullheads (Ameiurus sp.), bluegill (Lepomis sp.), crappie
(Pomoxis sp.,) and brown trout (Salmo trutta). We agree that all
nonnative fish species pose some level of threat to native aquatic
ecosystems. However, it is important to highlight those nonnative fish
species that pose the greatest threat to assist in prioritizing future
conservation actions that are most beneficial to northern Mexican and
narrow-headed gartersnakes. Therefore, we have specifically defined in
the beginning of this final rule, what nonnative fish species are
considered ``predatory'' and what nonnative species we consider
``harmful.''
Comment 2: It would be helpful to the reader to visualize the
historical and current ranges of the two snakes if range maps were
included.
Our Response: Current distribution maps were provided and are
available in the proposed rule to designate critical habitat for the
northern Mexican and narrow-headed gartersnake, which accompanied the
proposed rule to list the species in the Federal Register (78 FR 41550,
July 10, 2013, p. 41586).
Comment 3: The sentence ``Fleharty (1967, p. 227) reported narrow-
headed gartersnakes eating green sunfish, but green sunfish is not
considered a suitable prey item'' needs clarification. Specifically,
the authors need to provide evidence that green sunfish is not a
suitable prey item. Just because green sunfish has spines in their
medial (caudal excluded) and lateral fins does not mean that it is not
suitable prey.
Our Response: We added further clarification to this text to
support this statement in the final rule under ``Habitat and Natural
History'' for the narrow-headed gartersnake.
Comment 4: Please provide examples of ``barriers to movement'' of
narrow-headed gartersnakes and additional information on the ``salvage
efforts'' in the discussion leading into Table 2.
Our Response: We provided examples and additional information in
the text in the final rule under ``Current Distribution and Population
Status.''
Comment 5: With respect to nonnative fish species in the Gila River
basin, all were either intentionally or accidentally introduced by
humans; there is no evidence that any species gained access to the
basin through natural colonization as inferred in the proposed rule.
Our Response: We agree that no evidence exists to support
unassisted migration of nonnative fish species into the Gila River
basin from outside the basin. However, we acknowledge that harmful
nonnatives, once introduced, are fully capable of naturally dispersing
within the watershed where habitat connectivity permits. This latter
concept was the impetus for the notion of ``natural colonization'',
which is also referred to as dispersal.
Comment 6: The proposed rule mentions only trout of the genus Salmo
as occurring in habitat occupied by either gartersnake. Rainbow trout
(Oncorynchus mykiss) and brook trout (Salvelinus fontinalis) also
occur.
Our Response: This oversight has been corrected in the final rule
in the subsection ``Fish'' within the subheading ``Decline of the
Gartersnake Prey Base.''
[[Page 38724]]
Comment 7: The statements that nonnative fish ``tend to occupy the
middle and upper zones in the water column'' while native fish tend to
occur ``along the bottom'' is not entirely accurate. For example, all
of the catfishes (all of which are nonnative in the Gila River system)
are benthic in habit, and these are among the species considered
harmful to gartersnakes and their prey. Among native fishes in the Gila
River system only loach minnow would be characterized as benthic,
although most native suckers and minnows (chubs largely excluded) do
forage along surfaces, including the bottom. Moreover, large numbers of
native fish, longfin dace (Agosia chrysogaster) in particular, occur in
shallow habitats where differentiating a position in the water column
is problematic.
Our Response: We have amended the discussion in the subsection
``Fish'' within the subheading ``Decline of the Gartersnake Prey Base''
in the final rule to specify which groups of native or nonnative fish
are likely to occur where in the water column.
Comment 8: It seems unlikely that Yaqui catfish were suitable prey
for gartersnakes, given their stiff pectoral and dorsal spines, and
humpback chub likely never co-occurred with either gartersnake.
Woundfin, conversely, has records from the lower Salt River at Tempe
and would have been a listed prey species.
Our Response: We have removed humpback chub and Yaqui catfish, and
added woundfin, as species noted that were possible prey species of
either gartersnake and that are now listed under the Act.
Comment 9: Brown trout are highly predacious and should be
considered as harmful nonnative wildlife by the Service.
Our Response: We have reevaluated potential effects of brown trout
predation on native aquatic vertebrates and concur that brown trout are
highly predatory in all size classes and in a wide range of water
temperatures. Thus, we have identified the brown trout as a
``predatory'' nonnative fish species and discuss its ecological
significance in the final rule in the subsection ``Fish'' within the
subheading ``Decline of the Gartersnake Prey Base.''
Comment 10: In the proposed rule, the Service identified several
streams in Arizona or New Mexico where nonnative fish present
management issues. However, nonnative fish are a concern for management
of native fish throughout Arizona and New Mexico, not only those
streams specifically mentioned. They are an issue where they already
are present and in those habitats where they may invade or be
introduced in the future, which included virtually any watercourse or
body of water throughout the region.
Our Response: We added language to reflect this fact in the
subsection ``Fish'' within the subheading ``Decline of the Gartersnake
Prey Base.''
Comment 11: With respect to potential effects from fisheries
management activities, it would appear that gartersnakes still occur in
many of the streams that have received piscicide treatments. If so, why
are these streams and their renovation history discussed in the
proposed rule because there is no evidence that chemical treatment in
any of these instances eliminated, depleted, or otherwise impacted a
resident gartersnake population. The loss of a major portion, or
entire, prey base of a gartersnake population will result in the loss
of individuals from starvation, which is expected to result in weakened
population viability and, potentially, the loss of that population
depending on the presence of other stressors, the proximity of the
next-closest source population, and the status of the population prior
to treatment.
Our Response: If the intent of a renovation is to remove all fish
from a stream, and the stream is occupied by either gartersnake, which
wholly or partially requires fish in their prey base, the logical
conclusion is that adverse effects to gartersnakes, at least
temporarily, are likely under these circumstances. The presence of
either gartersnake in a treated stream after the treatment is not
evidence that no adverse effects to individuals have occurred.
Comment 12: Traditionally, pre-treatment salvage and post-treatment
restocking favor larger-bodied size classes of native fish, which could
reproduce and provide smaller prey for gartersnakes over a period of
time. Small-bodied species would also be saved for salvage and
restocking, but are more difficult to find. How are the interests of
the gartersnakes rectified in these situations? Alternatively,
gartersnakes themselves could be salvaged and restocked at a later date
after a prey base has been established.
Our Response: We agree that fish salvage operations, prior to
treatment, are likely to favor larger individuals that may exceed the
size classes most preferred by gartersnakes as prey. For this reason,
we intend to explore partnerships and opportunities for raising native
fish of appropriate size classes in hatchery settings for subsequent
release into treated streams, post treatment. Based upon our evaluation
of the literature and cooperative work with gartersnakes, alternative
prey species and appropriate size classes are well-understood. We are
not, however, aware of any studies that focused on how long a
gartersnake could go without food before physiological stress or
starvation. We do know that, compared to snakes within other genera or
families, gartersnakes have a relatively fast metabolism and are active
foragers, implying that physiological stress or starvation may be more
of a concern in the absence of prey.
There are significant challenges with salvaging gartersnakes for
long-term captivity. First, facilities with the space, equipment, and
knowledge to care for larger numbers of gartersnakes for long periods
of time are very few, and currently those that are capable, are nearly
at full capacity because of their involvement with captive breeding
efforts. Second, narrow-headed gartersnakes have proven to be difficult
to maintain in captivity due to their unique physiological and prey
requirements. Lastly, it may prove difficult if not impossible to
salvage gartersnakes from low-density populations within complex
habitat and therefore the risk of their complete extirpation from a
renovation activity is elevated. In the event an isolated population is
extirpated, the risk of forever losing their unique genetic lineage is
also elevated and unacceptable.
Comment 13: The discussion about electrofishing impacts to
gartersnakes is misleading and misinformed. The statement that
``gartersnakes present within the water are often temporarily paralyzed
from electrical impulses intended for fish'' is true only to the extent
that the gartersnake actually is present and available to intercept the
electrical current. Personal experience and interviews with colleagues
suggest that encounters of electroshockers and gartersnakes are
exceptionally rare, not ``often'' as suggested by the Service. Next,
use of the term ``electrocution'' is inappropriate as it by definition
means killing, which is not only rare for electroshocked fishes, but
unknown for gartersnakes.
Our Response: The statement in the proposed rule, ``gartersnakes
present within the water are often temporarily paralyzed from
electrical impulses intended for fish'' was intended to mean that
gartersnakes had to be present in the water and within the affected
radius of the electroshocker, otherwise the assumption is they would
not be affected and thus, not detected. By use of the term
``electrocuted,'' it was not
[[Page 38725]]
our intention to imply that gartersnakes which received an electrical
charge were mortally wounded. We have removed the use of this term from
the final rule. ``Detections'' as cited in the document are not
``electrocutions.'' Reports of gartersnakes detected during
electrofishing may be misleading because it is unclear if those
attributed to Hellekson (2012, pers. comm.) were during surveys for
fishes or for reptiles and amphibians, while detections reported by
Pettinger and Yori (2011) apparently were during surveys for Chiricahua
leopard frog and not for fishes. Lastly, the references cited where
gartersnakes were detected via electroshocking referred to fisheries
surveys; electroshocking is not a recognized method for aquatic
herpetofauna surveys. We amended the text in this final rule under the
heading ``Risks to Gartersnakes from Fisheries Management Activities,''
subheading ``Mechanical Methods'' to better communicate our assessment
of the potential effect of electrofishing surveys on gartersnakes.
Comment 14: The term ``self-baiting'' is rarely if ever used by
fisheries professionals in reference to wire minnow traps.
Our Response: We used the term ``self-baiting'' with respect to how
these types of mechanical traps work for gartersnake surveys, which is
indeed through the function of self-baiting with minnows, amphibian
larvae, etc. However, the term's use in discussing the use of these
traps for fisheries surveys was inaccurate, and the term has been
removed from the sentence where it was used in the proposed rule.
Comment 15: The proposed rule provides two references documenting
examples of gartersnakes that drowned in wire minnow traps. One
reported from Holycross et al. (2006) and the other from Boyarski
(2011). Holycross et al. (2006) never mentions the word ``drown'' in
their report. It is also noted that these few minnow-trap related
fatalities occurred during surveys specifically to capture
gartersnakes, that is, the investigators were targeting gartersnakes
with this effort. The inadvertent capture of a gartersnake is an
exceptionally rare occurrence and has not been reported from fisheries
survey activities.
Our Response: The reference of Holycross et al. (2006) describes
the flooding event, but not the death of an individual gartersnake,
which was incidentally killed in a trap when flooding occurred
(observed by Service biologists). We discuss the potential threat of
gartersnake fatality from minnow traps used in fishery surveys because
the threat is real. Gartersnakes will forage at any position within the
water column; northern Mexican gartersnakes often forage at the water
surface and in intermediate depths, while the narrow-headed gartersnake
forages most frequently along the bottom. The fact that minnow traps
for fishery surveys are generally set overnight and checked at least
twice daily, and always during morning does not alleviate this threat.
The reason that minnow traps used for gartersnake surveys are set at
the surface with half of the trap above the water line is to prevent
drowning of captured gartersnakes. When used for fisheries purposes,
these traps incidentally self-bait with gartersnake prey species (the
intended purpose is to capture fish) and are set below the water line.
Checking the traps a few times daily will not prevent air-breathing,
nontarget organisms from drowning if captured. We also note that both
gartersnake species can be active at night, but are not certain their
activity includes foraging. We did not intend to portray that the
incidental capture of gartersnakes by minnow-trapping for fishery
surveys happens frequently, but where it could incidentally result in
the loss of one or more reproductive females in low population
densities, a population-level effect could result. Lastly, we clarified
in the final rule that funnel traps are not used in fishery surveys.
Comment 16: Relative to fisheries management activities, it cannot
be stressed enough that there currently is no effective strategy to
eliminate harmful nonnative fishes other than use of piscicides and
their use is critical for native fish recovery. It should also be noted
that fisheries activities effects are trivial compared to those
attributed to herpetological activities and other human factors.
Our Response: We concur that chemical renovations are vital to
native fish recovery. To further clarify the vital importance of
piscicide use in the recovery of the gartersnakes' native prey base and
the gartersnakes themselves, we amended the passage in the final rule
under the heading ``Risks to Gartersnakes from Fisheries Management
Activities,'' subheading ``Piscicides.''
We are confident that the discussion in the proposed and final
rules attributed to the potential threats to these gartersnakes from
the implementation of fishery management activities is objective,
thoroughly referenced, and balanced. We agree that other human-caused
threats can pose comparably greater risks to gartersnakes. But, we
disagree with the notion that incidental fatality from herpetological
surveys are potentially more significant than activities that eliminate
an entire suite of prey species from habitat occupied by gartersnakes.
We also stress that listing these two gartersnakes should not be
construed as an obstacle to native fish recovery under any
circumstances. Rather, the recovery of these gartersnakes is
inextricably and ecologically linked to native fish recovery.
Comment 17: How many stock tanks are known within the range of
northern Mexican gartersnake and what proportion of these meet criteria
for being ``well-managed?'' Few stock tanks are well-managed, and most
lack peripheral vegetation that would function as suitable habitat for
gartersnakes. The Service provides no information to address these
questions, which is necessary to evaluate the actual or potential
contribution of stock tanks to gartersnake conservation.
Our Response: The actual number of stock tanks that occur within
the distribution of the northern Mexican gartersnake is not currently
known because not all tanks are georeferenced in GIS databases.
However, based upon their common occurrence on the landscape, we
conclude that the number is very large, possibly in the 100's. We also
have no quantitative data on the number of tanks that are ``well-
managed.'' Regardless, based upon our collective knowledge of how these
habitats are used by northern Mexican gartersnakes and primary prey
species, particularly in southern Arizona, we consider their existence
as a vital contribution to conservation of the northern Mexican
gartersnake. Based on our knowledge of habitat variables that best
predict whether a gartersnake population could be sustained, the
presence of a native prey community and the absence of harmful
nonnative species appear to be the most predictive factors. Peripheral
vegetation may provide cover for gartersnakes in stock tanks where
harmful nonnatives occur, but it is not necessary for gartersnake
populations in all circumstances. It may be possible that stock tanks
have replaced, in part, the role of natural cienegas as important
gartersnake habitat, although no direct study has been attributed to
this hypothesis. While stock tanks in different drainages can be
invaded by bullfrogs or crayfish by means of natural dispersal, they
can also represent easily managed habitat to protect against (or
rectify) invasion of harmful nonnative species. For these reasons, we
currently value the
[[Page 38726]]
existence of stock tanks for northern Mexican gartersnake conservation.
Comment 18: Mine spills are a threat to gartersnakes and to their
fish prey. For example, mine spills made the San Pedro River toxic for
a time, and a naturally occurring population of endangered Gila
topminnow in Cocio Wash, Arizona, was exterminated by a mine spill.
Numerous other examples of this threat are available and should be
included.
Our Response: We expanded our discussion of the threat of mining
pollution under the heading ``Environmental Contaminants,'' to include
the example from the San Pedro River.
Comment 19: Regarding the discussion about management emphasis
relative to native and nonnative fishes, it should be acknowledged
that, at least in Arizona, the management priority is recreational
fisheries, and the operative AGFD's policy is ``no net loss'' of sport
fishing opportunities when attempting to balance sport fish and native
fish management. It is well documented by literature cited in the
proposed rule that native fishes and nonnative fishes cannot coexist in
the long term other than under exceptional circumstances.
Our Response: We understand the concern for the future of native
fish and by extension, northern Mexican and narrow-headed gartersnakes.
We included discussion of the ``no net loss'' policy in the final rule
under the heading ``Current Conservation of Northern Mexican and
Narrow-headed Gartersnakes.''
Comment 20: The Service used the presence of a native prey species
as evidence that a given area or stream may be occupied by northern
Mexican gartersnakes. This approach seems optimistic at best, and
perhaps, when the importance of habitat is also considered, not
scientifically justified. If native prey species are present, but the
habitat extent is too small, it is possible that northern Mexican
gartersnakes did not occur or will not persist.
Our Response: In determining whether historically occupied habitat
remains occupied, we considered habitat surrogates in the determination
where gartersnake survey data was limited. Native prey species remain
an important attribute for northern Mexican gartersnake habitat and
their presence in an area is evidence that the resident, native biotic
community may still offer native prey. It is also reasonable to assume
that not every site along a stream course is suitable habitat for
northern Mexican gartersnakes; these sites may be occupied by
dispersing individuals, however. We think that using these habitat
parameters as surrogates for occupied areas by the northern Mexican
gartersnake is an appropriate use of the best available information, in
the absence of more detailed information.
Comment 21: We have recently surveyed and trapped Little Ash Creek
(August 2013); it has abundant nonnative fish species and crayfish,
scarce native dace populations, and very few (n = 1 captured)
bullfrogs. The habitat extent (creek size) is small and we suspect it
no longer supports northern Mexican gartersnakes so the population is
likely extirpated.
Our Response: We appreciate the updated information. However, the
continued presence of some native fish and limited bullfrog detections
are signs that northern Mexican gartersnakes could still exist, albeit
at low or very low abundance, in Little Ash Creek. Moreover, individual
gartersnakes could disperse from the Agua Fria River, to which Little
Ash Creek is a tributary. We have not yet officially adopted a protocol
to establish population extirpation, but at a minimum, we expect such a
protocol should include robust survey data from multiple consecutive
years to account for detectability constraints in low-density
populations. Until such a protocol is adopted, we hesitate to conclude
that gartersnakes are extirpated from a given area, such as Little Ash
Creek.
Comment 22: Additional sites not encompassed by Table 1 include:
Tavasci Marsh (Nowak et al. 2011; population possibly not viable but
likely supported by recruitment from the Verde River); Peck's Lake
(Schmidt et al. 2005; population possibly not viable but likely
supported by recruitment from the Verde River), and Dead Horse Ranch
State Park (Emmons and Nowak 2013; population likely viable).
Our Response: We are aware of these populations and included them
with the Verde River mainstem due to their close proximity.
Comment 23: The proposed rule cites Rosen and Schwalbe (1988, pp.
34-35) for a list of plant species associations for narrow-headed
gartersnake habitat. Reliance on a single citation (whose results were
based on visual encounter surveys) to infer distribution-wide habitat
use is inappropriate. Please include intensive study data from Nowak
and Santana-Bendix (2002) and Nowak (2006) for a more complete look at
narrow-headed gartersnake-plant associations.
Our Response: Rosen and Schwalbe (1988, entire) sampled narrow-
headed gartersnake populations in a multitude of streams across their
range in Arizona and, therefore, represent a more comprehensive list of
plant species associations in a rangewide context. Nowak and Santana-
Bendix (2002) and Nowak (2006) focus solely on one population at Oak
Creek and, therefore, do not account for variability of preferred
habitat across the species' range.
Comment 24: The Service stated that sexual maturity in narrow-
headed gartersnakes occurs at 2.5 years of age in males and at 2 years
of age in females (Deganhardt et al. 1996, p. 328). I suspect this
assertion is overstated and scientifically inaccurate, based on field
studies and on animals currently maintained in captivity. Captive-born
female narrow-headed gartersnakes from the Black River (Arizona)
maintained in captivity did not lay eggs until their third summer, even
though they reached adult size within their second year (Nowak,
unpublished data, 2012).
Our Response: In the absence of other published data, we will
continue to rely on published information regarding the sexual maturity
data presented and referenced. In addition, observations made in
captive situations may be misleading because they may not reflect
factors affecting wild populations.
Comment 25: The proposed rule provided a list of areas where
narrow-headed gartersnakes could be reliably found. The Upper Verde
River, Tonto Creek, and the Blue River should also be included in this
list. While occurring in low densities, individuals in these
populations can still be reliably found with minimal to moderate effort
(e.g., Upper Verde River: Emmons and Nowak 2012a, Emmons and Nowak
2013; Tonto Creek: Madara-Yagla 2010, 2011; and Blue River: Rosen and
Nowak unpubl. data, 2012).
Our Response: The population and survey data reported in Appendix A
provide the basis for where narrow-headed gartersnakes are reliably
found. Populations considered likely viable have received significantly
more field study in most cases and, where they haven't, recent survey
data show robust population densities with minimal survey effort. We
understand the inherent challenges with defining a population's status
with a single phrase or term, but the data do not currently show that
narrow-headed gartersnake populations in the Upper Verde, Tonto Creek,
or the Blue River are near as robust as those identified as likely
viable in Table 2. In the case of Tonto Creek, narrow-headed
gartersnake records are comparably few, and Madara-Yagla (2010, 2011)
address only northern Mexican gartersnakes. Unpublished data from the
Blue River
[[Page 38727]]
were not provided to us, and until those data are provided and
reviewed, we are unable to update the status of that population, if
warranted.
Comment 26: If only 8 to 10 percent of historic populations are
viable, with significant post-fire concerns for populations from
Whitewater Creek and the Black River, should this species be proposed
for listing as ``Endangered?''
Our Response: The current status of the northern Mexican and
narrow-headed gartersnakes meets the definition of threatened, not
endangered. We found that both gartersnakes are not currently in danger
of extinction because they remain extant in most of the subbasins where
they historically occurred, and known threats have not yet resulted in
substantial range reduction or substantial number of population
extirpations to put either species on the brink of extinction. However,
we do find that the ongoing effects of the threats make both species
likely to become endangered in the foreseeable future. Please see the
sections entitled ``Determination for Northern Mexican Gartersnakes''
and ``Determination for Narrow-headed Gartersnakes'' for further
discussion of our determinations.
Comment 27: Regarding Table 2, state that the population at Saliz
Creek, New Mexico is introduced; three recaptured individuals were
found there in 2013; however, the population is likely not viable. In
addition, I do not know of any post 1990's records from the San
Francisco River in New Mexico; this population is ``likely extirpated''
(Hibbitts et al. 2009).
Our Response: Saliz Creek is a tributary to the San Francisco
River. The San Francisco River formerly had a robust population of
narrow-headed gartersnakes. Saliz Creek lies between two additional
tributaries to the San Francisco River, Whitewater Creek and the
Tularosa River, which historically and currently (respectively) also
had robust populations. Saliz Creek also boasts a largely native fish
community, with the exception of its lower-most reach. Furthermore,
prior to 2012, a total of 10 person-search hours were spent surveying
for narrow-headed gartersnakes attributed to Saliz Creek, which does
not constitute adequate survey effort to determine presence or absence.
No compelling data suggest that narrow-headed gartersnakes never
historically occurred in Saliz Creek prior to their release in 2012.
Regarding population status in the San Francisco River, more recent
survey efforts from 2009-2011, consisting of approximately 100 person-
search hours, reconfirmed the narrow-headed gartersnake as extant in
the San Francisco River in New Mexico with documentation of three
narrow-headed gartersnakes (Hellekson 2012a, pers. comm.). Therefore,
we treat this population as likely not viable rather than likely
extirpated.
Comment 28: The statement attributed to Rosen et al. (2001, p. 22)
that the presence and expansion of nonnative predators is the primary
cause of decline in northern Mexican gartersnakes and their prey in
southeastern Arizona may not have been properly characterized. This
paper does not state that nonnative predators are the only factor, but
instead it explicitly states the importance of other factors such as
climate and interspecific competition. Also, the paper's conclusions
are subjective and are generally presented as testable hypotheses, and
should be cited with caution rather than presented as scientifically
tested facts.
Our Response: We agree that Rosen (2001) did not state that
nonnative species are the only reason for northern Mexican gartersnake
declines in southern Arizona, rather harmful nonnatives were considered
as the primary cause at most sites surveyed, as described in the
proposed rule. Rosen (2001, p. 21) postulated that ``natural climatic
fluctuation'' may be responsible for a northern Mexican population
decline at one site in southern Arizona, which is not to say that it
was regarded in equal value as harmful nonnative species in affecting
northern Mexican gartersnakes in southern Arizona. Interspecific
competition was also discussed in Rosen (2001) as a cause for concern
at some sites. We evaluated the role of climate change and
interspecific competition in other sections of the proposed and final
rules as their discussion is not appropriately placed in the section
referred to here. However, we changed the word ``concluded'' in this
sentence to ``hypothesized.''
Comment 29: The proposed rule discusses the importance of a varied
prey base and cites a study that experimented with food deprivation on
the common gartersnake (T. sirtalis). There is no scientifically valid
reason to conclude that a varied diet could not include bullfrogs as a
replacement for native leopard frogs, especially where bullfrogs are
currently abundant. It may not be scientifically valid to infer that
foraging, physiological, and behavioral data collected from the common
gartersnakes will be representative of the populations of southwestern
gartersnakes. As such, I disagree that the common gartersnake is an
``ecologically similar species'' to northern Mexican gartersnake.
Our Response: We state on several occasions in the proposed rule
that larval and sub-adult bullfrogs are eaten by northern Mexican
gartersnakes in the mid- to larger-size classes. However, bullfrogs are
not always available for gartersnake populations that exist where
native ranid frogs have disappeared, and bullfrogs pose a significant
threat to population recruitment of northern Mexican gartersnakes in
many areas. This impact outweighs any benefit of their existence as a
source of prey. We consider relevant data from the common gartersnake
as valid for a general biology discussion as both species have a varied
prey base and both species occupy varied habitats, albeit the northern
Mexican gartersnake may be more aquatic.
Comment 30: In the discussion of the role of harmful nonnative
species relative to other threats implicated in the decline of native
fisheries, the proposed rule stated, ``Aquatic habitat destruction and
modification is often considered a leading cause for the decline in
native fish in the southwestern United States. However, Marsh and Pacey
(2005, p. 60) predict that despite the significant physical alteration
of aquatic habitat in the southwest, native fish species could not only
complete all of their life functions but could flourish in these
altered environments, but for the presence of (harmful) nonnative fish
species, as supported by a `substantial and growing body of evidence
derived from case studies.''
I would like to see a more robust consideration, including
citations beyond March and Pacey (2005), of the importance of the loss
of habitat in native fish declines relative to harmful nonnative
species. It is my understanding that many species of native fish rely
on seasonal flooding to induce spawning.
Our Response: We agree that the role of a natural flood regime is
extremely important to the maintenance of native fish populations as
well as important in (temporarily) depressing resident harmful
nonnative fish populations, and the proposed rule provides a thorough
review of this topic, citing numerous references. Natural flood regimes
have largely disappeared from several large perennial mainstem rivers
and from a small number of streams associated with small reservoirs in
Arizona and New Mexico. However, many native fish are doing markedly
poorly across their ranges where they co-occur with harmful nonnative
fish species, regardless of whether a natural flood
[[Page 38728]]
regime exists or not. No other threat is as geographically ubiquitous
as that from harmful nonnative species, which is clearly reflected, in
robust fashion, within the published literature. The proposed and final
rules review how threats to aquatic habitat that are not directly
associated with nonnative species have also resulted, in part, in the
decline of numerous native fish species in the United States and
Mexico. Based on our consultations with native fish experts in private
and public sectors and the breadth of available literature, the
findings of Marsh and Pacey (2005) are consistent on the scope and
magnitude of the effect of harmful nonnative fish on the decline of
native fish species.
Comment 31: In the discussion of the effects of bullfrogs on
gartersnake populations, the proposed rule states that bullfrogs may
lower recruitment and lead to population declines of northern Mexican
gartersnake populations. This is an over-generalization and is not
supported by scientific data across the range of the species. In
addition, the conclusion that bullfrogs more effectively prey on young
age classes is likely true but has not been substantiated by
experimental studies. This statement does not accurately reflect the
situation in the Verde Valley (AZ), where all age classes of northern
Mexican gartersnakes are well-documented to co-occur with bullfrogs.
Low recruitment could be due to a number of factors other than
nonnative species predation.
Our Response: The scientific community is in consensus, and we
agree, that bullfrogs negatively affect recruitment of northern Mexican
gartersnakes in areas where gartersnakes occur with bullfrogs in high
densities. The presence of other harmful nonnatives or other possible
threats can confound our understanding of the specific effects of
bullfrogs, and we presented an extensive discussion of this issue
citing numerous scientific references. We believe our treatment of the
ecological effects of bullfrogs on northern Mexican gartersnakes is
well supported by the best available scientific information. It is true
that published examples of this concern come from gartersnake
populations in southern Arizona, and we agree that any gartersnake
population could face a unique array of potential threats that could
also effect successful recruitment across its distribution.
Comment 32: Given that northern Mexican gartersnakes have been
documented to prey on bullfrogs in multiple locations, it is misleading
and scientifically inaccurate to imply that the recovery of northern
Mexican gartersnakes is dependent on recovery of native leopard frogs.
Our Response: We agree that bullfrogs in their larval and subadult
age classes can be prey for northern Mexican gartersnakes and, in some
populations, may be their primary prey items. However, unlike native
leopard frogs, bullfrogs in their adult age class become a significant
threat to resident northern Mexican gartersnake populations and can
depress or eliminate recruitment of young snakes into the reproductive
age classes within a population. Adult bullfrogs can extirpate a
population of northern Mexican gartersnakes by directly preying upon
snakes and out-competing them for available prey. Bullfrogs can also
prevent the recolonization of an area by dispersing gartersnakes via
these same ecological mechanisms. The view that bullfrogs are an
adequate substitute for native leopard frogs in the ecosystems of the
northern Mexican gartersnake is not supported by the best available
scientific information and, therefore, we do not support this
supposition.
Comment 33: Regarding the incidence of tail injuries in gartersnake
populations, observations of this phenomenon in upper Oak Creek,
Arizona, at sites where crayfish and bullfrogs are absent, seem to
point to fish or bird predation attempts, given wide oval injury marks
with pointed ends.
Our Response: We noted in the final rule under the heading ``The
Effects of Predation-Related Injuries to Gartersnakes'' that tail
injuries could be caused by other predators other than strictly
bullfrogs or crayfish.
Comment 34: A more quantitative evaluation on habitat loss to
dewatering would be worth sharing, assuming any is available. Extensive
dry reaches in the San Francisco River now exist, including locations
that have historic records for the narrow-headed gartersnake.
Our Response: We agree that a quantitative evaluation of dewatered
stream habitat would be important to fully characterize this threat.
However, we were unable to locate georeferenced data to assist in this
effort and had to rely on existing literature to describe this threat.
Comment 35: The adverse effects of crayfish on narrow-headed
gartersnakes may be overstated, at least with respect to New Mexico. A
clear connection between crayfish presence and declining narrow-headed
gartersnake populations has yet to be definitely made in field study.
The two sites with the highest apparent densities of narrow-headed
gartersnakes in New Mexico also have fairly abundant crayfish and
bullfrogs. When small- to medium-sized native fish are abundant,
crayfish seem to be tolerated by the gartersnakes. In New Mexico very
few sites have crayfish that can reach sizes where they would be a
potential predator on narrow-headed gartersnakes; in virtually all
other sites, the crayfish are uniformly small in size due to periodic
years with flooding that extirpates them or drastically lowers their
numbers.
Our Response: We added discussion under ``Effects of Crayfish on
Native Aquatic Communities'' to reflect extraneous influences on the
threat of crayfish to gartersnake populations while noting that the
available literature strongly suggests that crayfish in larger size
classes or in high densities are cause for significant concern for
gartersnakes and their prey species, especially with other threats
simultaneously affecting gartersnake populations.
Comment 36: The Middle Fork Gila River, Little Creek, and South
Fork Negrito Creek populations of narrow-headed gartersnakes were
identified as likely having been impacted by the 2012 Whitewater-Baldy
Complex fire and considered as not likely viable. Post-fire condition
data were largely not available in 2012, but information from 2013
indicated that fish populations were showing signs of recovery.
Our Response: Based on the potentially significant effects of
wildfire on fish populations and, therefore, on the narrow-headed
gartersnake (detailed in the proposed and final rules), we
conservatively assessed these narrow-headed gartersnake populations as
likely not viable, given the size and scope of the Whitewater-Baldy
Complex Fire. We were also involved with narrow-headed gartersnake
salvage operations from the Middle Fork Gila River, strictly because it
was assessed to have been heavily impacted by wildfire. We treat
Appendix A as a ``living'' document and can update the status of
gartersnake populations as necessary and as population data become
available, for sharing and conservation and recovery planning purposes.
Comment 37: Narrow-headed gartersnakes in the mainstem San
Francisco River are reliably detected, and the population should be
considered as likely viable.
Our Response: Gartersnake captures per unit effort have
significantly declined in the San Francisco River since they first
became regularly monitored in the 1980's. While individuals are still
detected,
[[Page 38729]]
population data we present in Appendix A clearly describe the narrow-
headed gartersnake population in the San Francisco River as one in
significant decline.
Federal Agency Comments
Comment 38: The proposed rule references the Management Indicator
Species, Regional Foresters' Sensitive Species List, and land
management decisions, but states that there are no specific protective
measures conveyed to these species. However, the northern Mexican and
the narrow-headed gartersnakes have been considered sensitive species
on the Regional Forester's sensitive species list for a long time. An
impact to these species is, therefore, considered as part of the
environmental analysis for every forest management action. The USFS
Sensitive Species Policy is to manage for viable populations of these
species. Further, the USFS policy for sensitive species provides
protective measures such as direction to ``Avoid or minimize impacts to
species whose viability has been identified as a concern'' (Forest
Service Manual (FSM) 2670.32 3). A decision that would impact
sensitive species ``. . . must not result in loss of species viability
or create significant trends toward Federal listing'' (FSM 2670.32
4).
Our Response: We more accurately summarized what protections are
afforded to ``sensitive species'' in the final rule. We found no
examples (although we did not have the opportunity to review all
previous planning documents the USFS has developed in the past), and we
were not provided any examples of measures that have been implemented
by the USFS to ``avoid or minimize impacts'' to either the northern
Mexican or narrow-headed gartersnake. We look forward to working with
the USFS in developing such measures.
Comment 39: What is the basis for assuming there is ``continued
anxiety'' from the public regarding rotenone use?
Our Response: We have been an active participant in the public
debate over potential threats to human health from rotenone use. The
new and very process-rich procedures now in place for planning and
implementing rotenone use in Arizona are testament that piscicide use
in the recovery of rare and listed fish is still considered
controversial; although it is scientifically well-supported that there
is no public harm from its use.
Comment 40: We disagree that, on the Gila National Forest, heavy
recreation use within occupied narrow-headed gartersnake habitat is
thought to impact populations along the Middle Fork Gila River,
mainstem Gila River between Cliff Dwellings and Little Creek, and
Whitewater Creek from Catwalk to Glenwood. Recreation use along the
Middle Fork Gila River is certainly not heavy; most use is by hikers
and backpackers utilizing the existing trail to access the Gila
Wilderness. The stream between the Cliff Dwellings and Little Creek is
the West Fork Gila River not the mainstem. This reach of stream is
located on National Park Service, NMDGF, and USFS lands. The majority
of this reach is on the NMDGF's Heart Bar Wildlife Area. Whitewater
Creek from the Catwalk to Glenwood is predominately private property.
Approximately 0.25 mile of stream, downstream of the Catwalk, is USFS
lands and the remainder of this reach is private property.
Our Response: We amended this discussion in the final rule to state
that much of the recreation use in these areas is related to hiking and
backpacking, which are generally not considered a threat to
gartersnakes outside of the fact that increased human visitation leads
to more gartersnake encounters and potentially more killing of
gartersnakes where the foot trail is near the canyon bottom.
Comment 41: Throughout the proposed rule and during personal
communications with the Service, livestock grazing has not been
identified as a significant threat to these species. However, the
Service appears to be saying that, unless livestock are excluded by
fencing, adverse effects may occur. The Service goes further by stating
that the adverse effects of livestock are somehow most likely to occur
when nonnative species are present but that the species are resilient
to these disturbances if nonnatives are absent. So, grazing along a
stream adversely affects the species if nonnatives are present but does
not have these same impacts if nonnatives are absent?
Our Response: We continue to believe that livestock grazing is
largely compatible with northern Mexican and narrow-headed gartersnakes
based on the species' apparent resiliency to perturbations to their
physical habitat, depending on the resident aquatic community. In our
literature review and field experience, we found populations of these
gartersnakes to be resilient to activities that affect their physical
habitat (vegetation abundance, structure, composition) when harmful
nonnative species are absent or at low levels that allow for effective
recruitment of snakes in the population. When recruitment of
gartersnakes within a population is hampered by harmful nonnatives,
this resiliency is diminished and the presence of adequate vegetation
cover for protection against these nonnatives becomes more important.
When Federal actions are planned, all aspects of project evaluations
should consider potential effects to whatever prey base the gartersnake
population is using in a given area. This idea should be the logical
``framework'' used in developing projects in gartersnake habitat to
manage aggressively against harmful nonnatives to improve population
resiliency and recruitment of gartersnakes. We also note that ``adverse
effects'' can have varying degrees of magnitude and scope and that,
through section 7 of the Act, most activities that could adversely
affect species include measures to reduce effects and potential for
take though the issuance of an incidental take permit.
Comment 42: While nonnative, spiny-rayed fish such as green sunfish
and smallmouth bass were common in the lower reach of Turkey Creek near
its confluence with the mainstem Gila River prior to the Dry Lakes
Fire, they did not make up the majority of the fish community. More
upstream reaches were occupied by native fishes including Gila chub,
speckled dace, Sonora and desert suckers, and longfin dace along with
Gila X Rainbow trout hybrids. All of the native species survived the
fire runoff events, and, although populations were depressed for some
time, they had recovered well until recent fires.
Our Response: We amended this discussion in the final rule to more
accurately describe the fish community and effects of wildfire on
Turkey Creek.
Comment 43: We disagree that significant threats to these
gartersnakes, such as those related to nonnative species, are not
addressed on USFS lands. The role of the USFS is to manage land,
addressing the needs of species' habitat. Management actions related to
nonnative fish and aquatic species stocking, control, or eradication is
under direction of the State. Collaborative efforts are occurring on
USFS lands to improve species' habitat through construction of fish
barriers and stream chemical renovations.
Our Response: We acknowledge the proactive measures taken by the
USFS to assist in restoring fish communities to wholly native
assemblages.
Comment 44: The proposed rule states that USFS management policies
of the past favored fire suppression. However, new policies have
allowed for managing wildfires that have a resource benefit, as well as
prescribed fire. The Guidance
[[Page 38730]]
for Implementation of Federal Wildland Fire Management Policy is the
Department of Agriculture's single cohesive Federal fire policy. This
policy contributes to landscape restoration, controls invasive species,
reduces uncharacteristic wildfire across the broader landscape, and
improves the resiliency of these potential natural vegetation types to
adapt to climate change.
Our Response: We have updated this discussion under the heading,
``High-Intensity Wildfires and Sedimentation of Aquatic Habitat'' in
the final rule to include reference to the updated fire policy and what
it hopes to achieve in the mid to long term.
Comment 45: The proposed rule states that the 2011 Wallow Fire
impacted 97 percent of perennial streams in the Black River subbasin
and 70 percent of perennial streams in the Gila River subbasin. We
request the Service clarify how they are defining a subbasin.
Typically, a subbasin is a fourth code Hydrologic Unit. We do not
consider the Wallow Fire to have affected any of the Gila River
subbasins in New Mexico.
Our Response: We use the term subbasin in a general sense as a
stream basin within a larger stream basin. We further defined the area
impacted by the 2011 Wallow Fire as within Apache-Sitgreaves National
Forest, White Mountain Apache Indian Tribe, and San Carlos Apache
Indian Reservation lands in Apache, Navajo, Graham, and Greenlee
counties in Arizona, as well as Catron County, New Mexico. We recommend
the review of InciWeb (2011), Meyer (2011; p. 3, Table 1), and Coleman
(2011, pp. 2-3) for information on the effects of the 2011 Wallow Fire.
Comment 46: On the Apache-Sitgreaves National Forest forested
vegetation types, historic fire-return intervals varied from frequent,
low-intensity surface fires in ponderosa pine types (every 2-17 years),
to mixed-severity fires in wet mixed-conifer forests (every 35-50
years), to high-severity, stand-replacement fires of the spruce-fir
ecosystems (every 150-400 years).
Our Response: We included these fire-return interval data under the
heading, ``High-Intensity Wildfires and Sedimentation of Aquatic
Habitat'' in the final rule.
Comments From States
Comment 47: The AGFD recognizes that both species have declined
considerably throughout their respective ranges in Arizona, and
acknowledge that listing under the Act is warranted. We also applaud
the Service's decision to propose a 4(d) rule that would exempt take of
northern Mexican gartersnakes as a result of livestock use at or
maintenance of livestock tanks located on non-federal lands. We also
encourage the Service to continue to work closely with the AGFD to
effect meaningful conservation actions for both species.
Our Response: We agree, and we look forward to continued
coordination with the AGFD in addressing the most serious threats that
affect either species and to exploring opportunities for recovery with
Federal, State, and local partners and stakeholders.
Comment 48: The statement that ``The decline of the northern
Mexican gartersnake is primarily the result of predation by and
competition with harmful nonnative species . . .'' should be modified
to reflect that this is a leading theory, but not necessarily true.
Our Response: We think that harmful nonnative species (bullfrogs,
crayfish, and warm-water, predatory fish) are the primary driving
factors behind the decline of the northern Mexican and narrow-headed
gartersnake. In the proposed and final rules to list these
gartersnakes, we reviewed the best available scientific and commercial
information to reach this conclusion. We do acknowledge that other
threats such as climate change-induced drought, dewatering of habitat,
large-scale wildfires, and others may have also significantly
contributed to the decline of these gartersnakes, often in synergistic
fashion with other threats affecting primary prey species. We also
acknowledge that some populations of northern Mexican gartersnakes in
particular, have persisted in the presence of harmful nonnative species
to which further study is under way. However, these ecological
situations are rare within the distribution of these gartersnakes, as
evidenced by widespread population declines, and they should not be
construed as evidence that either gartersnake is ecologically
compatible with harmful nonnative species in the long term. Rather, the
scientific information is convincing that harmful nonnative species are
largely responsible for the declines in these gartersnakes.
Comment 49: Reducing the status of the species at each historical
locality as either ``likely viable,'' ``likely not viable,'' or
``likely extirpated'' as described in tables 1 and 2 may not accurately
capture the status of gartersnake populations. Perhaps an ``Unknown''
category would have been useful. Also, a low-density population does
not always indicate that the population is not viable.
Our Response: We agree that adequately describing the status of
each population at each historic locality as falling into one of three
categories is challenging. However, the general lack of data on many
populations does not allow us to refine these categories further. In
most cases, we have more information on the presence of threats at each
locality than good information on the resident gartersnake population.
It was our interpretation that, in the presence of known, and in some
cases severe, threats that a low-density population is, at a minimum,
at risk of losing viability, most notably from effects to reproduction
and recruitment such as in the presence of harmful nonnative species.
Additionally, the process of designating critical habitat requires
us to create a rule set for determining whether the species is present
or not in each historic locality, therefore, a category called
``Unknown'' is not appropriate. Appendix A provides background
information that contributed to our site-by-site determinations of
population status.
Comment 50: We caution against using percentages to express
possible population extirpations or shifts to low densities because
unrealistic expectations of recovery can be established.
Our Response: We use percentages in this listing rule and others to
capture the rangewide context of the status of a given species'
populations to allow the public a coarse, quantitative assessment of
the perceived status of a species, given the best available scientific
and commercial data.
Comment 51: We suggest removing the word ``harmful'' when referring
to the suite of nonnative species that have been identified as the most
incompatible with the gartersnakes. While they may be incompatible,
they are not harmful in a general context.
Our Response: We use the adjective ``harmful'' to distinguish those
nonnative species that pose unique ecological risks to sustaining wild
populations of northern Mexican and narrow-headed gartersnakes and
their prey species. We consider bullfrogs, crayfish, and warm-water,
predatory sport fish as ``harmful nonnative species.'' This distinction
is based on the predatory, or otherwise, notably adverse interactions
these species have with the gartersnakes and their prey. This
distinction is important because not all nonnative species are
completely incompatible with gartersnakes, and some are used as prey
for wild gartersnake populations; nonnative trout are an example.
[[Page 38731]]
Comment 52: There are no direct data to prove that declines in
native leopard frogs have contributed to declines in northern Mexican
gartersnake populations. The Service should caveat the statement with a
degree of uncertainty.
Our Response: We specifically used the word ``contributed'' to
acknowledge that leopard frog declines are a contributing factor to
northern Mexican gartersnake declines, not the sole factor. As noted by
the AGFD, leopard frogs are an extremely important component to the
northern Mexican gartersnake's prey base--a fact also accepted within
the scientific community and demonstrated in field study.
Comment 53: Potential risks to gartersnake populations from
fisheries management activities were mischaracterized in the proposed
rule. Potential effects to gartersnakes are evaluated by the AGFD
though an Environmental Assessment Checklist process.
Our Response: In our evaluation of how fisheries management
activities could adversely affect gartersnake populations, we reviewed
procedures specific to fisheries management as provided in adopted
protocols. The Environmental Assessment Checklist process is a
parallel, internal process implemented by the AGFD in planning
exercises that applies to multiple types of management activities
considered by the State. We have added discussion of this process to
the final rule under the heading ``Risks to Gartersnakes from Fisheries
Management Activities'' and appreciate that potential effects to these
gartersnakes (or any nontarget species) are fully evaluated prior to
implementing any activity within occupied or designated critical
habitat for the gartersnakes.
Comment 54: In Arizona, the trapping and subsequent use of baitfish
in angling is generally constrained to areas where sport fish and sport
fishing dominate, and, therefore, there is little chance the activity
would affect gartersnakes. In addition, regulations specify that bait
fish must be used at the point of capture and not transported elsewhere
for use.
Our Response: We agree that, where angling activities are
concentrated, it is likely due to the presence of sport fish and in the
case where warm-water, predatory fish species are present, it is less
likely that northern Mexican or narrow-headed gartersnakes are
immediately present. However, there are a few areas where angling is
concentrated in habitat that could be occupied by either or both
gartersnake species such as Oak Creek, the Verde River, Tonto Creek, or
Parker Canyon Lake in Arizona where it is possible that effects to
resident gartersnakes could occur. Regardless, we included a statement
in this final listing rule that notes that AGFD requires that baitfish
must be used where they are captured and appreciate being notified of
the regulation and its benefits for gartersnake conservation.
Comment 55: Please elaborate on what is meant by the statement in
reference to the rate of Lake Roosevelt water level fluctuation as a
benefit to harmful nonnative fish species. Reservoir levels there
fluctuate substantially.
Our Response: We agree that water levels in Lake Roosevelt do
fluctuate and further qualified the statement on this issue in the
final rule. We intended to frame this discussion for comparative
purposes. That is to say, that compared to Horseshoe Reservoir, which
is managed to minimize reproduction of harmful nonnative species in
most years, Lake Roosevelt has several times the capacity of Horseshoe
Reservoir and fluctuation in water levels occur at a slower rate. The
rate at which water levels decline in these reservoir systems affects
the reproduction and recruitment of harmful nonnative fish species; the
faster the decline, the more negative the effect.
Comment 56: It is not clear how ``build-out'' (in reference to
human population growth and urban development) will affect Redrock
Canyon (in the vicinity of Patagonia, Arizona).
Our Response: The discussion in the proposed and final rules where
the issue of build-out is addressed refers to the long-term development
plan along the major transportation corridors of I-19, I-10, and I-17
in Arizona. We identified extant gartersnake populations that were
geographically proximal to these proposed corridors which could
experience indirect effects of development and growth in the human
population (which is expected to double by 2030). Redrock Canyon is
near the Town of Patagonia, which is near Nogales and the I-19
corridor. If predictions for development and human population growth in
Arizona are accurate, we expect increased development in the Patagonia
area, higher levels of human recreation on public lands, and possible
effects to water availability as a result of increased regional
groundwater pumping or additional diversions. We acknowledge in the
final rule that, of the areas identified where there could be effects
to gartersnake populations, Redrock Canyon is buffered geographically
more so than other areas identified.
Comment 57: The section of the proposed rule that discusses the
Arizona Department of Water Resources Active Management Areas (AMAs)
overstates the significance of the AMA designation for both gartersnake
species. For example, the Phoenix AMA includes no modern records of
either species and will not affect long-term recovery. In another
example, the Pima AMA includes only short stretches of the Gila River;
the rest of the AMA is outside the range of either gartersnake's
distribution.
Our Response: In our evaluation of the effect of groundwater
pumping on gartersnake habitat, we found several references that
discuss the known hydrological connection between groundwater and
surface flow in southwestern streams. This is an established concept in
the scientific community and the basis for widespread public concern in
several areas of Arizona with respect to surface flows including the
Verde and San Pedro Rivers. We explained how overdrafts in groundwater
use exceed aquifer recharge (conditions that result in an AMA
designation) and result in a cone of depression that can reduce or
eliminate surface flows in affected streams. We listed the AMAs that
both overlap with the historical range of either gartersnake and
provide context for the discussion of effects of increasing human
population growth on gartersnake populations through indirect effects
of groundwater demands. In doing so, we accurately captured the links
in this cause and effect relationship. With respect to the Phoenix AMA,
we acknowledge that effects on gartersnake populations are no longer
occurring. However, it was our intent to discuss the causes of
historical population extirpations, which were a precursor to rangewide
declines observed today. Effects of the development of the greater
Phoenix metropolitan area include effects from increasing regional
demands on groundwater. Aquifer overdrafts were likely contributing
factors in the extirpation of northern Mexican gartersnake populations
in the lower Salt, lower Gila, and lower Agua Fria River systems.
Comment 58: No scientific evidence has been produced that confirms
a relationship between livestock grazing in occupied gartersnake
habitat in the presence of harmful nonnative species and that without
their presence.
Our Response: We concur that no specific scientific study has been
afforded to this specific issue with
[[Page 38732]]
respect to either the northern Mexican gartersnake or the narrow-headed
gartersnake. However, we have documented observations made of
gartersnake populations in Mexico in the presence of harmful nonnative
species, as well as in their absence, in habitat heavily affected by
other land uses such as unmanaged livestock grazing. As discussed at
length in the subsection below entitled ``The Relationship between
Harmful Nonnative Species and Adverse Effects to Physical Habitat,'' we
found a unique opportunity in Mexico to observe populations in habitat
significantly compromised by land use activities such as unmanaged
livestock grazing where the aquatic community was considered wholly
native. Opportunities to observe this scenario in the United States
generally do not occur due to applied grazing management prescriptions
that largely prohibit extreme effects to riparian habitat, and the fact
that harmful nonnative species are largely ubiquitous in habitat
occupied by these gartersnakes in the United States. Species experts
involved in the Mexico survey effort were in consensus that the most
significant predictor of gartersnake occupancy in these affected
habitats was the presence or absence of harmful nonnative species. The
fact that gartersnakes will use vegetative cover to hide from harmful
nonnative species, and the fact that, in the United States, gartersnake
populations that currently persist at seemingly adequate densities in
the presence of harmful nonnatives also occur in habitat with adequate
vegetative cover, provides further support of this relationship. The
best available scientific and commercial data, coupled with the opinion
of species experts, suggests this relationship is most likely real, and
we fully endorse further scientific study of this issue, if that
opportunity exists.
Comment 59: In Mexico, the Mexican gartersnake is listed as
threatened throughout its range in that country and at the species
level of its taxonomy. The discussion of the threatened status of
northern Mexican gartersnake, as it applies to this rulemaking, is,
therefore, misleading given that there are currently 10 subspecies, and
the northern Mexican gartersnake in Mexico occurs in some of the least
accessible and least likely disturbed aquatic habitats in the country.
Our Response: In Mexico, the clear majority of the distribution of
the Mexican gartersnake (T. eques) is composed of the northern Mexican
gartersnake (T. e. megalops). The Mexican gartersnake (T. e. eques)
comprises the second highest percentage of the species' distribution
along the southwestern quadrant of the species' distribution in Mexico
(Rossman et al. 1996, p. 173). The remaining eight subspecies have much
smaller distributions and in some cases are highly endemic; constrained
to perhaps a single lake. In our analysis of the status of northern
Mexican gartersnake in Mexico, we made every attempt to analyze only
those threats that geographically overlap our understanding of the
subspecies' distribution, which supports the position of a weakened
status, commensurate with Mexico's listing. We do not disagree that
there are likely habitats within its distribution in Mexico that remain
largely intact, physically and ecologically. We also note that harmful
nonnative species, once introduced into a system, have an ecological
advantage over native species and will expand their distribution and,
therefore, the scope of their effects on the landscape, much like what
has been observed in Arizona for decades. This fact, and the
preponderance of scientific and commercial data we evaluated that
pertained to threats in Mexico, supports the position taken by the
Mexican Government in listing the Mexican gartersnake (T. eques) as
threatened and is largely applicable to the northern Mexican
gartersnake.
Comment 60: We recommend removing the discussion referring to the
fact that many of the recovery projects for the Chiricahua leopard frog
have not provided direct benefits to the northern Mexican gartersnake.
The Service does not provide citations for their statement that
indirect benefits for both gartersnake species occur through recovery
actions designed for their prey species, and since the Chiricahua
leopard frog was listed under the Act, significant strides have been
made in its recovery and the mitigation of its known threats.
Our Response: In assessing how recovery activities for currently
listed species may benefit either gartersnake, it is important to
discuss both the benefits and limitations of these activities on
conserving or recovering nontarget species such as the northern Mexican
gartersnake. We used reasonable principles in conservation biology in
making the basic assertion that either gartersnake may benefit by
recovery activities implemented for their native prey species, such as
the Chiricahua leopard frog. For example, when harmful nonnative
species removal projects are implemented on regional scales, such as
for bullfrogs, the predation and competition pressure on gartersnake
prey species are reduced, which may lead to significant expansions in
prey species distribution or increases in their biomass or population
densities. This activity benefits the gartersnakes that use these prey
communities. In another example, the construction of a fish barrier to
prevent the upstream migration of harmful nonnative fish into a stream
provides direct benefits to the resident gartersnake population by
reducing predation pressure on the gartersnakes and their prey base. As
for the recovery achievements made for the Chiricahua leopard frog, we
agree that, in some areas, these activities have benefited the
gartersnakes, particularly for the northern Mexican gartersnake where
they have occurred in lentic habitat on landscape scales, and
specifically in southern Arizona. However, many recovery actions
specific to the Chiricahua leopard frog have occurred at specific tanks
higher in the watershed, not within the floodplain of larger perennial
stream systems, where they would yield much more significant benefits
to gartersnake populations.
Comment 61: Maintaining nonnative sport fish populations does not
necessarily ``significantly reduce the potential for the conservation
and recovery on northern Mexican and narrow-headed gartersnakes.'' The
Biological and Conference Opinion issued by the Service that addresses
the AGFD's 10-year sport fish stocking program (``sport fish
consultation'') includes mitigation measures to ``address the effects
of the proposed action and improve the baseline conditions for native
aquatic species.''
Our Response: We agree that maintaining nonnative sport fish
populations in some areas may have little effect or may even benefit
some gartersnake populations. Not all nonnative species have the same
ecological effect on native aquatic communities. For this reason, and
for the purposes of the greater listing analysis afforded to these two
gartersnakes in this rulemaking, we specifically use the phrase
``harmful nonnative species'' when discussing those which significantly
threaten the northern Mexican or narrow-headed gartersnake. As
previously stated, we consider harmful nonnative species to include
bullfrogs, crayfish, and warm-water, predatory fish. The majority of
specific stocking activities that were subject to the sport fish
consultation involved primarily salmonids (i.e., trout), which we do
not consider to be particularly harmful to these gartersnakes or many
of their prey species. For example, in some areas,
[[Page 38733]]
nonnative trout are an important component to the narrow-headed
gartersnake prey base. Stocking activities under the sport fish
consultation that involved harmful nonnative species were few, were
constrained to lentic habitat (lakes, ponds, etc.), and were a
significant factor behind the ``likely to adversely affect''
determination made for these gartersnakes and several of their prey
species.
Comment 62: In the discussion regarding potential ramifications for
gartersnake recovery with respect to watershed-level fisheries
management designations, the conclusions that were drawn seem
premature. Not all nonnative fishes are considered as, or managed as,
sport fish in Arizona, including many of the nonnative fishes that are
problematic for gartersnakes.
Our Response: Our intention was not to predict which watersheds or
particular streams would likely be designated as nonnative sport
fisheries in the future. Rather, we simply acknowledged that surface
water is generally scarce in the arid Southwest and large perennial
streams, even more so. We assume that some streams currently occupied
by the gartersnakes are likely to be designated for nonnative fisheries
because of the scarcity of these aquatic systems in Arizona, the
existing access infrastructure, and the fish communities that currently
reside in larger perennial streams. We are concerned that if large,
perennial streams, which are important occupied habitat for northern
Mexican and narrow-headed gartersnakes (as well as their prey species),
are designated as nonnative sport fisheries in the future, they will be
lost to the gartersnakes, which would negatively affect their recovery
rangewide. Furthermore, we have a high degree of certainty that if any
habitat occupied by either gartersnake is designated strictly as a
nonnative fishery (that includes warm-water, predatory species), that
habitat will no longer possess the values that are important (or
imperative) for species recovery and the value of these areas for
recovery will be largely eliminated. Regarding nonnative species that
are problematic to gartersnakes and which are not considered sport fish
by the AGFD, we look forward to partnering with the AGFD and other
public and private stakeholders in the removal of these species where
they occur, and view this and similar recovery actions as the highest
priority.
Comment 63: The proposed rule discussed at length the issue of
declining native fishes and degradation of aquatic systems in Mexico
but did so without discussing the status of the northern Mexican
gartersnake. This type of argument is an apparent effort to build the
case for listing the subspecies throughout its range based on inferred
effects of the decline of native fish communities and habitat
degradation, despite the fact that clear data for the northern Mexican
gartersnake decline are only available for Arizona and New Mexico.
Our Response: We do not have population studies of northern Mexican
gartersnakes in Mexico. However, we have used the best scientific and
commercial data available. The information shows the status of native
aquatic vertebrates in habitat currently or formerly occupied by the
northern Mexican gartersnake generally correlate to the status of
northern Mexican gartersnakes. We cited examples of how aquatic
ecosystems are adversely affected by leading threats, such as
dewatering or the expansion of harmful nonnative species, can affect
the northern Mexican gartersnake and its native prey species, such as
fish. Native fish comprise an important prey source for northern
Mexican gartersnakes. Gartersnakes need them for nutrition in order to
carry out their life-history functions. We found a significant amount
of information that concluded that native fish communities were
significantly at risk, as documented by declines of many species in
several subbasins across the distribution of the northern Mexican
gartersnake in Mexico. Therefore, when a major source of prey for
northern Mexican gartersnakes becomes rare or disappears entirely, the
gartersnake population will be negatively affected through declines in
the fitness of individuals associated with poor nutrition, stress, and
starvation. Several different factors that are contributing to the
decline in native fish communities include harmful nonnative species,
dewatering of habitat, and pollution of habitat. These stressors also
negatively affect northern Mexican gartersnake populations both
directly and indirectly. Native fish are, therefore, an effective
surrogate for use in determining how threats are acting on individual
northern Mexican gartersnakes and their populations throughout their
distribution in Mexico.
Comment 64: We caution against extrapolation, such as the statement
that there has been a 17-fold increase (since 1961) in the number of
native fish species in Mexico that have been listed by the Mexican
Federal Government as either endangered, facing extinction, under
special protection, or likely extinct. The data cited do not speak to
the status of these native fish species rangewide.
Our Response: We cited references that discuss the status of native
fish in Mexico in our discussion of the status of the northern Mexican
gartersnake in Mexico, and we did not imply those trends represented
their status rangewide.
Comment 65: The Service identified a number of streams or aquatic
communities in Mexico that have been adversely affected by threats such
as declining native fisheries, sedimentation from logging, pollution,
etc. Yet, our observations often point to the inverse in several
headwaters of these identified streams. In other examples, such as the
R[iacute]o Colorado in Sonora, the vicinity of Mexico City, or unnamed
streams draining the Sierra Madre, evidence that these areas were
occupied by the northern Mexican gartersnake or occur within its
distribution was not clearly presented.
Our Response: Much like what has been observed and documented in
the southwestern United States, headwater streams are often less
impacted than the mainstem rivers they feed. This is often because of
the remote nature of these headwaters, which can limit the effect of
human-caused threats (watershed-scale effects increase in the
downstream direction), as well as the presence of natural or man-made
barriers that prevent upstream migration of harmful nonnative species.
Therefore, it may not be appropriate to infer that, simply because a
headwater system is intact, that the same holds true for the system
lower in the watershed. With respect to whether streams identified as
being impacted by various threats in Mexico are within the distribution
of the northern Mexican gartersnake, the references cited were not
presented at a geographic scale fine enough to definitively conclude
that a complete overlap with the distribution of the northern Mexican
gartersnake exists, but rather a portion of the stream overlaps. In
addition, a number of the streams that were called into question by the
AGFD occur at the periphery of the subspecies' range in Mexico, which
is still not precisely understood by the scientific community.
Therefore, we presented the data in a regional context, as evidence
that such threats could affect the gartersnake where they overlap.
Regarding whether the northern Mexican gartersnake ever existed in
the R[iacute]o Colorado in Sonora, there are two verified records from
the Colorado River at Yuma from 1889 and 1890. We assume the species
also occurred downstream into Mexico where suitable
[[Page 38734]]
habitat historically existed. We also presented data on threats to
aquatic habitat in the vicinity of Mexico City. While we agree that
this area represents the extreme southern end of the subspecies'
distribution, we also acknowledge that threats, particularly harmful
nonnative species, can have a larger geographic impact over time.
Lastly, we presented information that suggested that threats may be
affecting streams that drain the Sierra Madre, which in some cases were
not specifically identified by the principal investigators. Considering
that the Sierra Madre represents a large portion of the northern
Mexican gartersnakes' distribution in Mexico, it was appropriate to
include these data in our evaluation in a conservative assumption that
many, if not most, of the streams were historically or currently
occupied by this subspecies.
Comment 66: The New Mexico Department of Game and Fish encourages
an expansion of activities authorized under a special rule under
section 4(d) of the Act to exempt landowners from prohibitions of take
under section 9 of the Act, for those actions that benefit the two
gartersnakes, such as: (1) Enhancement and restoration of native
riparian vegetation and stream structure; (2) control of harmful
nonnative species, such as American bullfrogs and crayfish; (3)
intensive research into the biology of the two species of gartersnake;
and (4) continuing research into captive rearing and repatriation of
the northern Mexican and narrow-headed gartersnakes.
Our Response: We agree that section 4(d) of the Act can provide
important conservation potential in the recovery of these two
gartersnakes, and we appreciate the New Mexico Department of Game and
Fish's willingness to explore such opportunities. We have included a
section 4(d) rule for the northern Mexican gartersnake in this
rulemaking, which addresses the management of livestock tanks on non-
Federal lands. Of the four special rule possibilities offered by the
New Mexico Department of Game and Fish, controlling (removing) harmful
nonnative species is most likely to provide the highest conservation
benefit for northern Mexican and narrow-headed gartersnakes, and we are
interested in looking further into this issue with our cooperators and
stakeholders, such as the New Mexico Department of Game and Fish. In
order to be most effective, such a 4(d) rule would have to be developed
in close coordination with affected agencies, explicitly authorize the
removal of bullfrogs, crayfish, and predatory fish species, and include
precautions to minimize potential harm to affected gartersnake
populations during project implementation. However, at this time, we do
not have sufficient information to allow us to adequately confirm
whether such a 4(d) rule would be necessary and advisable for the
conservation of the species. We can consider such a rule in the future.
Permitting authority for research needs is addressed through the
issuance of section 10(a)(1)(A) permits. With respect to the
enhancement and restoration of native riparian vegetation and stream
structure, where water occurs, the vegetative structure is not viewed
as limiting for gartersnake occupation in most cases. Where water has
been removed from streams by dams, diversions, or groundwater pumping,
correcting these scenarios and returning water to the system would be
construed as a beneficial effect. For any activity not explicitly
addressed in our proposed 4(d) rule that would result in take of either
gartersnake, a section 10 permit would be required to avoid a violation
of section 9 of the Act.
Tribes
Comment 67: In discussing the potential impacts of dams and
reservoirs on resident fish communities, the proposed rule identifies
the San Carlos Reservoir as an example of a reservoir that benefits
harmful nonnative species and, therefore, negatively affects the
northern Mexican and narrow-headed gartersnakes. This statement should
be omitted from the final rule for two reasons. First, the proposed
rule makes this conclusory adverse effect determination without any
support whatsoever. Second, this conclusory determination is
unnecessary to establish that the northern Mexican gartersnake or the
narrow-headed gartersnake should be designated as threatened. In 1924,
Congress enacted the San Carlos Project Act, which authorized the
construction of the Coolidge Dam and the creation of the San Carlos
Reservoir ``for the purpose . . . of providing water for the irrigation
of lands allotted to the Pima Indians on the Gila River Reservation,
Arizona.'' A statement in the proposed rule that the San Carlos
Reservoir adversely affects northern Mexican and narrow-headed
gartersnakes could affect the federally mandated delivery of water to
the Gila River Indian Community. Any impediment to the Gila River
Indian Community's irrigation system threatens the Gila River Indian
Community's agriculture, economy, and most importantly, the survival of
its culture, the value of which is immeasurable.
Our Response: In the final rule, we deleted the reference to the
San Carlos Reservoir as an example of a reservoir within the range of
the gartersnakes that may be benefitting harmful nonnative species,
because there are several other examples. USFWS (2008, pp. 112-131)
provides a complete scientific analysis of the relationship of
reservoirs to resident aquatic communities upstream and downstream,
includes many scientific references that have been incorporated by
reference in this final rule, and comprises the basis for the issuance
of a section 10(a)(1)(B) incidental take permit for the operation of
Horseshoe and Bartlett Reservoirs, in that case. We believe the same
relationships likely are true at San Carlos Reservoir. We look forward
to work with interested parties to identify solutions that meet water
use interests and the conservation needs of listed species.
Public Comments
General
Comment 68: Threats to the gartersnakes are those caused by Federal
and State fish and wildlife management actions, or on Federal lands
that can be dealt with outside of the Act. Approximately 85 percent of
the habitat for the northern Mexican gartersnake is in Mexico. In
Mexico, any activity that intentionally destroys or adversely modifies
occupied northern Mexican gartersnake habitat is prohibited.
Our Response: As stated in the proposed rule, the Act requires us
to make listing determinations based on the five threat factors, singly
or in combination, as set forth in section 4(a)(1) of the Act. The Act
further requires us to make listing determinations solely on the basis
of the best scientific and commercial data available after taking into
account those efforts, if any, being made by any State or foreign
nation, or any political subdivision of a State or foreign nation, to
protect such species, whether by predator control, protection of
habitat and food supply, or other conservation practices within any
area under its jurisdiction. The Act requires us to give consideration
to species that have been designated as requiring protection from
unrestricted commerce by any foreign nation or pursuant to any
international agreement; or identified as in danger of extinction or
likely to become so within the foreseeable future, by any State agency
or by any agency of a foreign nation that is responsible for the
conservation of fish or wildlife or plants.
[[Page 38735]]
A number of existing regulations potentially address issues
affecting the northern Mexican and narrow-headed gartersnakes and their
habitats. However, existing regulations within the range of northern
Mexican and narrow-headed gartersnakes typically address only the
direct take of individuals without a permit and provide little, if any,
protection of gartersnake habitat. Arizona and New Mexico statutes do
not provide protection of habitat and ecosystems. Legislation in Mexico
prohibits intentional destruction or modification of northern Mexican
gartersnake habitat, but neither that, nor prohibitions of take, appear
to be adequate to address ongoing threats. See ``The Inadequacy of
Existing Regulatory Mechanisms'' in the proposed rule for further
information.
Comment 69: There is more recent data on surface activity of
northern Mexican gartersnakes than Rosen (1991, pp. 308-309). More
recent observations indicate radio-tracked snakes were not surface
active 64 percent of the time at Bubbling Ponds and 60 percent of the
time at Tavasci Marsh (upper Verde River) and the middle Verde River.
Our Response: We have updated the discussion under ``Habitat and
Natural History'' for the northern Mexican gartersnake in this final
rule to reflect more recent information, such as the information
provided in the comment.
Comment 70: The proposed rule states that the northern Mexican
gartersnake appears to be most active during July and August, followed
by June and September. Based on recent survey efforts it would probably
be most accurate to state that the species appears to be most active
between May and September.
Our Response: We have updated the discussion under ``Habitat and
Natural History'' for the northern Mexican gartersnake in this final
rule to reflect more recent information, such as the information
provided in the comment.
Comment 71: The proposed rule so broadly describes the species'
physical habitat that it is difficult to determine what types of
riparian, wetland, and terrestrial habitats are important to each of
the gartersnakes and is conflicting with previous characterizations.
Our Response: The habitat descriptions we provide in the proposed
and final rules reflect the current understanding of the types of
habitat that are used by either gartersnake species. The descriptions
appear broad because these gartersnakes, in particular the northern
Mexican gartersnake, can occur in varied ecological settings.
Comment 72: All five of the waters where there are viable
populations of Mexican gartersnakes are already protected and do not
need further protection under the Act. Oak Creek, Tonto Creek, and the
Upper Verde River are protected by spikedace and loach minnow critical
habitat. The San Rafael Valley is protected by The Nature Conservancy
and San Rafael State Park. The Bill Williams River is a National
Wildlife Refuge.
Our Response: We acknowledged in our proposed rule that other
listed species' historic ranges overlap with the historical
distribution of northern Mexican and narrow-headed gartersnakes.
However, as stated above and in the proposed rule, the Act requires us
to make listing determinations based on the five threat factors, singly
or in combination, after taking into account those efforts being made
by any State or foreign nation to protect such species. Management by
Federal or State agencies, or non-governmental organizations does not
necessarily eliminate activities that threaten these subspecies.
Comment 73: The northern Mexican gartersnake in the United States
is not a distinct population segment and does not require protection
under the Act.
Our Response: We did not propose to list either gartersnake as a
distinct population segment. We proposed to list the northern Mexican
and narrow-headed gartersnakes as threatened throughout their ranges.
We also reviewed the best available scientific and commercial
information to conclude that the northern Mexican gartersnake is a
valid subspecies as defined under the Act.
Comment 74: The Service must follow the guidance of Executive Order
13563 of January 18, 2011, concerning making a new Federal rule.
Our Response: Executive Order (E.O.) 13563 reaffirms the principles
of E.O. 12866 while calling for improvements in the nation's regulatory
system to promote predictability, to reduce uncertainty, and to use the
best, most innovative, and least burdensome tools for achieving
regulatory ends. The executive order directs agencies to consider
regulatory approaches that reduce burdens and maintain flexibility and
freedom of choice for the public where these approaches are relevant,
feasible, and consistent with regulatory objectives. E.O. 13563
emphasizes further that regulations must be based on the best available
science and that the rulemaking process must allow for public
participation and an open exchange of ideas. We have developed this
rule in a manner consistent with these requirements.
Comment 75: These gartersnakes are already protected by the New
Mexico Department of Game and Fish.
Our Response: A number of existing regulations potentially address
issues affecting the northern Mexican and narrow-headed gartersnakes
and their habitats. However, existing regulations within the range of
northern Mexican and narrow-headed gartersnakes typically address only
the direct take of individuals without a permit, and provide little, if
any, protection of gartersnake habitat. Arizona and New Mexico statutes
do not provide protection of habitat and ecosystems. Legislation in
Mexico prohibits intentional destruction or modification of northern
Mexican gartersnake habitat, but neither that legislation, nor
prohibitions of take, completely address ongoing threats. See ``The
Inadequacy of Existing Regulatory Mechanisms'' in this final rule for
further information.
Comment 76: The Strategic Water Reserve, managed by the New Mexico
Interstate Stream Commission, already holds and utilizes water rights
to benefit endangered fish and wildlife species in New Mexico. Since
the Service gives strongest weight to statutes because they are
nondiscretionary and enforceable, the New Mexico Interstate Stream
Commission expects the Service to give weight to the Strategic Water
Reserve statute in this final rule.
Our Response: We considered the Strategic Water Reserve managed by
the New Mexico Interstate Stream Commission and have updated the
discussion in the final rule with this new information. However,
collectively, existing regulations within the range of northern Mexican
and narrow-headed gartersnakes are not fully ameliorating ongoing
threats such that the subspecies would not meet the definition of
threatened. See ``The Inadequacy of Existing Regulatory Mechanisms'' in
this final rule for further information.
Comment 77: Contrary to what is implied in the proposed rule, Clean
Water Act section 404 nationwide permits receive rigorous environmental
review by the Corps.
Our Response: We recognize that the Clean Water Act section 404
nationwide permits receive environmental review by the Corps; however,
this process does not appear to be ameliorating ongoing threats to
northern Mexican or narrow-headed gartersnakes such that the subspecies
would not meet the definition of threatened. See ``The Inadequacy of
Existing Regulatory Mechanisms'' in this final rule for further
information.
Comment 78: What is the problem with the management or resources at
the
[[Page 38736]]
Buenos Aires National Wildlife Refuge (BANWR) that makes populations
likely not viable.
Our Response: The abundance of bullfrogs on the BANWR, specifically
in the vicinity of Arivaca Lake and Arivaca Cienega, contributes to the
northern Mexican gartersnake population being categorized as likely not
viable. As stated in our proposed rule, bullfrogs (and other harmful
nonnatives) are a primary threat to the gartersnakes. The presence of a
single juvenile northern Mexican gartersnake was confirmed on the BANWR
in 2000 (Rosen et al. 2001, Appendix I). The observation of this
juvenile suggests that at least some level of reproduction had occurred
and may still be occurring but more recent survey work has not occurred
there. The presence of dense cover probably helps any remaining
northern Mexican gartersnakes to avoid predation.
In recent years, there has been a concerted management effort on
the BANWR to recover the Chiricahua leopard frog in an array of tanks
and their associated drainages, all of which have been designated as
critical habitat for the Chiricahua leopard frog. As a result, it is
likely that any northern Mexican gartersnakes that successfully
immigrate into the central tanks area of the BANWR have an increased
chance of persistence because of improved available habitat and a
stable prey base in an area that is likely free of nonnative predators.
We also expect that dispersing Chiricahua leopard frogs might help
sustain a low-density population of northern Mexican gartersnakes on
the refuge. We consider the northern Mexican gartersnake to be extant
as a low-density population on the BANWR based on historical and recent
records and the abundance of available, suitable habitat and prey
populations in the vicinity of the most recent record. Appendix A
contains additional details on the status of the northern Mexican
gartersnake at this and other refuges.
Comment 79: What is the relationship of the Arizona Department of
Water Resource laws and the proposed listing of the two gartersnakes?
For New Mexico, the New Mexico State Engineer indicated that any person
in New Mexico can apply to the State Engineer for a permit for the
lease of a valid existing water right to augment or maintain stream
flow for the beneficial use of fish and wildlife habitat, maintenance
or restoration. Further, permits for the permanent transfer of water
rights for such purposes have already been granted to the New Mexico
Interstate Stream Commission. Both the Strategic Water Reserve option
and the leasing option retain a water right's original priority date.
Our Response: Existing water laws in Arizona and New Mexico may not
be fully adequate to protect gartersnake habitat from the dewatering
effects of groundwater withdrawals. New Mexico water law now includes
provisions for instream water rights to protect fish and wildlife and
their habitats. Arizona water law also recognizes such provisions;
however, because this change is relatively recent, instream water
rights have low priority and are often never fulfilled because more
senior diversion rights have priority. With respect to New Mexico, we
have updated the discussion on New Mexico water rights laws in the
final rule to correct any inaccuracies.
Comment 80: The information in Table 1 of the proposed rule does
not match the information on page 41515. Page 41515 states that a
former large, local population of northern Mexican gartersnakes at the
San Bernardino National Wildlife Refuge has experienced correlative
decline of leopard frogs and are now thought to occur at very low
population density or may be extirpated. Table 1 states likely not
viable.
Our Response: We consider gartersnake populations with very low
population densities, and thus at higher risk of extirpation, such as
the one at San Bernardino National Wildlife Refuge, to be likely not
viable. While the population could already be extirpated, we did not
have sufficient information to categorize it as likely extirpated and
so called it likely not viable.
Surveys and Monitoring
Comment 81: The proposed rule states that the northern Mexican
gartersnake has declined significantly in the last 30 years, but then
goes on to state that there are several areas where the species was
known to occur but has received no or very little survey effort in the
past decades.
Our Response: We based our conclusions on the best scientific and
commercial data available at the time of listing. We have concluded
that, in as many as 24 of 29 known localities in the United States (83
percent), the northern Mexican gartersnake population is likely not
viable and may exist at low population densities that could be
threatened with extirpation or may already be extirpated. In most
localities where the species may occur at low population densities,
existing survey data are insufficient to verify extirpation. Only five
populations of northern Mexican gartersnakes in the United States are
considered likely viable.
Comment 82: The Service assumes the populations at Whitewater Creek
and Middle Fork Gila River are likely deteriorated or have been
severely jeopardized after the Whitewater-Baldy Complex Fire, but
subsequent survey data have not been collected. In the absence of
subsequent survey data, the Service lacks information to supports its
assumption that the narrow-headed gartersnake populations have
deteriorated. Further, we understand that some of the northern Mexican
gartersnakes discovered in the Gila National Forest in June 2013 were
found precisely in Whitewater Creek. Among the discovered snakes were
young males and at least one viable reproducing female, suggesting that
the populations of northern Mexican gartersnakes are living and
reproducing in the area. The discovery of a reproducing population of
northern Mexican gartersnakes in this area suggests that populations of
narrow-headed gartersnakes may not be as likely deteriorated as the
Service suggests.
Our Response: The proposed rule states that the status of those
populations has likely deteriorated as a result of subsequent declines
in resident fish communities due to wildfires followed by heavy ash and
sediment flows, resulting fish kills, and the removal of snakes.
Immediately after the Whitewater-Baldy Complex Fire, but before the
subsequent monsoon, we were actively working with other agencies and
species experts on assessing the likely damage to the resident fish
community and planning salvage operations for narrow-headed
gartersnakes. As stated in Appendix A (available at https://www.regulations.gov, Docket No. FWS-R2-ES-2013-0071), populations are
thought to remain extant at Whitewater Creek and Middle Fork Gila
River, but in the short to mid term we anticipate the density of the
narrow-headed gartersnake population to be low due to the Whitewater-
Baldy Complex Fire. These sites may rebound in the mid to long term
when subbasin conditions stabilize and fish begin to recolonize the
stream or are otherwise reintroduced through restoration efforts. See
``High-Intensity Wildfires and Sedimentation of Aquatic Habitat''
section of the final rule for additional information. The best
available scientific and commercial data indicated that high-intensity
wildfires have the potential to eliminate gartersnake populations
through a reduction or loss of their prey base.
Northern Mexican gartersnakes have never been documented in
Whitewater
[[Page 38737]]
Creek, but were rediscovered in the Gila River in 2013.
Comment 83: Haney et al. (2008, p. 61) declared the northern
Mexican gartersnake as nearly lost from the Verde River, but also
suggested that diminished river flow may be an important factor. Given
the multiple recent detections of northern Mexican gartersnakes along
the upper and middle Verde River, this statement does not seem relevant
to include in the proposed rule.
Our Response: More recent population status data for the northern
Mexican gartersnake for the Verde River were preliminary and
unpublished at the time the proposed rule was drafted. These newer data
have been incorporated into the final rule and Appendix A.
Comment 84: Is a consistent survey protocol being followed each
year? Is data collected from different surveys comparable? Without
scientific survey protocol implemented consistently for at least 10
years, there can be no real evidence of population trends.
Our Response: There is currently no accepted protocol for northern
Mexican or narrow-headed gartersnake surveys; however, some
investigators have attempted to revisit locations where others have
surveyed in the past in an attempt to establish population trends.
Variability in survey design and effort makes it difficult to compare
population sizes or trends among sites and between sampling periods.
For each of the sites discussed in Appendix A, we have attempted to
translate and quantify search and capture efforts into comparable units
(i.e., person-search hours and trap-hours) and have conservatively
interpreted those results. Where population trends have been
established, they have been reported and reflect significant declines
in both species.
Comment 85: The Service has failed to survey, analyze data, and
incorporate the effects of the thousands of livestock tanks and other
impoundments that have been constructed in recent times that are now
occupied by the narrow-headed and northern Mexican gartersnakes. These
stock tanks and manmade impoundments offer the best opportunity for
refugia for the narrow-headed and northern Mexican gartersnakes and
could prove to be very important for the future survival of these
gartersnakes, as well as the Chiricahua leopard frog. Given the
quantity of tanks and other impoundments constructed in the last 50
years, the number of these structures that are used by the gartersnakes
could be substantial, and, therefore, the potential population count
for the species could be significantly higher than speculated.
Our Response: Surveys of every stock tank that could occur within
the distribution of both gartersnake species have not been done. The
Act requires that we base our evaluation on the best scientific and
commercial information available. We agree that well-managed stock
tanks represent conservation and recovery opportunities for the
northern Mexican gartersnake and have consequently developed a rule
under section 4(d) of the Act that exempts otherwise unauthorized take
of northern Mexican gartersnakes from livestock use or maintenance of
stock tanks on non-Federal lands. Stock tanks are not considered
suitable habitat for narrow-headed gartersnakes, and the species has
never been reported using a stock tank.
Harmful Nonnative Species and Other Threats
Comment 86: No information is provided describing San Carlos
Reservoir operations and their effects on nonnative and native aquatic
species, whether there are or ever has been gartersnakes in or near the
San Carlos Reservoir and the status of any nonnative fish populations
on the Gila River at San Carlos Reservoir. This is not based on the
best available science.
Our Response: Distribution data strongly suggest that northern
Mexican and narrow-headed gartersnakes historically occurred along the
middle Gila River, as this was formerly a major perennial river with
several known populations both upstream and within numerous
tributaries, with suitable habitat, and a robust native prey base.
Post-construction of the San Carlos Reservoir, survey data are limited.
Thus it remains difficult to ascertain the current status of
gartersnake populations upstream, downstream, or within the reservoir
itself. As far as the effect of the reservoir on the up- or downstream
aquatic community, similar analysis have been performed for the
Horseshoe and Bartlett Reservoirs, which resulted in the issuance of a
section 10(a)(1)(B) permit for the incidental take of native fish
species, the lowland leopard frog, the northern Mexican gartersnake,
and the narrow-headed gartersnake. USFWS (2008, pp. 112-131) supports
our rationale as to how adverse effects to native aquatic species occur
from the presence and operation of reservoirs in the Gila River basin
of Arizona.
Comment 87: In the proposed rule, the Service refers to the
potential development of the Hooker Dam on the mainstem Gila River
above Mogollon Creek and below Turkey Creek. The U.S. Bureau of
Reclamation has abandoned any intention of completing Hooker Dam, and
its reference as a possible future project should be deleted from the
final rule.
Our Response: We have confirmed with the U.S. Bureau of Reclamation
that there are no current plans to develop Hooker Dam, and it is not
referenced in the final rule.
Comment 88: Barriers to fish movement out of Roosevelt Lake should
be acknowledged in the final rule. The Roosevelt Dam on the Salt River
serves as an effective barrier to upstream fish movement, which would
prevent nonnative fish from moving upstream.
Our Response: In the final rule, we added a statement in our
discussion of dams to reflect this fact.
Comment 89: The proposed rule states that additional land and water
use activities along Tonto Creek and the Salt River, including areas
upstream of Roosevelt Lake, contribute to the persistence of nonnative
aquatic species that negatively affect the gartersnakes. However, the
Tonto Creek exhibits seasonally intermittent flows in the lower reaches
below Gun Creek. Sections of dry streambed serve as a barrier to
upstream fish migration. Further, high flow events have been documented
to remove nonnative species by flushing them downstream. In addition,
nonnative spiny-rayed fish are not typically motivated to migrate
upstream out of lakes because they prefer lentic over lotic habitats.
Our Response: Connectivity between otherwise spatially intermittent
reaches is established during seasonal periods of snowmelt runoff as
well as during medium- to large-scale flood pulses. These opportunities
contribute to the distribution of harmful nonnative fish throughout
Tonto Creek, as demonstrated in fish survey data that has been
collected, reviewed, and reported in Appendix A. With respect to
whether harmful nonnative fish are ``not typically motivated to migrate
upstream out of lakes,'' the data are lacking to clearly defend this
statement, especially when reservoir levels decrease, which lessens the
amount of space available in reservoirs, which may in turn trigger
dispersal or movement behaviors in harmful nonnative fish that are
known to be territorial by their nature. Additionally, the simple
presence of otherwise ``lentic'' nonnative species in lotic habitat
upstream of reservoirs to which they are hydrologically connected,
suggests this perceived preference may not be altogether true; green
sunfish are an excellent example.
[[Page 38738]]
Comment 90: A number of other activities (both present and
historical) in the area of Tonto Creek and the Salt River in the
vicinity and upstream of Roosevelt Lake are likely contributing to the
decline of gartersnakes and the aquatic and riparian habitat on which
they depend. Specifically, a historical stocking program of nonnatives,
manmade impoundments within the Tonto Creek floodplain, and other
activities identified in the proposed rule, such as groundwater
pumping, flood control projects, urbanization, and livestock grazing.
The major activities reducing flows and dewatering habitat are
occurring upstream of Roosevelt Lake. A bridge is proposed over Tonto
Creek, and 320 to 640 residences are projected to be built on the east
side of Tonto Creek, under the Gila County's comprehensive plan. This
would increase water and recreational use. The U.S. Forest Service's
Motorized Travel Management Plan has the potential to open 2,567 miles
(4,131 km) of road to high clearance vehicles and 967 miles (1,556 km)
to passenger vehicles. The Tonto National Forest's Salt River
Allotments Vegetative Management Plan would allow continued grazing on
more than 275,000 acres (111,000 ha) along the Upper Salt River.
Potential impacts to the narrow-headed gartersnake are noted, and the
potentially suitable habitat for the northern Mexican gartersnake that
occurs along the Salt River is the same area that the USFS proposes for
grazing.
Our Response: We agree that numerous threats are affecting the
status of both gartersnake species in Tonto Creek. The final rule (see
``Altering or Dewatering Aquatic Habitat'') references land use
activities in this area that we consider as having an effect on
resident gartersnake populations.
Comment 91: The Service's generalized and unsupported assertions
that all dams have the same impacts on gartersnakes should be removed
from the final rule. The ``Altering or Dewatering Aquatic Habitat''
section of the proposed rule is not supported by any citations
regarding water level fluctuations in reservoirs and cross-section
profiles of a reservoir. This section should provide citations and
recognize the diversity of the various types of reservoirs.
Statements regarding the effect of Roosevelt Lake on gartersnake
populations in Tonto Creek and the upper Salt River lack any scientific
or technical basis and should be removed from the final rule. Other
than referencing a biological opinion (USFWS 2008, pp. 112-131), the
proposed rule provides no basis for the assertion that harmful
nonnative fish are moving upstream out of Roosevelt Lake into Tonto
Creek or the Salt River. Since the biological opinion in 2008,
monitoring conducted under the Horseshoe-Bartlett Habitat Conservation
Plan has been implemented to document the movement of nonnative fish
upstream of the Horseshoe Reservoir into the Verde River, and reaches
of the Verde River have been sampled, and to date no evidence of fish
movement has been detected.
Our Response: We agree that not every dam has the same effect on
the stream on which it is located. We disagree that our treatment of
the effects of dams on occupied lotic habitat are unsupported. The
identified section discusses general effects of dams, based on
available literature, as a suite of effects common in all instances in
various degrees. This same section also includes referenced discussion
of specific dams or diversions and their specific effects on certain
gartersnake populations. The relationship of the cross-sectional
profiles and water level fluctuations of reservoirs to benefits to
harmful nonnative fish communities was an integral part of a 4-year
evaluation, in close collaboration with the operators of those
reservoirs themselves, dedicated to the development of the habitat
conservation plan for Bartlett and Horseshoe Reservoirs on the Verde
River. We incorporated by reference this exhaustive analysis, which
used the best available data to date (see SRP 2008, entire; USFWS 2008,
pp. 112-131).
We are not aware of any analysis afforded specifically to the
potential benefits of Roosevelt Dam operations to the sustainment or
production of harmful nonnative fish populations in Roosevelt Lake,
Tonto Creek, or the Salt River, upstream of Roosevelt Dam. The
exhaustive analysis of these effects as they are attributed to
similarly sized dams and reservoirs on the Verde River system
referenced immediately above represent the most applicable, current,
and robust analyses to date. We do note that Roosevelt Lake does not
fluctuate as much as does Horseshoe Reservoir on the Verde River and,
therefore, most likely provides greater benefits to the resident
harmful nonnative fish community. With respect to fish sampling data
from the implementation of the Horseshoe and Bartlett HCP, sampling
events do not occur during the most appropriate time to capture
movement of fish out of the reservoir (during periods of rapid drawdown
or during drawdown after periods of prolonged storage) and thus may not
adequately capture these relationships. Additionally, more fish have to
be marked in the reservoir to create better opportunities for their
discovery elsewhere in the watershed. Lastly, recent northern Mexican
gartersnake records have been reported immediately upstream, if not
adjacent to, Roosevelt Lake, which affirms that adverse effects from
harmful nonnative species that occur in Roosevelt Lake present a
demonstrable threat to that population of northern Mexican
gartersnakes.
Comment 92: The proposed rule states that, on the upper Verde
River, native species dominated the total fish community at greater
than 80 percent from 1994 to 1996, before dropping to approximately 20
percent in 1997 and 19 percent in 2001. This statement points to
specific empirical data regarding declining native fish species in the
upper Verde River watershed, but there is no reference to verify the
sources, context, or specific species to which it is referring.
Our Response: Rinne et al. (2005, pp. 6-7) contains a discussion of
shifting fish communities in the Verde River, and Bonar et al. (2004,
entire) contains a detailed analysis of the role harmful nonnative
fishes have had on the native fish community of the Verde River. Also
Bonar et al. (2004, pp. 6-7) summarizes this information.
Comment 93: If it is true that the narrow-headed and northern
Mexican gartersnakes have declined substantially in the United States
and the decline of these species is most likely due to the introduction
of nonnative predator and competitor species as stated in the 2006 and
2008 status reports, then the listing of these species as threatened
will do little for their recovery.
Our Response: As stated in the proposed rule, conservation measures
provided to species listed as endangered or threatened species under
the Act include recognition, recovery actions, requirements for Federal
protection, and prohibitions against certain practices. Recognition of
conservation needs of species through listing under the Act results in
public awareness and conservation by Federal, State, tribal, and local
agencies, private organizations, and individuals. The Act encourages
cooperation with the States and recovery plans will identify recovery
actions that will benefit listed species. See ``Available Conservation
Measures'' in this final rule for additional information on this
subject.
Comment 94: Local persons are catching gartersnakes in contests and
seeing how many they can kill to win the contest.
Our Response: We have no information to indicate that collection of
[[Page 38739]]
gartersnakes is a significant threat. However, if this activity is
occurring, it will be considered a prohibited take of the species, once
listed.
Comment 95: The Service should take into account the adverse
effects of the past Federal land management agency burning programs and
the recent wildfires that have occurred in the narrow-headed and
northern Mexican gartersnakes home ranges. Closer scrutiny of the
current Federal land management burning program, and lack of a coherent
thinning and logging program, coupled with a better understanding of
the effects of the recent large wildfires, should be completed in order
to focus future protection and restoration efforts towards what is
truly causing the decline of the narrow-headed and northern Mexican
gartersnakes. There is no benefit to immediately listing these
gartersnakes as threatened when there is doubt concerning the current
and future potential cause for decline of the species.
Our Response: In the proposed rule, we discuss effects of recent
fire management policies on aquatic communities in Madrean Oak Woodland
biotic communities in the southwestern United States. Existing wildfire
suppression policies intended to protect the expanding number of human
structures on forested public lands have altered the fuel loads in
these ecosystems and increased the probability of high-intensity
wildfires (Rinne and Neary 1996, p. 143). The historical actions
affecting a species are considered as background in our assessment in
terms of their contribution to the present-day status of these species.
However, in evaluating the status of the species, the Act requires that
we assess present and future factors that may threaten the species. If
past actions are continuing threats, these threats are evaluated under
the five-factor analysis. If these past actions are not continued
factors, then these actions are not assessed in the analysis of the
future status because they are no longer present or future factors
threatening the species.
Section 7(a)(1) of the Act requires that all Federal agencies shall
utilize their authorities in furtherance of the purposes of the Act by
carrying out programs for the conservation of endangered and threatened
species. Section 7(a)(2) of the Act requires Federal agencies to ensure
that activities they authorize, fund, or carry out are not likely to
jeopardize the continued existence of the species or destroy or
adversely modify its critical habitat. If a Federal action may affect a
listed species or its critical habitat, the responsible Federal agency
must enter into formal consultation with us. Lastly, while we
acknowledge in the proposed and final rules that large wildfires can
have significant adverse effects on gartersnake populations and their
prey base (in particular for narrow-headed gartersnakes), the
literature is clear that harmful nonnative species pose the most
significant threat to both species, rangewide, through a variety of
ecological mechanisms.
Comment 96: The proposed rule states that Cavazos and Arriaga
(2010, entire) found that average temperatures along the Mexican
Plateau in Mexico could rise by as much as 1.8[emsp14][deg]F (1 [deg]C)
in the next 20 years and by as much as 9[emsp14][deg]F (5 [deg]C) in
the next 20 years, according to their models. This statement is
confusing because the reference cites two different temperatures for
the same timeframe in the same area.
Our Response: Climate models often report a range of scenarios, as
was the case in this instance. We did revise that language for clarity.
However, we expect precipitation and temperature trends, as modeled
under future climate change projections, to increase regional aridity
in Mexico within the distribution of the northern Mexican gartersnake,
which is expected to place additional drought stress on stream flow and
reduce the permanency of cienegas, marshes, and livestock tanks. As
streams dry, they will become unsuitable as habitat for this
gartersnake and its prey base over the next several decades.
Comment 97: We request that the Service provide clarification and
more information regarding the presence of mercury in Tonto Creek and
likely sources of this substance. No study was cited for the claim that
mercury appears to be bioaccumulating in fish in the lower reaches of
the Tonto Creek, only a personal communication with Arizona Department
of Environmental Quality. The information in the proposed rule is
contrary to the Arizona Department of Environmental Quality's 2011
report on ``Fish Consumption Risk Analysis for Tonto Creek, Arizona.''
Specifically, desert suckers have the fourth highest mercury levels,
not the second.
Our Response: We updated this discussion under ``Environmental
Contaminants'' in the final rule to include data reported by ADEQ
(2011, entire), as well as other information, and acknowledged in the
proposed and final rules that no study on the bioaccumulation of
mercury in resident gartersnakes has been implemented that we are aware
of. The suggestion that bioaccumulation of mercury could be occurring
is based on the accepted scientific premise regarding the toxicology of
mercury in ecosystems and its ability to increase its concentration in
tissue with increasing trophic orders. Gartersnakes are tertiary
consumers and, therefore, are expected to bioaccumulate contaminants
such as mercury in their tissues.
Comment 98: The term excessive sedimentation as used in the
proposed rule is open to interpretation and should be defined to
eliminate unnecessary waste of resources of the Service in defending
its finding. Any large storm event that changes the morphology of a
channel or adjoining riparian habitat can be used to control all human
activities in that they can be construed to have caused the resulting
flooding.
Our Response: It is beyond our scope to quantitatively define what
level of sedimentation is excessive for every stream. However, we agree
that flood pulses naturally liberate sediment in arid southwestern
watersheds. In the absence of absolute values or metrics, we consider
excessive sedimentation that level in which resident gartersnake prey
species or gartersnakes themselves are not able to adequately carry out
life-history functions such as feeding, sheltering, or breeding as a
result of the effects of sedimentation. Arizona and New Mexico also
have turbidity or total dissolved solid standards for surface water,
which can also be used as a reference.
Comment 99: The proposal to list is based on the false premise that
riparian habitats are declining in the Southwest (see Webb et al.
2007).
Our Response: A comprehensive analysis of the scientific literature
supports our evaluation of the status of habitat where these
gartersnakes historically or currently occur.
Comment 100: We request the Service clarify the year of reference
in their projection that annual precipitation amounts in the
southwestern United States may decrease by 10 percent by the year 2100.
Our Response: Overpeck (2008, entire) is a presentation where this
information was originally presented although much of the information
used in Overpeck (2008) was from the Intergovernmental Panel on Climate
Change (IPCC 2007). We presume the year(s) of reference may be 2007-
2008 because that is the time period when the reference was created.
Comment 101: The Service should acknowledge the uncertainty of
broad predictions associated with climate change in their final rule.
Our Response: In our analyses, we use our expert judgment to weigh
relevant information, including uncertainty, in
[[Page 38740]]
our consideration of various aspects of climate change and their
predicted effects on northern Mexican and narrow-headed gartersnakes.
Comment 102: The Service states that wildfire is a threat to the
narrow-headed gartersnake throughout its range. However, the Service
also discusses the Dry Lakes Fire of 2002, which resulted in a complete
fish kill in Turkey Creek. Turkey Creek has since been recolonized by
native fish species almost exclusively. Consequently, it is conceivable
that snakes that survived a period without fish might then find
themselves in an environment better suited to their needs (i.e., devoid
of nonnative species) than before the fire. Further, the Service states
that both species of gartersnakes are somewhat resilient to physical
habitat disturbance where harmful nonnative species are absent.
Our Response: We agree that if enough individual narrow-headed
gartersnakes can survive the post-fire period of ash flows and fish
kills, without risking genetic bottlenecking within the population,
that an ensuing native-only fish community would be highly beneficial.
However, field research has proven that over time and without a barrier
to upstream movement, harmful nonnative fish ultimately make their way
back into these streams and negatively affect the native aquatic
community. Therefore, any plausible post-fire benefits to surviving
narrow-headed gartersnakes are most likely short-lived.
Information Quality and Quantity
Comment 103: Personal communications of a graduate student are a
weak basis for determining the current status of the narrow-headed
gartersnake in New Mexico (or, as found in other citations, the effects
of the Whitewater Baldy fire on the narrow-headed and northern Mexican
gartersnakes). Personal communications or gray literature are not
subject to the necessary vigorous peer review and substantiation that
would meet the Act's requirements for science-based or commercial data.
Our Response: As required by the Act, we based our proposal and
this final rule on the best available scientific and commercial data.
Our Policy on Information Standards Under the Act (published in the
Federal Register on July 1, 1994 (59 FR 34271)), the Information
Quality Act (section 515 of the Treasury and General Government
Appropriations Act for Fiscal Year 2001 (Pub. L. 106-554; H.R. 5658)),
and our associated Information Quality Guidelines, provide criteria,
establish procedures, and provide guidance to ensure that our decisions
are based on the best scientific data available. Information sources
may include the recovery plan for the species, articles in peer-
reviewed journals, conservation plans developed by States and counties,
scientific status surveys and studies, biological assessments, other
unpublished materials, or experts' opinions or personal knowledge. We
receive and use information on the biology, ecology, distribution,
abundance, status, and trends of species from a wide variety of sources
as part of their responsibility to implement the Act. This information
includes status surveys, biological assessments, and other unpublished
material (that is, ``gray literature'') from State natural resource
agencies and natural heritage programs, Tribal governments, other
Federal agencies, consulting firms, contractors, and individuals
associated with professional organizations and higher educational
institutions. We also use published articles from juried professional
journals. The reliability of the information contained in these sources
can be as variable as the sources themselves. As part of their routine
activities, our biologists are required to gather, review, and evaluate
information from these sources prior to undertaking listing, recovery,
consultation, and permitting actions.
Comment 104: If science-based and commercial data are not available
for populations, then any projections for populations in the United
States based on northern Mexican gartersnake populations would
necessarily be speculative.
Our Response: The Act requires that we use the best scientific and
commercial data available at the time of listing. Appendix A (available
at https://www.regulations.gov, Docket No. FWS-R2-ES-2013-0071)
discusses such considerations as the physical condition of habitat, the
composition of the aquatic biological community, the existence of
significant threats, and the length of time since the last known
observation of the subspecies in presenting rationale for determining
occupancy status at each locality.
Comment 105: The Service's statement that as much as 90 percent of
historical populations in the United States either occur at low
densities or are extirpated due to the total number of stream miles
that are now permanently dewatered appears to be pure speculation and
not supported by factual data. It is doubtful that an accurate
accounting exists of stream miles in the United States that
historically supported the northern Mexican gartersnakes, and it is
further doubtful that an accurate accounting exists of stream miles
that historically were perennial and are now ephemeral. This kind of
information would require dealing with specific time periods and
specific stream reaches, which is not offered in the statement.
Our Response: This assessment is based on the best available
scientific and commercial data for northern Mexican gartersnakes in the
United States. Museum records and habitat requirements indicate the
species technically occurred in every county and nearly every subbasin
within Arizona. We used GIS and information on threats and status of
historical populations as well as habitat preferences, in arriving at
the 90 percent figure, which we consider to be reasonably accurate
given the information available. Considering the large number of stream
miles that were historically perennial within the historical
distribution of the northern Mexican gartersnake in Arizona that are
now ephemeral, and the degraded status of populations as a result of a
multitude of threats, our presentation of the data represents the most
accurate possible.
Effect of Listing on Non-Federal Interests
Comment 106: The language in the proposed rule that lists
activities which could result in the reduction of the distribution or
abundance of important gartersnake prey species, as well as reduce the
distribution and amount of suitable physical habitat on a regional
landscape for the gartersnakes themselves, is an invitation for many
organizations to sue the Service for allowing activities deemed to
affect the gartersnake on a regional landscape basis. This gives the
gartersnakes' prey species endangered status under the Act also.
Our Response: The Act and its implementing regulations set forth a
series of general prohibitions and exceptions that apply to all
wildlife listed under the ESA. The prohibitions of section 9(a)(2) of
the Act make it illegal for any person subject to the jurisdiction of
the United States to take (includes harass, harm, pursue, hunt, shoot,
wound, kill, trap, capture, or collect; or to attempt any of these),
import, export, ship in interstate commerce in the course of commercial
activity, or sell or offer for sale in interstate or foreign commerce
any listed species.
We may issue permits to carry out otherwise prohibited activities
involving endangered and threatened wildlife species under certain
[[Page 38741]]
circumstances. A permit must be issued for the following purposes: For
scientific purposes, to enhance the propagation or survival of the
species, and for incidental take in connection with otherwise lawful
activities.
It is our policy, as published in the Federal Register on July 1,
1994 (59 FR 34272), to identify to the maximum extent practicable at
the time a species is listed, those activities that would or would not
constitute a violation of section 9 of the Act. The intent of this
policy is to increase public awareness of the effect of a proposed
listing on proposed and ongoing activities within the range of species
proposed for listing. See the Available Conservation Measures section
in the proposed rule for a list of activities that could potentially
result in a violation of section 9 of the Act. Lastly, it is important
to note that our emphasis for the recovery of listed species is to
assess and improve ecosystem function as a basic tenant of conservation
biology; this includes the physical habitat and biological community
where a listed species occurs. This management construct is not unique
to these gartersnakes.
Comment 107: Listing will hinder conservation efforts of the New
Mexico Department of Game and Fish.
Our Response: We disagree. Once these species are listed, funding
for recovery actions may be more accessible from a variety of sources,
including Federal grants, State programs, and cost-share grants for
non-Federal landowners, the academic community, and nongovernmental
organizations. In addition, pursuant to section 6 of the Act, the
States of Arizona and New Mexico will be eligible for Federal funds to
implement management actions that promote the protection or recovery of
the narrow-headed and northern Mexican gartersnakes.
Section 4(d) Rule
Comment 108: If the Service decides to list the species, then we
recommend the development of a 4(d) rule to exempt landowners from
prohibitions of take under section 9 of the Act for those actions
benefitting the two species of gartersnakes, as was the case for the
Chiricahua leopard frog.
Our Response: We proposed a special rule for the northern Mexican
gartersnake under section 4(d) of the Act that would exempt take of
northern Mexican gartersnakes as a result of livestock use at or
maintenance of livestock tanks located on non-Federal lands, and a
final 4(d) rule is incorporated into this final rule. We do not have
the necessary information at this time to determine that general
actions benefitting the two species of gartersnakes would meet the
standard of a 4(d) rule to be necessary and advisable for the
conservation of the species. We would need more specific information
regarding the actions under consideration.
Comment 109: Concerned with the language in the proposed 4(d) rule,
which states: ``Incidental take of northern Mexican gartersnakes is not
a violation of section 9 of the Act if it occurs from any other
otherwise legal activities involving northern Mexican gartersnakes and
their habitat that are conducted in accordance with applicable State,
Federal, tribal, and local laws and regulations.'' This language could
be interpreted to allow incidental take for any activity in the snake's
habitat as long as the activity was legal. We suggest the following
language: (3) What activities are allowed? Incidental take of northern
Mexican gartersnakes is not a violation of section 9 of the Act if it
occurs from (a) otherwise legal activities involving northern Mexican
gartersnakes and their habitat that are conducted in accordance with
applicable State, Federal, tribal, and local laws and regulations, and
(b) such activities occurring in northern Mexican gartersnake habitat
pertain to maintenance activities at livestock tanks located on
private, State, or tribal lands. A livestock tank is an existing or
future impoundment in an ephemeral drainage or upland site constructed
primarily as a watering site for livestock.
Our Response: We have amended the 4(d) rule, in the final rule, to
reflect this recommendation. We revised the language in the 4(d) rule
to better describe our intention for the rule to exempt only activities
related to the construction, use, and maintenance of stock tanks for
livestock watering. These changes did not alter the scope of the 4(d)
rule.
Determination--Standard for Review
Section 4 of the Act (16 U.S.C. 1533), and its implementing
regulations at 50 CFR part 424, set forth the procedures for adding
species to the Federal Lists of Endangered and Threatened Wildlife and
Plants. Under section 4(a)(1) of the Act, we may list a species based
on (A) The present or threatened destruction, modification, or
curtailment of its habitat or range; (B) Overutilization for
commercial, recreational, scientific, or educational purposes; (C)
Disease or predation; (D) The inadequacy of existing regulatory
mechanisms; or (E) Other natural or manmade factors affecting its
continued existence. Listing actions may be warranted based on any of
the above threat factors, singly or in combination.
Until recently the Service has presented its evaluation of
information under the five listing factors in an outline format,
discussing all of the information relevant to any given factor and
providing a factor-specific conclusion before moving to the next
factor. However, the Act does not require findings under each of the
factors, only an overall determination as to the species' status (for
example, threatened, endangered, or not warranted). Ongoing efforts to
improve the efficiency and efficacy of the Service's implementation of
the Act have led us to present this information in a different format
that we believe leads to greater clarity in our understanding of the
science, its uncertainties, and our application of our statutory
framework to that science. Therefore, while the presentation of
information in this rule differs from past practice, it differs in
format only. We have evaluated the same body of information we would
have evaluated under the five listing factors outline format in the
past, we are applying the same information standard, and we are
applying the same statutory framework in reaching our conclusions.
Determination for Northern Mexican Gartersnake
The Act defines an endangered species as any species (or
subspecies) that is ``in danger of extinction throughout all or a
significant portion of its range'' and a threatened species as any
species ``that is likely to become endangered throughout all or a
significant portion of its range within the foreseeable future.'' We
have carefully assessed the best scientific and commercial information
available regarding the status of the northern Mexican gartersnake and
have determined that this subspecies meets the definition of a
threatened subspecies under the Act based on its current status and the
future threats to the subspecies.
We find that the northern Mexican gartersnake is not currently in
danger of extinction because it remains extant in most of the subbasins
where it historically occurred, and its known threats have not yet
resulted in substantial range reduction or a substantial number of
population extirpations to put the subspecies on the brink of
extinction. Currently, only 6 former United States populations were
found to be likely extirpated, and 29 populations are believed to
remain extant. Therefore, we determined that the present risk of
extinction is not
[[Page 38742]]
sufficient to warrant a finding of endangered under the Act.
However, the northern Mexican gartersnake has undergone declines in
its abundance, and we found only 5 of 29 current populations in the
United States are likely viable into the foreseeable future, or what we
consider to be the next several decades. While we are not able to
quantify the status of all populations in Mexico, based on the threats
and the declining status of aquatic communities there, we assume a
similar status in the Mexican portion of its range. We expect the
status of the subspecies will decline in the next several decades
mainly as a result of the continuing and expanding impacts of harmful
nonnative species and the increasing nature of threats associated with
human population growth and climate change. As the effects of these
threats escalate on the landscape (as summarized below), we expect that
additional populations will be extirpated, and that the northern
Mexican gartersnake will be in danger of extinction in the foreseeable
future.
In our review of the best available scientific and commercial
information, we found that aquatic ecosystems upon which the northern
Mexican gartersnake relies have been significantly degraded by the
introduction and proliferation of harmful nonnative species (Factors C
and E). Harmful nonnative species (mainly predatory fishes, bullfrogs,
and crayfish) have been intentionally released or have naturally moved
into nearly every subbasin throughout the range of the northern Mexican
gartersnake. This has resulted in widespread declines in native fish
and amphibian communities, which are integral to the continued survival
of the northern Mexican gartersnake because they serve as their primary
food source. Harmful nonnative species have indirectly impacted
northern Mexican gartersnakes by predation on their prey base (native
fish and amphibians) and have directly impacted them through preying on
young gartersnakes (Factor B), which impacts gartersnake populations
through declines in the recruitment of young snakes into the
reproductive age class. In combination, these factors have resulted in
population declines, range restrictions within subbasins, and some
population extirpations. We found the threat related to harmful
nonnative species to be the most significant and pervasive of all
threats affecting the subspecies.
Additional threats to the habitat of northern Mexican gartersnakes
include water use activities, climate change, and drought (Factor A).
Dams, water diversions, flood-control projects, and groundwater pumping
have dewatered entire reaches of historically occupied habitat in some
areas. The rapidly growing human population in the arid southwestern
United States, combined with a drought-limited supply of surface water,
will further increase future needs for water supplies and associated
infrastructure (dams, diversions, and groundwater pumping) that will
also contribute to habitat losses in the next several decades. Losses
of aquatic habitats are also expected due to the impacts of climate
change, which includes increased aridity, lower annual precipitation
totals, lower snow pack levels, higher variability in flows (lower low-
flows and higher high-flows) in the southwestern United States and
northern Mexico. The population-level effect of factors that modify or
destroy the physical attributes of gartersnake habitat is amplified
when they act in the presence of harmful nonnative species.
Other factors act in combination to negatively affect the northern
Mexican gartersnake, including mismanaged or unmanaged livestock
grazing (Mexico; Factor A); road construction, use, and maintenance
(Factor A); adverse human interactions (Factor E); environmental
contaminants (Factor A); erosion control techniques (Factor A); and
possible competitive pressures from sympatric species (Factor E). These
threats occur within the distribution of this gartersnake and
contribute to further population declines or extirpations where
gartersnakes already occur at low population densities due to the
impacts of harmful nonnative species. The existing regulatory
mechanisms currently in place (Factor D) do not target the conservation
of this subspecies or its habitat in the United States or Mexico.
Therefore, on the basis of the best available scientific and
commercial information, we find the northern Mexican gartersnake is
likely to become in danger of extinction throughout all of its range
within the foreseeable future, and we are listing the northern Mexican
gartersnake as a threatened subspecies in accordance with sections
3(20) and 4(a)(1) of the Act.
Determination for Narrow-Headed Gartersnakes
The Act defines an endangered species as any species that is ``in
danger of extinction throughout all or a significant portion of its
range'' and a threatened species as any species ``that is likely to
become endangered throughout all or a significant portion of its range
within the foreseeable future.'' We have carefully assessed the best
scientific and commercial information available regarding the status of
the narrow-headed gartersnake and have determined that this species
meets the definition of a threatened subspecies under the Act based on
its current status and the future threats to the species.
We find that the narrow-headed gartersnake is not currently in
danger of extinction because it remains extant in most of the subbasins
where it historically occurred, and its known threats have not yet
resulted in substantial range reduction or a substantial number of
population extirpations to put the species on the brink of extinction.
Currently, only 5 former populations were found to be likely
extirpated, and 36 populations are believed to remain extant.
Therefore, we determined that the present risk of extinction is not
sufficient to warrant a finding of endangered under the Act.
However, the narrow-headed gartersnake has undergone declines in
its abundance, and we found only 5 of 36 current populations are likely
viable into the foreseeable future, or what we consider to be the next
several decades. We expect the status of the species will decline in
the next several decades mainly as a result of the continuing and
expanding impacts of harmful nonnative species and the increasing
nature of threats associated with human population growth and climate
change. As the effects of these threats escalate on the landscape (as
summarized below), we expect that additional populations will be
extirpated, and that the narrow-headed gartersnake will be in danger of
extinction in the foreseeable future.
In our review of the best available scientific and commercial
information, we found that native fish communities, upon which the
narrow-headed gartersnake relies heavily, have been significantly
degraded by the introduction and proliferation of harmful nonnative
species (Factors C and E). Harmful nonnative species (mainly predatory
fishes, bullfrogs, and crayfish) have been intentionally released or
have naturally moved into nearly every subbasin throughout the range of
the narrow-headed gartersnake. This has resulted in widespread declines
in native fish communities, which are integral to the continued
survival of the narrow-headed gartersnake because they serve as their
primary food source. Harmful nonnative species have indirectly impacted
narrow-headed gartersnakes by predation on their prey base (native
fish) and have directly impacted them through preying on young
gartersnakes (Factor B), which impacts gartersnake populations through
the decline in
[[Page 38743]]
recruitment of young snakes into the reproductive age class. In
combination, these factors have resulted in population declines, range
restrictions within subbasins, and some population extirpations. We
found the threat related to harmful nonnative species to be the most
significant and pervasive of all threats affecting the species.
Additional threats to the habitat of narrow-headed gartersnakes
include water use activities, climate change, and wildfires (Factor A).
Dams, water diversions, flood-control projects, and groundwater pumping
have dewatered entire reaches of historically occupied habitat in some
areas. The rapidly growing human population in the arid southwestern
United States, combined with a drought-limited supply of surface water,
will further increase future needs for water supplies and associated
infrastructure (dams, diversions, and groundwater pumping) that will
also contribute to habitat losses in the next several decades. Losses
of aquatic habitats are also expected due to the impacts of climate
change, which includes increased aridity, lower annual precipitation
totals, lower snow pack levels, higher variability in flows (lower low-
flows and higher high-flows), and enhanced stress on ponderosa pine
communities in the southwestern United States. Wildfires in the arid
southwestern United States have grown more frequent and severe, due in
part to the fire management policies of past decades. High-intensity
wildfires that affect large areas contribute to significant flooding
and sedimentation, resulting in fish kills and the filling-in of
interstitial spaces in river cobble, which the species uses for hunting
fish), as well as important pool habitat. These impacts negatively
affect the fish and amphibian prey base for narrow-headed gartersnakes
for extended periods of time. The frequency and intensity of large
wildfires is likely to increase in the foreseeable future as an
indirect effect of drier and hotter landscape conditions associated
with climate change. The population-level effect of factors that modify
or destroy the physical attributes of gartersnake habitat is amplified
when they act in the presence of harmful nonnative species.
Other factors act in combination to negatively affect the narrow-
headed gartersnake, including road construction, use, and maintenance
(Factor A); adverse human interactions (Factor E); environmental
contaminants (Factor A); and erosion control techniques (Factor A).
These threats occur within the distribution of this gartersnake and
contribute to further population declines or extirpations where
gartersnakes already occur at low population densities due to the
impacts of harmful nonnative species. The existing regulatory
mechanisms currently in place (Factor D) do not target the conservation
of this species or its habitat.
Therefore, on the basis of the best available scientific and
commercial information, we find the narrow-headed gartersnake is likely
to become in danger of extinction throughout all of its range within
the foreseeable future, and we are listing the narrow-headed
gartersnake as a threatened species in accordance with sections 3(20)
and 4(a)(1) of the Act.
Available Conservation Measures
Conservation measures provided to species listed as endangered or
threatened under the Act include recognition, recovery actions,
requirements for Federal protection, and prohibitions against certain
practices. Recognition through listing results in public awareness and
conservation by Federal, State, Tribal, and local agencies, private
organizations, and individuals. The Act encourages cooperation with the
States and requires that recovery actions be carried out for all listed
species. The protection required by Federal agencies and the
prohibitions against certain activities are discussed, in part, below.
The primary purpose of the Act is the conservation of endangered
and threatened species and the ecosystems upon which they depend. The
ultimate goal of such conservation efforts is the recovery of these
listed species, so that they no longer need the protective measures of
the Act. Subsection 4(f) of the Act requires the Service to develop and
implement recovery plans for the conservation of endangered and
threatened species. The recovery planning process involves the
identification of actions that are necessary to halt or reverse the
species' decline by addressing the threats to its survival and
recovery. The goal of this process is to restore listed species to a
point where they are secure, self-sustaining, and functioning
components of their ecosystems.
Recovery planning includes the development of a recovery outline
shortly after a species is listed, preparation of a draft and final
recovery plan, and revisions to the plan as significant new information
becomes available. The recovery outline guides the immediate
implementation of urgent recovery actions and describes the process to
be used to develop a recovery plan. The recovery plan identifies site-
specific management actions that will achieve recovery of the species,
measurable criteria that determine when a species may be downlisted or
delisted, and methods for monitoring recovery progress. Recovery plans
also establish a framework for agencies to coordinate their recovery
efforts and provide estimates of the cost of implementing recovery
tasks. Recovery teams (composed of species experts, Federal and State
agencies, nongovernmental organizations, and stakeholders) are often
established to develop recovery plans. When completed, the recovery
outline, draft recovery plan, and the final recovery plan will be
available on our Web site (https://www.fws.gov/endangered), or from our
Arizona Ecological Services Field Office (see FOR FURTHER INFORMATION
CONTACT).
Implementation of recovery actions generally requires the
participation of a broad range of partners, including other Federal
agencies, States, Tribal, nongovernmental organizations, businesses,
and private landowners. Examples of recovery actions include habitat
restoration (e.g., restoration of native vegetation), research, captive
propagation and reintroduction, and outreach and education. The
recovery of many listed species cannot be accomplished solely on
Federal lands because their range may occur primarily or solely on non-
Federal lands. To achieve recovery of these species requires
cooperative conservation efforts on private, State, and Tribal lands.
Following publication of this final listing rule, funding for
recovery actions will be available from a variety of sources, including
Federal budgets, State programs, and cost-share grants for non-Federal
landowners, the academic community, and nongovernmental organizations.
In addition, under section 6 of the Act, the States of Arizona and New
Mexico would be eligible for Federal funds to implement management
actions that promote the protection and recovery of the northern
Mexican and narrow-headed gartersnakes. Information on our grant
programs that are available to aid species recovery can be found at:
https://www.fws.gov/grants.
Please let us know if you are interested in participating in
recovery efforts for these species. Additionally, we invite you to
submit any new information on these species whenever it becomes
available and any information you may have for recovery planning
purposes (see FOR FURTHER INFORMATION CONTACT).
Section 7(a) of the Act requires Federal agencies to evaluate their
actions with respect to any species that is proposed or listed as
endangered or
[[Page 38744]]
threatened and with respect to its critical habitat, if any is
designated. Regulations implementing this interagency cooperation
provision of the Act are codified at 50 CFR part 402. Section 7(a)(4)
of the Act requires Federal agencies to confer with the Service on any
action that is likely to jeopardize the continued existence of a
species proposed for listing or result in destruction or adverse
modification of proposed critical habitat. If a species is listed
subsequently, section 7(a)(2) of the Act requires Federal agencies to
ensure that activities they authorize, fund, or carry out are not
likely to jeopardize the continued existence of the species or destroy
or adversely modify its critical habitat. If a Federal action may
affect a listed species or its critical habitat, the responsible
Federal agency must enter into formal consultation with the Service.
Federal agency actions within the species' habitats that may
require conference or consultation or both as described in the
preceding paragraph include management and any other landscape-altering
activities on Federal lands administered by the Fish and Wildlife
Service, U.S. Bureau of Reclamation, or U.S. Forest Service; issuance
of section 404 Clean Water Act permits by the U.S. Army Corps of
Engineers; construction and management of gas pipeline and power line
rights-of-way by the Federal Energy Regulatory Commission; construction
and maintenance of roads or highways by the Federal Highway
Administration; and other discretionary actions that affect the species
composition of biotic communities where these species or their habitats
occur, such as funding or permitting programs that result in the
continued stocking of nonnative, predatory fish.
The Act and its implementing regulations set forth a series of
general prohibitions and exceptions that apply to all endangered
wildlife. The prohibitions of section 9(a)(2) of the Act, codified at
50 CFR 17.21 for endangered wildlife, in part, make it illegal for any
person subject to the jurisdiction of the United States to take
(includes harass, harm, pursue, hunt, shoot, wound, kill, trap,
capture, or collect; or to attempt any of these), import, export, ship
in interstate commerce in the course of commercial activity, or sell or
offer for sale in interstate or foreign commerce any listed species.
Under the Lacey Act (18 U.S.C. 42-43; 16 U.S.C. 3371-3378), it is also
illegal to possess, sell, deliver, carry, transport, or ship any such
wildlife that has been taken illegally. Certain exceptions apply to
agents of the Service and State conservation agencies. The prohibitions
of section 9(a)(2) of the Act, codified at 50 CFR 17.31 for threatened
wildlife, make it such that all the provisions of 50 CFR 17.21 apply,
except Sec. 17.21(c)(5).
We may issue permits to carry out otherwise prohibited activities
involving endangered and threatened wildlife species under certain
circumstances. Regulations governing permits are codified at 50 CFR
17.22 for endangered species, and at Sec. 17.32 for threatened
species. A permit must be issued for the following purposes: For
scientific purposes, to enhance the propagation or survival of the
species, and for incidental take in connection with otherwise lawful
activities.
It is our policy, as published in the Federal Register on July 1,
1994 (59 FR 34272), to identify to the maximum extent practicable at
the time a species is listed, those activities that would or would not
constitute a violation of section 9 of the Act. The intent of this
policy is to increase public awareness of the effect of a proposed
listing on proposed and ongoing activities within the range of species
proposed for listing. The following activities could potentially result
in a violation of section 9 of the Act; this list is not comprehensive:
(1) Unauthorized collecting, handling, possessing, selling,
delivering, carrying, or transporting of the species, including import
or export across State lines and international boundaries, except for
properly documented antique specimens of these taxa at least 100 years
old, as defined by section 10(h)(1) of the Act;
(2) The unauthorized introduction of harmful nonnative species that
compete with or prey upon northern Mexican and narrow-headed
gartersnakes or their prey species, such as the stocking of nonnative,
predatory fish, or illegal transport, use, or release of bullfrogs or
crayfish in the States of Arizona and New Mexico;
(3) The unauthorized release of biological control agents that
attack any age class of northern Mexican and narrow-headed gartersnakes
or any life stage of their prey species;
(4) Unauthorized modification of the channel, reduction or
elimination of water flow of any stream or water body, or the complete
removal or significant destruction of riparian vegetation associated
with occupied northern Mexican or narrow-headed gartersnake habitat;
and
(5) Unauthorized discharge of chemicals or fill material into any
waters in which northern Mexican and narrow-headed gartersnakes are
known to occur.
Questions regarding whether specific activities would constitute a
violation of section 9 of the Act should be directed to the Arizona
Ecological Services Field Office (see FOR FURTHER INFORMATION CONTACT).
Requests for copies of the regulations concerning listed animals and
general inquiries regarding prohibitions and permits may be addressed
to the U.S. Fish and Wildlife Service, Endangered Species Permits, P.O.
Box 1306, Albuquerque, New Mexico 87103 (telephone (505) 248-6920,
facsimile (505) 248-6922).
Rule for the Northern Mexican Gartersnake Under Section 4(d) of the Act
The Act does not specify particular prohibitions, or exceptions to
those prohibitions, for threatened species. Instead, under section 4(d)
of the Act, the Secretary of the Interior has the discretion to issue
such regulations as she deems necessary and advisable to provide for
the conservation of such species. The Secretary also has the discretion
to prohibit by regulation with respect to any threatened species, any
act prohibited under section 9(a)(1) of the Act. Exercising this
discretion, the Service developed general prohibitions (50 CFR 17.31)
and exceptions to those prohibitions (50 CFR 17.32) under the Act that
apply to most threatened species. Alternately, for other threatened
species, the Service may develop specific prohibitions and exceptions
that are tailored to the specific conservation needs of the species. In
such cases, some of the prohibitions and authorizations under 50 CFR
17.31 and 17.32 may be appropriate for the species and incorporated
into a rule under section 4(d) of the Act. However, these rules, known
as 4(d) rules, will also include provisions that are tailored to the
specific conservation needs of the threatened species and may be more
or less restrictive than the general provisions at 50 CFR 17.31.
Provisions of the Section 4(d) Rule
Under section 4(d) of the Act, the Secretary may promulgate a
special rule that modifies the standard protections for threatened
species with measures tailored to the conservation of the species that
are determined to be necessary and advisable. Under this 4(d) rule, all
of the prohibitions under 50 CFR 17.31 and 17.32 will apply to the
northern Mexican gartersnake, except as discussed below. The 4(d) rule
will not remove or alter in any way the consultation requirements under
section 7 of the Act.
[[Page 38745]]
The creation, use, and maintenance of stock tanks are important
components of livestock grazing in the southwestern United States. A
stock tank (or livestock tank) is defined as an existing or future
impoundment in an ephemeral drainage or upland site (as opposed to an
active stream channel) constructed primarily as a watering site for
livestock. Well-managed stock tanks can provide important habitats for
northern Mexican gartersnakes and their prey base, especially when the
tank: (1) Remains devoid of harmful nonnative species while supporting
native prey species; (2) provides adequate vegetation cover for
predator aversion and prey base support; and (3) provides reliable
water sources in periods of prolonged drought. However, to create or
maintain these physical attributes of well-managed tanks, management
and maintenance can be necessary, which may have temporary negative
effects to these habitat attributes, but also long-term beneficial
effects to wildlife, including the northern Mexican gartersnake and its
prey. Therefore, the management of stock tanks is an important
consideration for northern Mexican gartersnakes.
The 4(d) rule allows for use of stock tanks by livestock and
construction, continued use, and maintenance of those stock tanks.
Stock tanks provide habitat for northern Mexican gartersnakes, and thus
their presence within the gartersnake's range provides a conservation
benefit to the species. This 4(d) rule allows landowners to construct
new stock tanks and to continue to use and maintain those stock tanks
on non-Federal lands without the need for Federal permitting or
oversight regarding compliance with the Act.
This provision may result in some harm or disturbance of individual
northern Mexican gartersnakes as a result of livestock or human
activities at the stock tanks; however, the level of disturbance is
expected to be minimal and outweighed by the benefit to the species
from the presence of these habitats that are provided by stock tanks.
Given the benefits of well-managed stock tanks, the presence of
well-managed stock tanks are an important component to northern Mexican
gartersnake conservation and recovery. This stock tank provision in the
4(d) rule allows for construction, continued use, and maintenance of
stock tanks on non-Federal lands, and, therefore, because of the
benefits associated with the habitat provided by well-managed stock
tanks, the 4(d) rule is necessary and advisable for the conservation of
the northern Mexican gartersnake.
Nothing in this 4(d) rule changes in any way the recovery planning
provisions of section 4(f) and consultation requirements under section
7 of the Act or the ability of the Service to enter into partnerships
for the management and protection of the northern Mexican gartersnake.
Livestock use and maintenance of stock tanks on Federal lands will be
addressed through the section 7 consultation process; this 4(d) rule
applies only to non-Federal lands.
4(d) Rule Determination
Section 4(d) of the Act states that ``the Secretary shall issue
such regulations as she deems necessary and advisable to provide for
the conservation'' of species listed as a threatened species.
Conservation is defined in the Act to mean ``to use and the use of all
methods and procedures which are necessary to bring any endangered
species or threatened species to the point at which the measures
provided pursuant to (the Act) are no longer necessary.'' Additionally,
section 4(d) states that the Secretary ``may by regulation prohibit
with respect to any threatened species any act prohibited under section
9(a)(1).''
The courts have recognized the extent of the Secretary's discretion
under this standard to develop rules that are appropriate for the
conservation of a species. For example, the Secretary may find that it
is necessary and advisable not to include a taking prohibition, or to
include a limited taking prohibition. See Alsea Valley Alliance v.
Lautenbacher, 2007 U.S. Dist. Lexis 60203 (D. Or. 2007); Washington
Environmental Council v. National Marine Fisheries Service, and 2002
U.S. Dist. Lexis 5432 (W.D. Wash. 2002). In addition, as affirmed in
State of Louisiana v. Verity, 853 F.2d 322 (5th Cir. 1988), the rule
need not address all the threats to the species. As noted by Congress
when the Act was initially enacted, ``once an animal is on the
threatened list, the Secretary has an almost infinite number of options
available to her with regard to the permitted activities for those
species.'' She may, for example, permit taking, but not importation of
such species, or she may choose to forbid both taking and importation
but allow the transportation of such species, as long as the measures
will ``serve to conserve, protect, or restore the species concerned in
accordance with the purposes of the Act'' (H.R. Rep. No. 412, 93rd
Cong., 1st Sess. 1973).
Section 9 prohibitions make it illegal for any person subject to
the jurisdiction of the United States to take (including harass, harm,
pursue, shoot, wound, kill, trap, capture, or collect; or attempt any
of these), import or export, ship in interstate commerce in the course
of commercial activity, or sell or offer for sale in interstate or
foreign commerce any wildlife species listed as an endangered species,
without written authorization. It also is illegal under section 9(a)(1)
of the Act to possess, sell, deliver, carry, transport, or ship any
such wildlife that is taken illegally. Prohibited actions consistent
with section 9 of the Act are outlined for threatened species in 50 CFR
17.31(a) and (b). This 4(d) rule applies all of the prohibitions in 50
CFR 17.31(a) and (b) to the northern Mexican gartersnake, except
activities on non-Federal lands that are incidental to construction,
continued use, and maintenance of stock tanks. Based on the rationale
explained above, the provisions included in this 4(d) rule are expected
to contribute to the conservation of the northern Mexican gartersnake
and are, therefore, necessary and advisable to provide for the
conservation of the northern Mexican gartersnake.
Required Determinations
National Environmental Policy Act (42 U.S.C. 4321 et seq.)
We have determined that environmental assessments and environmental
impact statements, as defined under the authority of NEPA, need not be
prepared in connection with listing a species as an endangered or
threatened species under the Act. We published a notice outlining our
reasons for this determination in the Federal Register on October 25,
1983 (48 FR 49244). As documented in the Service's Endangered Species
Listing Handbook (Service 1994), it is the position of the Service that
rules promulgated under section 4(d) of the Act concurrently with
listing of the species fall under the same rationale as outlined in the
October 25, 1983, determination; thus preparation of an environmental
assessment for the 4(d) rule is not required.
Government-to-Government Relationship With Tribes
In accordance with the President's memorandum of April 29, 1994
(Government-to-Government Relations with Native American Tribal
Governments; 59 FR 22951), Executive Order 13175 (Consultation and
Coordination with Indian Tribal Governments), and the Department of the
Interior's manual at 512 DM 2, we readily acknowledge our
responsibility
[[Page 38746]]
to communicate meaningfully with recognized Federal Tribes on a
government-to-government basis. In accordance with Secretarial Order
3206 of June 5, 1997 (American Indian Tribal Rights, Federal-Tribal
Trust Responsibilities, and the Endangered Species Act), we readily
acknowledge our responsibilities to work directly with tribes in
developing programs for healthy ecosystems, to acknowledge that tribal
lands are not subject to the same controls as Federal public lands, to
remain sensitive to Indian culture, and to make information available
to tribes.
Native American tribes potentially affected by the listing of these
two gartersnakes include the San Carlos Apache Tribe, White Mountain
Apache Tribe, and Yavapai Apache Tribe. On March 12, 2013, we mailed
correspondence to these three tribes to request to meet with each tribe
to discuss our listing recommendations for the gartersnakes. We met
with representatives of the San Carlos Apache Tribe on May 1, 2013, and
no concerns regarding the proposed listings were noted. We held a
government-to-government meeting with the White Mountain Apache Tribe
on September 27, 2013, to discuss the gartersnake listing
recommendations, and we agreed to review their Native Fish Management
Plan for conservation benefit to proposed and listed aquatic vertebrate
species that occur on their lands. We provided comments on that plan
during a conference call discussion on December 16, 2013. The Yavapai
Apache Tribe did not have any comments on the proposed gartersnake
listings.
References Cited
A complete list of references cited in this rulemaking is available
on the Internet at https://www.regulations.gov and upon request from the
Arizona Ecological Services Field Office (see FOR FURTHER INFORMATION
CONTACT).
Authors
The primary authors of this final rule are the staff members of the
Arizona Ecological Services Field Office.
List of Subjects in 50 CFR Part 17
Endangered and threatened species, Exports, Imports, Reporting and
recordkeeping requirements, Transportation.
Regulation Promulgation
Accordingly, we amend part 17, subchapter B of chapter I, title 50
of the Code of Federal Regulations, as follows:
PART 17--[AMENDED]
0
1. The authority citation for part 17 continues to read as follows:
Authority: 16 U.S.C. 1361-1407; 1531-1544; and 4201-4245,
unless otherwise noted.
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2. Amend Sec. 17.11(h) by adding entries for ``Gartersnake, narrow-
headed'' and ``Gartersnake, northern Mexican'' to the List of
Endangered and Threatened Wildlife in alphabetical order under Reptiles
to read as follows:
Sec. 17.11 Endangered and threatened wildlife.
* * * * *
(h) * * *
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Species Vertebrate
------------------------------------------------ population where Critical
Historic range endangered or Status When listed habitat Special rules
Common name Scientific name threatened
--------------------------------------------------------------------------------------------------------------------------------------------------------
* * * * * * *
Reptiles.....................
* * * * * * *
Gartersnake, narrow-headed... Thamnophis U.S.A. (AZ, NM). Entire.......... T............... ............... NA............. NA.
rufipunctatus.
Gartersnake, northern Mexican Thamnophis eques U.S.A. (AZ, NM), Entire.......... T............... ............... NA............. 17.42(g).
megalops. Mexico.
* * * * * * *
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3. Amend Sec. 17.42 by adding a new paragraph (g) to read as follows:
Sec. 17.42 Special rules--reptiles.
* * * * *
(g) Northern Mexican gartersnake (Thamnophis eques megalops). (1)
Prohibitions. Except as noted in paragraph (g)(2) of this section, all
prohibitions and provisions of Sec. Sec. 17.31 and 17.32 apply to the
northern Mexican gartersnake.
(2) Exemptions from prohibitions. Incidental take of the northern
Mexican gartersnake will not be considered a violation of section 9 of
the Act if the take occurs on non-Federal land and is incidental to
activities pertaining to construction, continued use, and maintenance
of stock tanks. A stock tank is an existing or future impoundment in an
ephemeral drainage or upland site constructed primarily as a watering
site for livestock.
Dated: June 9, 2014.
Stephen Guertin,
Acting Director, U.S. Fish and Wildlife Service.
[FR Doc. 2014-14615 Filed 7-7-14; 8:45 am]
BILLING CODE 4310-55-P
