Endangered and Threatened Wildlife and Plants; 12-Month Finding on a Petition To List the Northern Mexican Gartersnake (Thamnophis eques megalops) as Threatened or Endangered With Critical Habitat, 56228-56256 [06-7784]
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FOR FURTHER INFORMATION CONTACT:
DEPARTMENT OF THE INTERIOR
Steve Spangle, Field Supervisor,
Arizona Ecological Services Office (see
ADDRESSES) 602–242–0210.
SUPPLEMENTARY INFORMATION:
Fish and Wildlife Service
50 CFR Part 17
Endangered and Threatened Wildlife
and Plants; 12-Month Finding on a
Petition To List the Northern Mexican
Gartersnake (Thamnophis eques
megalops) as Threatened or
Endangered With Critical Habitat
Fish and Wildlife Service,
Interior.
ACTION: Notice of 12-month petition
finding.
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AGENCY:
SUMMARY: We, the U.S. Fish and
Wildlife Service (Service), announce a
12-month finding on a petition to list
the northern Mexican gartersnake
(Thamnophis eques megalops) as
threatened or endangered with critical
habitat under the Endangered Species
Act of 1973, as amended (Act). The
petitioners provided three listing
scenarios for consideration by the
Service: (1) Listing the United States
population as a Distinct Population
Segment (DPS); (2) listing Thamnophis
eques megalops throughout its range in
the United States and Mexico based on
its rangewide status; or (3) listing
Thamnophis eques megalops
throughout its range in the United States
and Mexico based on its status in the
United States. After thorough analysis
and review of all available scientific and
commercial information, we find that
listing of the subspecies, under any of
the three scenarios, is not warranted. Of
the three listing scenarios specified
above, we found scenario two provided
the most rigorous evaluation of the
status of the northern Mexican
gartersnake and herein provide detailed
discussion of our conclusions in that
context. We also provide additional
discussion of our evaluation of
scenarios (1) listing the United States
population as a DPS and (3) listing
Thamnophis eques megalops
throughout its range in the United States
and Mexico based on its status in the
United States.
DATES: The finding announced in this
document was made on September 26,
2006.
ADDRESSES: The complete supporting
file for this finding is available for
inspection, by appointment, during
normal business hours at the Arizona
Ecological Services Office, 2321 West
Royal Palm Road, Suite 103, Phoenix,
AZ 85021–4951. Please submit any new
information, materials, comments, or
questions concerning this species or this
finding to the above address.
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Background
Section 4(b)(3)(B) of the Act (16
U.S.C. 1531 et seq.), requires that, for
any petition to revise the Lists of
Threatened and Endangered Wildlife
and Plants that contains substantial
scientific and commercial information
that listing may be warranted, we make
a finding within 12 months of the date
of receipt of the petition on whether the
petitioned action is (a) not warranted,
(b) warranted, or (c) warranted, but that
the immediate proposal of a regulation
implementing the petitioned action is
precluded by other pending proposals to
determine whether any species is
threatened or endangered, and
expeditious progress is being made to
add or remove qualified species from
the Lists of Endangered and Threatened
Wildlife and Plants. Section 4(b)(3)(C) of
the Act requires that a petition for
which the requested action is found to
be warranted but precluded be treated
as though resubmitted on the date of
such finding, i.e., requiring a
subsequent finding to be made within
12 months. Each subsequent 12-month
finding will be published in the Federal
Register.
On December 19, 2003, we received a
petition dated December 15, 2003,
requesting that we list the northern
Mexican gartersnake as threatened or
endangered, and that we designate
critical habitat concurrently with the
listing. The petition, submitted by the
Center for Biological Diversity, was
clearly identified as a petition for a
listing rule and contained the names,
signatures, and addresses of the
requesting parties. Included in the
petition was supporting information
regarding the species’ taxonomy and
ecology, historical and current
distribution, present status, and actual
and potential causes of decline. We
acknowledged the receipt of the petition
in a letter to Mr. Noah Greenwald, dated
March 1, 2004. In that letter, we also
advised the petitioners that, due to
funding constraints in fiscal year (FY)
2004, we would not be able to begin
processing the petition at that time.
On May 17, 2005, the petitioners filed
a complaint for declaratory and
injunctive relief, challenging our failure
to issue a 90-day finding in response to
the petition as required by 16 U.S.C.
1533(b)(3)(A) and (B). In a stipulated
settlement agreement, we agreed to
submit a 90-day finding to the Federal
Register by December 16, 2005, and if
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positive, submit a 12-month finding to
the Federal Register by September 15,
2006 [Center for Biological Diversity v.
Norton, CV–05–341–TUC–CKJ (D. Az)].
The settlement agreement was signed
and adopted by the District Court of
Arizona on August 2, 2005.
On December 13, 2005, we made our
90-day finding that the petition
presented substantial scientific
information indicating that listing the
northern Mexican gartersnake
(Thamnophis eques megalops) may be
warranted, but we did not discuss the
applicability of any of the three listing
scenarios that were provided in the
petition. The finding and our initiation
of a status review was published in the
Federal Register on January 4, 2006 (71
FR 315). We are required, under the
court-approved stipulated settlement
agreement, to submit to the Federal
Register our 12-month finding pursuant
to the Act [16 U.S.C. 1533(b)(3)(B)] on
or before September 15, 2006. This
notice constitutes our 12-month finding
for the petition to list the northern
Mexican gartersnake as threatened or
endangered.
Previous Federal Actions
The Mexican gartersnake
(Thamnophis eques) (which included
the subspecies) was placed on the list of
candidate species as a Category 2
species in 1985 (50 FR 37958). Category
2 species were those for which existing
information indicated that listing was
possibly appropriate, but for which
substantial supporting biological data to
prepare a proposed rule were lacking. In
the 1996 Candidate Notice of Review
(February 28, 1996; 61 FR 7596), the use
of Category 2 candidates was
discontinued, and the northern Mexican
gartersnake was no longer recognized as
a candidate. In addition, on January 4,
2006, we published a 90-day finding on
a petition to list the northern Mexican
gartersnake (71 FR 315), as discussed
above.
Biology
Species Description. The northern
Mexican gartersnake may occur with
other native gartersnake species and can
be difficult for people without
herpetological expertise to identify.
With a maximum known length of 44
inches (in) (112 centimeters (cm)), it
ranges in background color from olive to
olive-brown to olive-gray with three
stripes that run the length of the body.
The middle dorsal stripe is yellow and
darkens toward the tail. The pale yellow
to light-tan lateral stripes distinguish
the Mexican gartersnake from other
sympatric (co-occurring) gartersnake
species because a portion of the lateral
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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 and the olive-gray ventrolateral
fields. A conspicuous, light-colored
crescent extends behind the corners of
the mouth. The two dark brown to black
blotches that occur behind the head of
several gartersnake species may be
diffuse or absent in the Mexican
gartersnake. The coloration of the venter
is bluish-gray or greenish-grey. The
dorsolateral scalation is keeled, the anal
plate is single, and there are eight or
nine upper labial scales (Rosen and
Schwalbe 1988, p. 4; Rossman et al.
1996, pp. 171–172).
Taxonomy. The northern Mexican
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), but
also 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 that have been
described in the gartersnake genus
Thamnophis (Rossman et al. 1996, p.
xvii–xviii). De Queiroz et al. (2002, p.
323) identified two large overlapping
clades (related taxonomic groups) of
gartersnakes that they called the
‘‘Mexican’’ and ‘‘widespread’’ clades
which were supported by allozyme and
mitochondrial DNA genetic analyses.
Thamnophis eques is a member of the
‘‘widespread’’ clade and is most closely
related taxonomically to, although
genetically and phenotypically distinct
from, the checkered gartersnake
(Thamnophis marcianus) (De Queiroz
and Lawson 1994, p. 217).
Rossman et al. (1996, p. 175) noted
that the current specific name eques was
not applied at the time of the original
description of the holotype because the
specimen was mistakenly identified as a
black-necked gartersnake (Thamnophis
cyrtopsis). In recent history and 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). T. eques displays considerable
phenotypic variability (variation in its
physical appearance) across its
distribution, and all subspecific
descriptions under T. eques have been
based on morphometrics or
morphological characters. The
subspecies T. e. eques and T. e.
megalops are distinguished by average
differences in sub-caudal scale counts,
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while T. e. virgatenuis is distinguished
from T. e. megalops based on having a
darker background color and a narrower
vertebral stripe (Rossman et al. 1996, p.
175). Rossman et al. (1996, p. 175) also
noted that the discontinuous
distributions of high-elevation and lowelevation T. e. virgatenuis and T. e.
megalops, respectively, are
‘‘zoogeographically peculiar and unique
among gartersnakes.’’
Rossman et al. (1996, p. 172) describe
the distribution of T. e. eques as
occurring from southern Nayarit
eastward along the Transverse Volcanic
Axis to west-central Veracruz, and
identified an additional disjunct
population in central Oaxaca. T. e.
virgatenuis is distributed in three
isolated, high-elevation populations in
southwestern Durango and in westcentral and northwestern Chihuahua
(Rossman et al. 1996, p. 172).
In 2003, an additional seven new
subspecies were identified under T.
eques: (1) T. e. cuitzeoensis; (2) T. e.
patzcuaroensis; (3) T. e. inspiratus; (4)
T. e. obscurus; (5) T. e. diluvialis; (6) T.
e. carmenensis; and (7) T. e. scotti
(Conant 2003, p. 3). These seven new
subspecies were described based on
morphological differences in coloration
and pattern; have high endemism
(degree of restriction to a particular
area) with 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). We are not
aware of any challenges within the
scientific literature of the validity of
current taxonomy of any of the 10
subspecies of T. eques.
The most widely distributed of the 10
subspecies under Thamnophis eques is
the northern Mexican gartersnake
(Thamnophis eques megalops), which is
the only subspecies that occurs in the
United States and the entity we address
in this finding. In Mexico, T. e.
megalops historically occurred
throughout the Sierra Madre Occidental
south to Guanajuato, and east across the
Mexican Plateau to Hidalgo, which
comprised approximately 85 percent of
the total rangewide distribution of the
species (Rossman et al. 1996, p. 173).
Robert Kennicott first described the
northern Mexican gartersnake in 1860,
as Eutenia megalops from the type
locality of Tucson, Arizona (Rosen and
Schwalbe 1988, p. 2). In 1951, Dr.
Hobart Smith renamed the subspecies
with its current scientific name (Rosen
and Schwalbe 1988, p. 3). A summary
of this species’ lengthy taxonomic
history can be found in Rosen and
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Schwalbe (1988, pp. 2–3). Several
common names have been applied to
the northern Mexican gartersnake in the
United States over the years, such as the
Arizona ribbon snake, the Emory’s
gartersnake, and the Arizona gartersnake
(Rosen and Schwalbe 1988, p. 2).
In summary, while the taxonomic
history of Thamnophis eques is robust,
we found no indication in the
significant body of taxonomic literature
we reviewed that its current taxonomy
is in doubt or in any way invalid (Rosen
and Schwalbe 1988, pp. 2–3; De Queiroz
and Lawson 1994, pp. 215–217; Liner
1994, p. 107; Rossman et al. 1996, pp.
171, 175; Conant 2003, p. 6; Crother et
al. 2000, p. 72; 2003, p. 202; De Queiroz
et al. 2002, p. 327).
Habitat. 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). The
northern Mexican gartersnake is
considered a riparian obligate (restricted
to riparian areas when not engaged in
dispersal behavior) and occurs chiefly
in the following general habitat types:
(1) Source-area wetlands [e.g., cienegas
(mid-elevation wetlands with highly
organic, reducing (basic, or alkaline)
soils), stock tanks (small earthen
impoundment), etc.]; (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; Arizona Game and Fish Department
2001). Vegetation characteristics vary
based on the type of habitat. For
example, in source-area wetlands, dense
vegetation consists of knot grass
(Paspalum distichum), spikerush
(Eleocharis), bulrush (Scirpus), cattail
(Typha), deergrass (Muhlenbergia),
sacaton (Sporobolus), Fremont
cottonwood (Populus fremontii),
Goodding’s willow (Salix gooddingii),
and velvet mesquite (Prosopis velutina)
(Rosen and Schwalbe 1988, pp. 14–16).
In riparian woodlands consisting of
cottonwood and willow or gallery
forests of broadleaf and deciduous
species along larger rivers, the northern
Mexican gartersnake may be observed in
mixed grasses along the bank or in the
shallows (Rossman et al. 1996, p. 176;
Rosen and Schwalbe 1988, p. 16).
Within and adjacent to the Sierra Madre
Occidental in Mexico, it occurs in
montane woodland, Chihuahuan
desertscrub, mesquite-grassland, and
´
Cordillera Volcanica montane woodland
(McCranie and Wilson 1987, pp. 14–17).
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In small streamside riparian habitat,
this snake is often associated with
Arizona sycamore (Platanus wrightii),
sugar leaf maple (Acer grandidentatum),
velvet ash (Fraxinus velutina), Arizona
cypress (Cupressus arizonica), Arizona
walnut (Juglans major), Arizona alder
(Alnus oblongifolia), alligator juniper
(Juniperus deppeana), Rocky Mountain
juniper (J. scopulorum), and a number
of oak species (Quercus spp.) (McCranie
and Wilson 1987, pp. 11–12; CirettGalan 1996, p. 156).
Behavior, Prey Base, and
Reproduction. The northern Mexican
gartersnake is surface active at ambient
temperatures ranging from 71 degrees
Fahrenheit (°F) to 91 °F [22 degrees
Celsius (°C) to 33 °C] and forages along
the banks of waterbodies. The northern
Mexican gartersnake is an active
predator and is believed to heavily
depend upon a native prey base (Rosen
and Schwalbe 1988, pp. 18, 20).
Generally, its diet consists
predominantly of amphibians and
fishes, such as adult and larval native
leopard frogs [e.g., lowland leopard frog
(Rana yavapaiensis) and Chiricahua
leopard frog (Rana 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 Schwalbe 1988, p.
18). Auxiliary prey items may also
include young Woodhouse’s toads (Bufo
woodhousei), treefrogs (Family Hylidae),
earthworms, deermice (Peromyscus
maniculatus), 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). To
a much lesser extent, this snake’s diet
may include nonnative species,
including juvenile fish, larval and
juvenile bullfrogs, and mosquitofish
(Gambusia affinis) (Holycross et al.
2006, p. 23).
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 ovoviviparous (eggs develop and
hatch within the oviduct of the female).
Mating occurs in April and May in their
northern distribution followed by the
live birth of between 7 and 26 neonates
(newly born individuals) (average is
13.6) in July and August (Rosen and
Schwalbe 1988, p. 16). Approximately
half of the sexually mature females
within a population reproduce in any
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one season (Rosen and Schwalbe 1988,
p. 17).
Distribution
Historical Distribution. The United
States comprises the northern portion of
the northern Mexican gartersnake’s
distribution. Within the United States,
the northern Mexican gartersnake
historically occurred predominantly in
Arizona with a limited distribution in
New Mexico that consisted of scattered
locations throughout the Gila and San
Francisco headwater drainages in
western Hidalgo and Grant counties
(Price 1980, p. 39; Fitzgerald 1986,
Table 2; Degenhardt et al. 1996, p. 317;
Holycross et al. 2006, pp. 1–2).
Fitzgerald (1986, Table 2) provided
museum records for the following
historical localities for northern
Mexican gartersnakes in New Mexico:
(1) Mule Creek; (2) the Gila River, 5
miles (mi) ( 8 kilometers (km)) east of
Virden; (3) Spring Canyon; (4) the West
Fork Gila River at Cliff Dwellings
National Monument; (5) the Tularosa
River at its confluence with the San
Francisco River; (6) the San Francisco
River at Tub Spring Canyon; (7) Little
Creek at Highway 15; (8) the Middle Box
of Gila River at Ira Ridge; (9) Turkey
Creek; (10) Negrito Creek; and (11) the
Rio Mimbres.
Within Arizona, the historical
distribution of the northern Mexican
gartersnake ranged from 130 to 6,150 ft
(40 to 1,875 m) in elevation and spread
variably based on the relative
permanency of water and the presence
of suitable habitat. In Arizona, the
northern Mexican gartersnake
historically occurred within several
perennial or intermittent drainages and
disassociated wetlands that included:
(1) The Gila River; (2) the Lower
Colorado River from Davis Dam to the
International Border; (3) the San Pedro
River; (4) the Santa Cruz River
downstream from the International
Border; (5) the Santa Cruz River
headwaters/San Rafael Valley and
adjacent montane canyons; (6) the Salt
River; (7) the Rio San Bernardino from
International Border to headwaters at
Astin Spring (San Bernardino National
Wildlife Refuge); (8) Agua Fria River; (9)
the Verde River; (10) Tanque Verde
Creek in Tucson; (11) Rillito Creek in
Tucson; (12) Agua Caliente Spring in
Tucson; (13) the downstream portion of
the Black River from the Paddy Creek
confluence; (14) the downstream
portion of the White River from the
confluence of the East and North forks;
(15) Tonto Creek from the mouth of
Houston Creek downstream to Roosevelt
Lake; (16) Cienega Creek from the
headwaters to the ‘‘Narrows’’ just
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downstream of Apache Canyon; (17)
Pantano Wash (Cienega Creek) from
Pantano downstream to Vail; (18)
Potrero Canyon/Springs; (19) Audubon
Research Ranch and vicinity near Elgin;
(20) Upper Scotia Canyon in the
Huachuca Mountains; (21) Arivaca
Creek; (22) Arivaca Cienega; (23)
Sonoita Creek; (24) Babocomari River;
(25) Babocamari Cienega; (26) Barchas
Ranch, Huachuca Mountain bajada; (27)
Parker Canyon Lake and tributaries in
the Canelo Hills; (28) Big Bonito Creek;
(29) Lake O’Woods, Lakeside area; (30)
Oak Creek from Midgley Bridge
downstream to the confluence with the
Verde River; and (31) Spring Creek
above the confluence with Oak Creek
(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; Rosen 2006;
Holycross 2006).
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 (De Queiroz and Smith 1996, p.
155); however, any populations of
northern Mexican gartersnakes that may
have historically occurred in Nevada
pertained directly to the Colorado River
and are likely extirpated.
Within Mexico, northern Mexican
gartersnakes historically occurred
within the Sierra Madre Occidental and
the Mexican Plateau in the Mexican
states of Sonora, Chihuahua, Durango,
Coahila, Zacatecas, Guanajuato, Nayarit,
´
Hidalgo, Jalisco, San Luis Potosı,
Aguascalientes, Tlaxacala, Puebla,
´
´
Mexico, Veracruz, and Queretaro, which
comprises approximately 70 to 80
percent of its historical rangewide
distribution (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).
Status in the United States. Holycross
et al. (2006, p. 12) included the northern
Mexican gartersnake as a target species
at 33 sites surveyed within drainages
along the Mogollon Rim. A total of 874
person-search hours and 63,495 traphours were devoted to that effort, which
resulted in the capture of 23 snakes total
in 3 (9 percent) of the sites visited. This
equates to approximately 0.03 snakes
observed per person-search hour and
0.0004 snakes captured per trap-hour
over the entire effort. For comparison, a
population of northern Mexican
gartersnakes at Page Springs, Arizona,
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that we consider stable yielded 0.22
snakes observed per person-search hour
and 0.004 snakes captured per trap-hour
(an order of magnitude higher)
(Holycross et al. 2006, p. 23). Survey
sites were selected based on the
existence of historical records for the
species or sites where the species may
occur based on habitat suitability within
the historical distribution of the species.
Holycross et al. (2006, p. 12) calculated
the capture rates for the northern
Mexican gartersnake as 12,761 traphours per snake and 49 person-search
hours per snake. Northern Mexican
gartersnakes were found at 2 of 11 (18
percent) historical sites and 1 of 22 (4
percent) sites where the species was
previously unrecorded (Holycross et al.
2006, p. 12). When compared with
extensive survey data in Rosen and
Schwalbe (1988, Appendix I), these data
demonstrate dramatic declines in both
capture rates and the total number of
populations of the species in areas
where multiple surveys have been
completed over time. However, these
data may be affected by differences in
survey efforts and drought.
In 2000, Rosen et al. (2001, Appendix
I) resurveyed many sites in southeastern
Arizona that were historically known to
support northern Mexican gartersnake
populations during the early to mid1980s, and also provided additional
survey data collected from 1993–2001.
Rosen et al. (2001, pp. 21–22) reported
their results in terms of increasing,
stabilized, or decreasing populations of
northern Mexican gartersnakes.
Three sites (San Bernardino National
Wildlife Refuge, Finley Tank at the
Audubon Research Ranch near Elgin,
and Scotia Canyon in the Huachuca
Mountains) were intensively surveyed
and yielded mixed results. The northern
Mexican gartersnake population on the
San Bernardino National Wildlife
Refuge experienced ‘‘major,
demonstrable declines’’ to near or at
extirpation over the span of a decade.
That population is now considered
extirpated (Radke 2006). The status of
the population at Finley Tank is
uncertain. Scotia Canyon was the last
area intensively resurveyed by Rosen et
al. (2001, pp. 15–16). In comparing this
information with survey data from Holm
and Lowe (1995, pp. 27–35), northern
Mexican gartersnake populations in this
area suggest a possible decline from the
early 1980s, as evidenced by low
capture rates in 1993 and even lower
capture rates in 2000.
The remaining 13 sites in
southeastern Arizona resurveyed by
Rosen et al. (2001, pp. 21–22) also
yielded mixed results. Population trend
information is difficult to ascertain
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given the variability of survey sample
design and effort used by Rosen et al.
(2001). However, the survey results
suggested population increases at one
site (lower Cienega Creek), possible
stability at two sites (lower San Rafael
Valley, Arivaca), and negative trends at
many other sites [Empire-Cienega Creek,
Babocomari, Bog Hole, O’Donnell Creek,
Turkey Creek (Canelo), Post Canyon,
Lewis Springs (San Pedro River), San
Pedro River near Highway 90, Barchas
Ranch Pond (Huachuca Mountain
bajada), Heron Spring, Sharp Spring,
and Elgin-Sonoita windmill well site
(San Rafael Valley)] (Rosen et al. 2001,
pp. 21–22). While this survey effort
could not confirm any specific
extirpations of northern Mexican
gartersnake populations on a local scale
in southeastern Arizona, most sites
yielded no snakes during resurvey
(Rosen et al. 2001, Appendix I).
Our analysis of the best available data
on the status of the northern Mexican
gartersnake distribution in the United
States indicates that its distribution has
been significantly reduced in the United
States, and it is now considered
extirpated from New Mexico (Nickerson
and Mays 1970, p. 503; Rosen and
Schwalbe 1988, pp. 25–26, Appendix I;
Holm and Lowe 1995, pp. 27–35; Sredl
et al. 1995b, pp. 2, 9–10; 2000, p. 9;
Rosen et al. 2001, Appendix I; Painter
2005, 2006; Holycross et al. 2006, p. 66;
Brennan and Holycross 2006, p. 123;
Radke 2006; Rosen 2006; Holycross
2006). Fitzgerald (1986, pp. 9–10)
visited 33 localities of potential habitat
for northern Mexican gartersnakes in
New Mexico in the Gila River drainage
and was unable to confirm its existence
at any of these sites. The New Mexico
Department of Game and Fish State
Herpetologist, Charles Painter, provided
several causes that have synergistically
contributed to the decline of northern
Mexican gartersnakes in New Mexico,
including bullfrog and nonnative fish
introductions, modification and
destruction of habitat, commercial
exploitation, direct human-inflicted
harm, and fragmentation of populations.
The last known observation of the
northern Mexican gartersnake in New
Mexico occurred in 1994 on private
land (Painter 2000, p. 36; Painter 2005).
Our analysis of the best available
information indicates that the northern
Mexican gartersnake has likely been
extirpated from a large portion of its
historical distribution in the United
States. We define a population as
‘‘likely extirpated’’ when there have
been no northern Mexican gartersnakes
reported for a decade or longer at a site
within the historical distribution of the
species, despite at least minimal survey
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56231
efforts, and natural recovery at the site
is not expected due to the presence of
known threats. The perennial or
intermittent stream reaches and
disassociated wetlands where the
northern Mexican gartersnake has likely
been extirpated include: (1) The Gila
River; (2) the Lower Colorado River
from Davis Dam to the International
Border; (3) the San Pedro River; (4) the
Santa Cruz River downstream from the
International Border at Nogales; (5) the
Salt River; (6) the Rio San Bernardino
from International Border to headwaters
at Astin Spring (San Bernardino
National Wildlife Refuge); (7) the Agua
Fria River; (8) the Verde River upstream
of Clarkdale; (9) the Verde River from
the confluence with Fossil Creek
downstream to its confluence with the
Salt River; (10) Tanque Verde Creek in
Tucson; (11) Rillito Creek in Tucson;
(12) Agua Caliente Spring in Tucson;
(13) Potrero Canyon/Springs; (14)
Babocamari Cienega; (15) Barchas
Ranch, Huachuca Mountain bajada; (16)
Parker Canyon Lake and tributaries in
the Canelo Hills; and (17) Oak Creek at
Midgley Bridge (Rosen and Schwalbe
1988, pp. 25–26, Appendix I; 1997, pp.
16–17; Rosen et al. 2001, Appendix I;
Brennan and Holycross 2006, p. 123;
Holycross 2006; Holycross et al. 2006,
pp. 15–51, 66; Radke 2006; Rosen 2006).
Information pertaining to the cause or
causes of extirpation of these sites is
summarized in Table 1 below.
Conversely, our review of the best
available information indicates the
northern Mexican gartersnake is likely
extant in a fraction of its historical range
in Arizona. We define populations as
‘‘likely extant’’ when the species is
expected to reliably occur in
appropriate habitat as supported by
recent museum records and/or recent
(i.e., less than 10 years) reliable
observations. The perennial or
intermittent stream reaches and
disassociated wetlands where we
conclude northern Mexican gartersnakes
remain extant include: (1) The Santa
Cruz River/Lower San Rafael Valley
(headwaters downstream to the
International Border); (2) the Verde
River from the confluence with Fossil
Creek upstream to Clarkdale; (3) Oak
Creek at Page Springs; (4) Tonto Creek
from the mouth of Houston Creek
downstream to Roosevelt Lake; (5)
Cienega Creek from the headwaters
downstream to the ‘‘Narrows’’ just
downstream of Apache Canyon; (6)
Pantano Wash (Cienega Creek) from
Pantano downstream to Vail; (7) Upper
Scotia Canyon in the Huachuca
Mountains; and (8) the Audubon
Research Ranch and vicinity near Elgin
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(Rosen et al. 2001, Appendix I; Caldwell
2005; Brennan and Holycross 2006, p.
123; Holycross 2006; Holycross et al.
2006, pp. 15–51, 66; Rosen 2006).
The current status of the northern
Mexican gartersnake is unknown in
several areas in Arizona where the
species is known to have historically
occurred. We base this determination on
mostly historical museum records for
locations where survey access is
restricted, survey data are unavailable or
insufficient, and/or current threats
could preclude occupancy. The
perennial or intermittent stream reaches
and disassociated wetlands where the
status of the northern Mexican
gartersnake remains uncertain include:
(1) The downstream portion of the Black
River drainage from the Paddy Creek
confluence; (2) the downstream portion
of the White River drainage from the
confluence of the East and North forks;
(3) Big Bonito Creek; (4) Lake O’Woods
near Lakeside; (5) Spring Creek above
the confluence with Oak Creek; (6) Bog
Hole Wildlife Area; (7) Upper 13 Tank,
Patagonia Mountain bajada; (8)
Babocamari River; and (9) Arivaca
Cienega (Rosen and Schwalbe 1988,
Appendix I; Rosen et al. 2001,
Appendix I; Brennan and Holycross
2006, p. 123; Holycross 2006; Holycross
et al. 2006, pp. 15–51; Rosen 2006).
In summary, after consultation with
species’ experts and land managers, and
based upon our analysis of the best
available scientific and commercial
data, we conclude that the northern
Mexican gartersnake has been extirpated
from 85 to 90 percent of its historical
distribution in the United States.
Status in Mexico. Throughout this
finding, and due to the significantly
limited amount of available literature
that addresses the status of and threats
to extant populations of the northern
Mexican gartersnake in Mexico, we rely
in part on (1) information that addresses
the status of and threats to both riparian
and aquatic biological communities
within the historical distribution of the
northern Mexican gartersnake in
Mexico; and (2) information that
addresses the status of and threats to
native freshwater fish within the
historical distribution of the northern
Mexican gartersnake in Mexico, which
we use as ecological surrogates due to
their similar habitat requirements and
their role as important prey species
utilized by the northern Mexican
gartersnake. Observations on the status
of riparian and aquatic communities in
Mexico are available but limited in
comparison to our knowledge of these
communities in the United States. The
current distribution of the northern
Mexican gartersnake in Mexico is also
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not well understood, although its status
is believed to be in decline in many
areas due to historical and continuing
threats to its habitat and prey base, as
discussed below. A large number of
springs have dried up in several
Mexican states within the distribution
of the northern Mexican gartersnake,
namely, Chihuahua, Durango, Coahila,
´
and San Luis Potosı (Contreras Balderas
and Lozano 1994, p. 381). Contreras
Balderas and Lozano (1994, p. 381) also
stated that several streams and rivers
throughout Mexico and within the
distribution of the northern Mexican
gartersnake have dried up or become
intermittent due to overuse of surface
and groundwater supplies. We further
acknowledge that northern Mexican
gartersnakes were historically
distributed in several regions within
Mexico that have remained roadless and
isolated and, according to the
information we were able to obtain
regarding the status of the northern
Mexican gartersnake in Mexico, few
ecological investigations have occurred
in these areas due to their remote nature
and the logistical difficulties that face
research in such areas. However,
Mexican biologists Ramirez Bautista and
Arizmendi (2004, p. 3) were able to
provide general information on the
principal threats to northern Mexican
gartersnake habitat in Mexico which
included the dessication of wetlands,
improper livestock grazing,
deforestation, wildfires, and
urbanization. In addition, nonnative
species, such as bullfrogs and sport and
bait 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).
Given the lack of specific data on the
status of the northern Mexican
gartersnake in Mexico, we cannot
conclude with any degree of certainty
its overall status in Mexico.
Northern Mexican Gartersnake Distinct
Population Segment
In the petition to list the northern
Mexican gartersnake, the petitioners
specified several listing options for our
consideration, including listing
northern Mexican gartersnake in the
United States as a DPS. Under the Act,
we must consider for listing any species,
subspecies, or DPSs of vertebrate
species/subspecies, if information is
sufficient to indicate that such action
may be warranted. To implement the
measures prescribed by the Act and its
Congressional guidance, we developed a
joint policy with the National Oceanic
and Atmospheric Administration
(NOAA) Fisheries entitled Policy
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Regarding the Recognition of Distinct
Vertebrate Population (DPS Policy) to
clarify our interpretation of the phrase
‘‘distinct population segment of any
species of vertebrate fish or wildlife’’ for
the purposes of listing, delisting, and
reclassifying species under the Act (61
FR 4721; February 7, 1996). Under our
DPS policy, we consider three elements
in a decision regarding the status of a
possible DPS as endangered or
threatened under the Act. The elements
are: (1) The population segment’s
discreteness from the remainder of the
taxon to which it belongs; (2) the
population segment’s significance to the
taxon to which it belongs; and (3) the
population segment’s conservation
status in relation to the Act’s standards
for listing (i.e., when treated as if it were
a species, is the population segment
endangered or threatened?). Our policy
further recognizes it may be appropriate
to assign different classifications (i.e.,
threatened or endangered) to different
DPSs of the same vertebrate taxon (61
FR 4721; February 7, 1996).
Discreteness
The DPS policy’s standard for
discreteness requires an entity given
DPS status under the Act to be
adequately defined and described in
some way that distinguishes it from
other populations of the species. A
population segment may be considered
discrete if it satisfies either one of the
following conditions: (1) Marked
separation from other populations of the
same taxon resulting from physical,
physiological, ecological, or behavioral
factors, including genetic discontinuity;
or (2) populations delimited by
international boundaries within which
differences in control of exploitation,
management of habitat, conservation
status, or regulatory mechanisms exist
that are significant in light of 4(a)(1)(D)
of the Act.
Marked Separation from Other
Populations of the Same Taxon as a
Consequence of Physical, Physiological,
Ecological or Behavioral Factors. We do
not have any information to indicate
that a marked separation exists between
the United States and Mexico that
would distinguish populations of
northern Mexican gartersnake in the
United States from those in Mexico.
There is no information to indicate that
a marked separation exists as a result of
physical, physiological, ecological, or
behavioral factors.
There has been no genetic analysis
completed for the northern Mexican
gartersnake. Thus, we have no
information to indicate that genetic
differences exist.
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Populations Delimited by
International Boundaries Within Which
Differences in Control of Exploitation,
Management of Habitat, Conservation
Status, or Regulatory Mechanisms Exist
that are Significant. In terms of the
conservation status of the northern
Mexican gartersnake, despite the
significantly limited amount of
monitoring and/or survey data for the
northern Mexican gartersnake in
Mexico, we believe there is a higher
probability that the subspecies is fairing
better overall in Mexico in terms of
having more total populations, because
a larger percentage of the overall range
of the subspecies (approximately 70 to
80 percent of it historical distribution)
occurs in Mexico. However, we have no
information to indicate that the
populations on either side of the United
States-Mexico border have a more stable
or better conservation status.
We recognize that differences in
management regulatory protection of
northern Mexican gartersnake
populations may exist between
populations within Mexico and those
within the United States. These
differences primarily pertain to
protections afforded to occupied habitat.
In Mexico, any activity that
intentionally destroys or adversely
modifies occupied northern Mexican
gartersnake habitat is prohibited
[SEDESOL 2000 (LGVS) and 2001
(NOM–059–ECOL–2001)]. Neither the
Arizona Game and Fish Department or
the New Mexico Department of Game
and Fish can offer protections to
occupied habitat. Instead, these agencies
regulate take in the form of lethal or live
collection of individuals which is
prohibited in both states. However, any
conclusions that may be drawn with
reference to differences in management
across the United States-Mexico border
are largely speculative due to the lack of
information available as to the efficacy
and protections of these regulations in
practice. Because we determine in the
following section that populations of the
northern Mexican gartersnake in the
United States are not significant to the
subspecies as a whole, we need not
address further the ‘‘discreteness’’ test
of the DPS policy. For further
information on regulatory
considerations, please see our
discussion under Factor D below.
Significance
Under our DPS policy, a population
segment must be significant to the taxon
to which it belongs. The evaluation of
‘‘significance’’ may address, but is not
limited to, (1) evidence of the
persistence of the discrete population
segment in an ecological setting that is
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unique for the taxon; (2) evidence that
loss of the population segment would
result in a significant gap in the range
of the taxon; (3) evidence that the
population segment represents the only
surviving natural occurrence of a taxon
that may be more abundant elsewhere as
an introduced population outside its
historic range; and (4) evidence that the
discrete population segment differs
markedly from other populations of the
species in its genetic characteristics.
Ecological Setting. Throughout its
rangewide distribution, the northern
Mexican gartersnake occurs at
elevations from 130 to 8,497 ft (40 to
2,590 m) (Rossman et al. 1996, p. 172).
The northern Mexican gartersnake is
considered a riparian obligate (restricted
to riparian areas when not engaged in
dispersal behavior) and occurs chiefly
in the following general habitat types in
both the United States and Mexico: (1)
Source—area wetlands [e.g., cienegas
(mid-elevation wetlands with highly
organic, reducing (basic, or alkaline)
soils), stock tanks (small earthen
impoundment), etc.]; (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; Arizona Game and Fish Department
2001). Based on this information, we
determine that populations of the
northern Mexican gartersnake in
Arizona do not occupy an ecological
setting differing enough from
populations that occur in Mexico to be
considered unique for the subspecies.
Gap in the Range. The Service can
determine that a gap in a taxon’s range
caused by the potential loss of a
population would be significant based
on any relevant considerations. One
factor which may support such a
determination is whether the loss of a
geographic area amounts to a substantial
reduction of a taxon’s range and this
reduction is biologically important. The
United States comprised the most
northern portion of the northern
Mexican gartersnake’s range and
constituted approximately 20–30
percent of its rangewide historical
distribution. Because we do not
currently know exactly what the status
of the northern Mexican gartersnake is
in Mexico at this time, we are unable to
ascertain what percentage of extant
populations occur in the United States
as compared to Mexico. However, this is
not sufficient evidence to support a
determination that loss of the northern
Mexican gartersnake in the United
States represents a substantial reduction
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in the subspecies’ range based on the
geographic area which would be lost.
Furthermore, no area that is uniquely
biologically significant to the northern
Mexican gartersnake is located within
the United States as compared to
Mexico.
Another factor relevant to
determining whether a gap is significant
is the biological significance of the
number of total individuals of the taxon
in the population that may be lost.
Although we have no data on the
absolute numbers of northern Mexican
gartersnakes in the United States or
Mexico, the best available science
suggests that there are far more
individuals in Mexico than in the
United States, based on the more
extensive range in Mexico and the
current low density and number of
extant populations in the United States.
Therefore, we have no information to
indicate that the loss of between 8 and
17 populations of northern Mexican
gartersnakes known in the United States
is biologically significant to the taxon as
a whole.
In conclusion, we have determined
that the gap in the range of the northern
gartersnake that would be caused by the
loss of the United States population
would not be significant because: (1)
Loss of the United States population
would not constitute a substantial and
biologically important reduction of the
range of the subspecies; (2) the loss of
the individuals in the United States
would not be biologically significant to
the subspecies; and (3) we have not
identified any other reason why loss of
the United States population would
result in a significant gap in the range
of the subspecies.
Marked Differences in Genetic
Characteristics. Within the distribution
of every species there exists a peripheral
population, an isolate or subpopulation
of a species at the edge of the taxon’s
range. Long-term geographic isolation
and loss of gene flow between
populations is the foundation of genetic
changes in populations resulting from
natural selection or change. Evidence of
changes in these populations may
include genetic, behavioral, and/or
morphological differences from
populations in the rest of the species’
range. We have no information to
indicate that genetic differences exist
between populations of the northern
Mexican gartersnake at the northern
portion of its range in the United States
from those in Mexico. Therefore, based
on the genetic information currently
available, the northern Mexican
gartersnake in the United States should
not be considered biologically or
ecologically significant based simply on
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genetic characteristics. Biological and
ecological significance under the DPS
policy is always considered in light of
Congressional guidance (see Senate
Report 151, 96th Congress, 1st Session)
that the authority to list DPS’s be used
‘‘sparingly’’ while encouraging the
conservation of genetic diversity.
Whether the Population Represents
the Only Surviving Natural Occurrence
of the Taxon. As part of a determination
of significance, our DPS policy suggests
that we consider whether there is
evidence that the population represents
the only surviving natural occurrence of
a taxon that may be more abundant
elsewhere as an introduced population
outside its historic range. The northern
Mexican gartersnake in the United
States is not the only surviving natural
occurrence of the subspecies.
Consequently, this factor is not
applicable to our determination
regarding significance.
Conclusion
Following a review of the available
information, we conclude that the
northern Mexican gartersnake in the
United States is not significant to the
remainder of the subspecies. We made
this determination based on the best
available information, which does not
demonstrate that (1) these populations
persist in an ecological setting that is
unique for the subspecies; (2) the loss of
these populations would result in a
significant gap in the range of the
subspecies; and (3) these populations
differ markedly from populations of
northern Mexican gartersnake in Mexico
in their genetic characteristics, or in
other considerations that might
demonstrate significance. Further,
available information does not
demonstrate that the life history and
behavioral characteristics of the
northern Mexican gartersnake in the
United States is unique to the
subspecies. Therefore, on the basis of
the best scientific and commercial
information available, we find that
proposing to list a DPS for the northern
Mexican gartersnake in the United
States is not warranted; these
populations do not meet the definition
of a distinct population segment. We are
not addressing the third prong of the
DPS policy (i.e. the population
segment’s conservation status in relation
to the Act’s standards for listing) since
we find that the United States portion
of the range of the northern Mexican
gartersnake does not qualify as a listable
entity pursuant to our DPS policy, as
discussed above.
Significant Portion of the Range
In the petition to list the northern
Mexican gartersnake, the petitioners
also requested that we consider listing
the species throughout its range based
on its status in the United States. As
required by the Act, we have considered
in this finding whether the northern
Mexican gartersnake is in danger of
extinction ‘‘in all or a significant portion
of its range’’ as defined in the terms
‘‘threatened species’’ and ‘‘endangered
species’’ pursuant to section 3 of the
Act. In order to determine if Arizona
constitutes a significant portion of the
range of the subspecies, we evaluate
whether threats in this geographic area
imperil the viability of the subspecies as
a whole due to any biological
importance of this portion of the
subspecies range. Based upon the best
scientific information available, we find
that the extant populations in the
United States are not considered a
stronghold for the subspecies, they do
not represent core or important breeding
habitat, we are not aware of any unique
genetic or behavioral characteristics,
and we are not aware that threats in this
portion of its range threaten the whole
subspecies with extinction. Therefore,
we determine that the extant
populations of the northern Mexican
gartersnake in Arizona do not constitute
a significant portion of the range of the
subspecies because there is no
particular characteristic to any segment
within this portion of its range that
would render it biologically more
significant to the taxon as a whole than
other portions of its current range.
We note that the court in Defenders of
Wildlife v. Norton, 258 F.3d 1136 (9th
Cir. 2001), appeared to suggest that a
species could be in danger of extinction
in a significant portion of its range if
there is a ‘‘major geographical area’’ in
which the species is no longer viable
but once was. Although we do not
necessarily agree with the court’s
suggestion, we have determined that the
historical range of the subspecies within
the United States does not constitute a
‘‘major geographical area’’ in this
context. The portion of the northern
Mexican gartersnake’s historical range
in United States (20 to 30 percent)
constitutes a small percentage of the
total range of the subspecies.
The petitioners also requested that we
consider listing the species throughout
its range based on its rangewide status.
Below we respond to the petitioners
request through our analysis of the five
listing factors for the United States and
Mexico.
Summary of Factors Affecting the
Northern Mexican Gartersnake
Section 4 of the Act (16 U.S.C. 1533),
and implementing regulations at 50 CFR
424, set forth procedures for adding
species to the Federal Lists of
Endangered and Threatened Wildlife
and Plants. Under section 4(a) of the
Act, we may list a species on the basis
of any of five factors, as follows: (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. In
making this finding, information
regarding the status of, and threats to,
the northern Mexican gartersnake in
relation to the five factors provided in
section 4(a)(1) of the Act is discussed
below and summarized in Table 1
below.
TABLE 1.—SUMMARY OF NORTHERN MEXICAN GARTERSNAKE STATUS AND THREATS BY POPULATION IN UNITED STATES
[All locations in Arizona unless otherwise specified.]
Current status
Regional historical/current threats
Gila River ........................................
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Population locality
Extirpated .......................................
Gila and San Francisco Headwaters in New Mexico.
Lower Colorado River from Davis
Dam to International Border.
Extirpated .......................................
Considered extirpated by nonnatives, improper grazing, recreation,
development, groundwater pumping, diversions, channelization,
dewatering, road construction/use, wildfire, intentional harm, dams,
prey base reductions.
Considered extirpated by nonnatives, improper grazing, recreation,
prey base reductions.
Considered extirpated by nonnatives, prey base reductions, recreation, development, road construction/use, borderland security/undocumented immigration, intentional harm, dams.
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Extirpated .......................................
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TABLE 1.—SUMMARY OF NORTHERN MEXICAN GARTERSNAKE STATUS AND THREATS BY POPULATION IN UNITED STATES—
Continued
[All locations in Arizona unless otherwise specified.]
Current status
Regional historical/current threats
San Pedro River in United States ...
Extirpated .......................................
Santa Cruz River downstream of
the Nogales area of the International Border.
Extirpated .......................................
Salt River .........................................
Extirpated .......................................
Rio San Bernardino from International Border to headwaters at
Astin Spring (San Bernardino National Wildlife Refuge).
Agua Fria River ...............................
Extirpated .......................................
Considered extirpated by nonnatives, prey base reductions, improper
grazing, groundwater pumping, road construction/use, borderland
security/undocumented immigrants, intentional harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, development, groundwater pumping, diversions, channelization, road construction/use, borderland security/undocumented
immigrants, intentional harm, contaminants.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, development, diversions, wildfire, channelization, road construction/use, intentional harm, dams.
Considered extirpated by nonnatives, prey base reductions, borderland security/undocumented immigration, intentional harm, competition with Marcy’s checkered gartersnake.
Verde River upstream of Clarkdale
Extirpated .......................................
Verde River from the confluence
with the Salt upstream to Fossil
Creek.
Extirpated .......................................
Potrero Canyon/Springs ..................
Extirpated .......................................
Tanque Verde Creek in Tucson ......
Extirpated .......................................
Rillito Creek in Tucson ....................
Extirpated .......................................
Agua Caliente Spring in Tucson .....
Extirpated .......................................
Babocamari Cienega .......................
Extirpated .......................................
Barchas Ranch, Huachuca Mountain bajada.
Extirpated .......................................
Parker Canyon Lake and tributaries
in the Canelo Hills.
Extirpated .......................................
Oak Creek at Midgley Bridge ..........
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Population locality
Extirpated .......................................
Santa Cruz River/Lower San Rafael
Valley (headwaters downstream
to International Border).
Verde River from the confluence
with Fossil Creek upstream to
Clarkdale.
Oak Creek at Page Springs ............
Tonto Creek from mouth of Houston Creek downstream to Roosevelt Lake.
Cienega Creek from headwaters
downstream to the ‘‘Narrows’’
just downstream of Apache Canyon.
Pantano Wash (Cienega Creek)
from Pantano downstream to Vail.
Upper Scotia Canyon in the
Huachuca Mountains.
Audubon Research Ranch and vicinity near Elgin.
Downstream portion of the Black
River drainage from the Paddy
Creek confluence.
Extant .............................................
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Extirpated .......................................
Extant .............................................
Considered extirpated by nonnatives, prey base reductions, improper
grazing, development, recreation, dams, road construction/use,
wildfire, intentional harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, development, groundwater pumping, diversions, channelization, road construction/use, intentional harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, groundwater pumping, diversions, channelization, road construction/use, wildfire, development,intentional harm,
dams.
Considered extirpated by nonnatives, prey base reductions, improper
grazing.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, development, groundwater pumping, road construction/use, intentional harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, development, groundwater pumping, road construction/use, intentional harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, development, groundwater pumping, road construction/use, intentional harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, borderland security/undocumented immigration, intentional
harm.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, road construction/use, borderland security/undocumented immigration, intentional harm, dams.
Considered extirpated by nonnatives, prey base reductions, improper
grazing, recreation, development, intentional harm.
Nonnatives, prey base reductions, improper grazing, borderland security/undocumented immigration, intentional harm.
Extant .............................................
Nonnatives, prey base reductions, improper grazing, recreation, development, groundwater pumping, diversions, channelization, road
construction/use, intentional harm, dams.
Nonnatives, prey base reductions.
Nonnatives, prey base reductions, improper grazing, recreation, development, diversions, channelization, road construction/use, wildfire, intentional harm, dams.
Nonnatives, prey base reductions, improper grazing.
Extant .............................................
Nonnatives, prey base reductions, improper grazing, wildfire.
Extant .............................................
Nonnatives, prey base reductions, wildfire.
Extant .............................................
Nonnatives, prey base reductions, improper grazing.
Unknown ........................................
Nonnatives, prey base reductions, improper grazing, recreation, intentional harm.
Extant .............................................
Extant .............................................
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TABLE 1.—SUMMARY OF NORTHERN MEXICAN GARTERSNAKE STATUS AND THREATS BY POPULATION IN UNITED STATES—
Continued
[All locations in Arizona unless otherwise specified.]
Population locality
Current status
Regional historical/current threats
Downstream portion of the White
River drainage from the confluence of the East/North.
Big Bonito Creek .............................
Lake O’ Woods (Lakeside) .............
Unknown ........................................
Nonnatives, prey base reductions, improper grazing, recreation, road
construction/use, intentional harm.
Unknown ........................................
Unknown ........................................
Spring Creek above confluence
with Oak Creek.
Bog Hole Wildlife Area ....................
Upper 13 Tank, Patagonia Mountains bajada.
Babocamari River ............................
Arivaca Cienega ..............................
Unknown ........................................
Nonnatives, prey base reductions, improper grazing.
Nonnatives, prey base reductions, recreation, development, road construction/use, intentional harm.
Nonnatives, prey base reductions, development.
Unknown ........................................
Unknown ........................................
Nonnatives, prey base reductions.
Nonnatives, prey base reductions, improper grazing.
Unknown ........................................
Unknown ........................................
Nonnatives, prey base reductions, improper grazing.
Nonnatives, prey base reductions, improper grazing, borderland security/undocumented immigration, intentional harm.
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Note: ‘‘Extirpated’’ means that there have been no northern Mexican gartersnakes reported for a decade or longer at a site within the historical
distribution of the species, despite survey efforts, and there is no expectation of natural recovery at the site due to the presence of known or
strongly suspected causes of extirpation. ‘‘Extant’’ means areas where the species is expected to reliably occur in appropriate habitat as supported by museum records and/or recent, reliable observations. ‘‘Unknown’’ means areas where the species is known to have occurred based on
museum records (mostly historical) but access is restricted, and/or survey data is unavailable or insufficient, or where threats could preclude occupancy. The information used to develop this table can be found in the sources listed below.
Sources: Hyatt undated, p. 71; Nickerson and Mays 1970, pp. 495, 503; Hulse 1973, p. 278; Vitt and Ohmart 1978, p. 44; Hendrickson and
Minckley 1984, p. 131, 138–162; Meffe 1985, pp. 179–185; Rosen 1987, p. 5; Ohmart et al. 1988, pp. 143–147, 150; Rosen and Schwalbe 1988,
Appendix I; 1995, p. 452; 1996, pp. 1–3; 1997, p. 1; 2002b, pp. 223–227; 2002c, pp. 31, 70; Bestgen and Propst 1989, pp. 409–410; Clarkson
and Rorabaugh 1989, pp. 531–538; Marsh and Minckley 1990, p. 265; Medina 1990, pp. 351, 358–359; Sublette et al. 1990, pp. 112, 243, 246,
304, 313, 318; Abarca and Weedman 1993, pp. 2, 6–12; Girmendonk and Young 1993, pp. 45–52; Sullivan and Richardson 1993, pp. 35–42;
Stefferud and Stefferud 1994, p. 364; Bahre 1995, pp. 240–252; Hale et al. 1995, pp. 138–140; Holm and Lowe 1995, pp. 5, 27–35, 37–38, 45–
46; Rosen et al. 1995, p. 254; 1996b, pp. 8–9; 2001, Appendix I; Sredl et al. 1995a, p. 7; 1995b, p. 9; 1995c, p. 7; 2000, p. 10; Degenhardt et al.
1996, p. 319; Fernandez and Rosen 1996, pp. 6–19, 52–56; Stromberg et al. 1996, pp. 113–114, 123–128; Yuhas 1996; Drost and Nowak 1997,
p. 11; Weedman and Young 1997, pp. 1, Appendices B, C; Inman et al. 1998, Appendix B; Rinne et al. 1998, pp. 75–80; Nowak and Spille
2001, pp. 11, 32–33; Esque and Schwalbe 2002, pp. 161–193; Nowak and Santana-Bendix 2002, p. 39; Stromberg and Chew 2002, pp. 198,
210–213; Tellman 2002, p. 43; USFWS 2002a, pp. 40802–40804; 2002b, Appendix H; 2006, pp. 91–105; Voeltz 2002, pp. 40, 45–81; Krueper et
al. 2003, pp. 607, 613–614; Bonar et al. 2004, pp. 1–108; Forest Guardians 2004, p. 1; Unmack and Fagan 2004, p. 233; Fagan et al. 2005, pp.
34–41; Olden and Poff 2005, pp. 75, 82–87; Painter 2005; Philips and Thomas 2005; Webb and Leake 2005, pp. 302, 305–310, 318–320;
ADWR 2006; American Rivers 2006; Brennan and Holycross 2006, p. 123; Holycross et al. 2006, pp. 15–61; McKinnon 2006a, 2006b, 2006c,
2006d, 2006e; Paradzick et al. 2006, pp. 88–93, 104–110; Segee and Neeley 2006, Executive Summary, pp. 5–7; 10–12, 15–16, 21–23.
In the discussions of Factors A
through E below, we describe the
known factors that have contributed to
the current status of the northern
Mexican gartersnake. The majority of
this assessment is specific to those
factors that have contributed to its status
in the United States. The following
discussion of these factors that pertain
to the status and threats to the northern
Mexican gartersnake in Mexico are
mainly regional, or statewide, in scope
because in many cases we were unable
to find specific information
documenting that populations of the
northern Mexican gartersnake in Mexico
are directly affected by these threats. In
some instances, we do include
discussion on more refined geographic
areas of Mexico when supported by the
literature. However, many of the threats
that affect the northern Mexican
gartersnake in the United States are also
present in Mexico. Thus, the
relationship between the threats to the
habitat and species in Mexico may be
similar to what we have documented in
the United States.
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A. The Present or Threatened
Destruction, Modification, or
Curtailment of Its Habitat or Range
In the following discussion, we
elaborate on the physical threats to
northern Mexican gartersnake habitats
(i.e., riparian and aquatic communities)
that have occurred and continue to
occur within the distribution of the
species in the United States and Mexico.
Various threats that have affected and
continue to affect riparian and aquatic
communities include dams, diversions,
groundwater pumping, introduction of
nonnative species (vertebrates, plants,
and crayfish), woodcutting, mining,
contaminants, urban and agricultural
development, road construction,
livestock grazing, wildfires, and
undocumented immigration
(Hendrickson and Minckley 1984, p.
161; Ohmart et al. 1988, p. 150; Bahre
1995, pp. 240–252; Medina 1990, p. 351;
Sullivan and Richardson 1993, pp. 35–
42; Fleischner 1994, pp. 630–631;
Hadley and Sheridan 1995; Hale et al.
1995, pp. 138–140; DeBano and Neary
1996, pp. 73–75; Rinne and Neary 1996,
p. 135; Stromberg et al. 1996, pp. 124–
127; Girmendock and Young 1997, pp.
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45–52; Rinne et al. 1998, pp. 7–11;
Belsky et al. 1999, pp. 8–12; Esque and
Schwalbe 2002, pp. 165, 190; Hancock
2002, p. 765; Voeltz 2002, pp. 87–88;
Webb and Leake 2005, pp. 305–308;
Holycross et al. 2006, pp. 52–61;
McKinnon 2006a, 2006b, 2006c, 2006d,
2006e; Paradzick et al. 2006, pp. 88–93;
Segee and Neeley 1996, Executive
Summary, pp. 10–12, 21–23). These
activities and their effects on the
northern Mexican gartersnake are
discussed in further detail below.
It is important to recognize that in
most areas where northern Mexican
gartersnakes historically or currently
occur, two or more threats may be acting
synergistically in their influence on the
suitability of those habitats or on the
northern Mexican gartersnake itself. In
our assessment of the status of these
habitats, discussion of the role that
nonnative species introductions have
had on habitat suitability is critical.
However, we provide that discussion
under ‘‘Factor C. Disease and Predation’’
due to the intricate and complex
relationship nonnative species have
with respect to direct and indirect
pressures applied to the northern
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Mexican gartersnake and to its native
prey base.
Threats to Riparian and Aquatic
Biological Communities in the United
States. The modification and
destruction of aquatic and riparian
communities in the post-settlement arid
southwestern United States is well
documented and apparent in the field
(Medina 1990, p. 351; Sullivan and
Richardson 1993, pp. 35–42; Fleischner
1994, pp. 630–631; Stromberg et al.
1996, pp. 113, 123–128; Girmendock
and Young 1997, pp. 45–52; Belsky et
al. 1999, pp. 8–12; Webb and Leake
2005, pp. 305–310; Holycross et al.
2006, pp. 52–61). Several threats have
been identified in the decline of many
native riparian flora and fauna species
through habitat modification and
destruction as well as nonnative species
introductions. Researchers agree that the
period from 1850 to 1940 marked the
greatest loss and degradation of riparian
and aquatic communities in Arizona,
which were caused by anthropogenic
(human) land uses and the primary and
secondary effects of those uses
(Stromberg et al. 1996, p. 114; Webb and
Leake 2005, pp. 305–310). Many of
these land activities continue today and
are discussed at length below. An
estimated one-third of Arizona’s presettlement wetlands have dried or have
been rendered ecologically
dysfunctional (Yuhas 1996).
Modification and Loss of Cienegas in
the United States. Cienegas are
particularly important habitat for the
northern Mexican gartersnake and are
considered ideal for the species (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 soils.’’ Many of
these unique communities of the
southwestern United States, and
Arizona in particular, have been lost in
the past century to streambed
modification, improper livestock
grazing, cultural impacts, stream flow
stabilization by upstream dams,
channelization, and stream flow
reduction from groundwater pumping
and 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 along many southwestern
streams, including the San Pedro River.
Conservation of the remaining natural
cienegas in Arizona will be contingent
on their protection from severe flooding
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and from lowering of groundwater
levels (Hendrickson and Minckley 1984,
p. 169).
Many sub-basins where cienegas have
been severely modified or lost entirely
overlap, wholly or partially, the
historical distribution of the northern
Mexican gartersnake, including the San
Simon, Sulphur Springs, San Pedro, and
Santa Cruz valleys of southeastern and
south-central Arizona. The San Simon
Valley possessed several natural
cienegas with luxuriant vegetation prior
to 1885, and was used as a watering stop
for pioneers, military, and surveying
expeditions (Hendrickson and Minckley
1984, pp. 139–140). In the subsequent
decades, the disappearance of grasses
and commencement of severe erosion
were the result of heavy grazing
pressure by large herds of cattle as well
as the effects from wagon trails that
paralleled arroyos, occasionally crossed
them, and often required stream bank
modification (Hendrickson and
Minckley 1984, p. 140). Today, only the
artificially-maintained San Simon
Cienega exists in this valley. Similar
accounts of past conditions, adverse
effects from historical anthropogenic
activities, and subsequent reduction in
the extent and quality of cienega
habitats in the remaining valleys are
also provided in Hendrickson and
Minckley (1984, pp. 138–160).
Urban and Rural Development in the
United States. 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). Riparian communities are
sensitive to even low levels (less than 10
percent) of urban development within a
watershed (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). 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, Gila, and Salt rivers, respectively).
Urbanization and development of these
areas, along with the introduction of
nonnative species, are largely
responsible for the extirpation of the
northern Mexican gartersnake from
these areas.
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Urbanization on smaller scales can
also impact habitat suitability and the
prey base for the northern Mexican
gartersnake. Medina (1990, pp. 358–359)
concluded that perennial streams had
greater tree densities in all diameter size
classes of Arizona alder and box elder
(Acer negundo) as compared to
ephemeral reaches where small
diameter trees were absent. Small
diameter trees assist the northern
Mexican gartersnake by providing
additional habitat complexity and cover
needed to reduce predation risk and
enhance the usefulness of areas for
thermoregulation. Regional
development and subsequent land use
changes, spurred by increasing
populations, along lower Tonto Creek
and within the Verde Valley where
northern Mexican gartersnakes are
extant continue to threaten this snake’s
habitat and affect the habitat’s
suitability for the northern Mexican
gartersnake and its prey species
(Girmendock and Young 1997, pp. 45–
52; Voeltz 2002, pp. 58–59, 69–71;
Paradzick et al. 2006, pp. 89–90).
Holycross et al. (2006, pp. 53, 56)
recently documented adverse effects to
northern Mexican gartersnake habitat in
the vicinity of Rock Springs along the
Agua Fria River and also throughout the
Verde Valley along the Verde River.
The effects of urban and rural
development are expected to increase as
populations increase. Consumer interest
in second home and/or retirement real
estate investments has increased
significantly in recent times within the
southwestern United States. Medina
(1990, p. 351) points out that many real
estate investors are looking for
aesthetically scenic, mild climes to
enjoy seasonally or year-round and
hence choose to develop pre- or postretirement properties that are within or
adjacent to riparian areas due to their
aesthetic appeal and available water.
Arizona increased its population by 394
percent from 1960 to 2000, and is
second only to Nevada as the fastest
growing State in terms of human
population (SSDAR 2000). Over the
same time period, population growth
rates in Arizona counties where the
northern Mexican gartersnake
historically occurred or may still be
extant have varied by county but are no
less remarkable: 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 (2004 percent) (SSDAR 2000).
Population growth trends in Arizona,
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and Maricopa County in particular, are
expected to continue into the future.
The Phoenix metropolitan area, founded
in part due to its location at the junction
of the Salt and Gila rivers, is a
population center of 3.63 million
people. The Phoenix metropolitan area
is the sixth largest in the United States
and resides in the fastest growing
county in the United States since the
2000 census (Arizona Republic 2006).
Development growth predictions have
also been made for traditionally rural
portions of Arizona. The populations of
developing cities and towns of the
Verde watershed are expected to more
than double in the next 50 years, which
may pose exceptional threats to riparian
and aquatic communities of the Verde
Valley where northern Mexican
gartersnakes occur (Girmendock and
Young 1993, p. 47; American Rivers
2006; Paradzick et al. 2006, p. 89).
Communities in Yavapai and Gila
counties such as the Prescott-Chino
Valley, Strawberry, Pine, and Payson
have all seen rapid population growth
in recent years. For example, the
population in the town of Chino Valley,
at the headwaters of the Verde River,
has grown by 22 percent between 2000
and 2004; Gila County, which includes
reaches of the Salt, White, and Black
rivers and Tonto Creek, grew by 20
percent between 2000 and 2003
(https://www.census.gov). The upper San
Pedro River is also the location of rapid
population growth in the Sierra VistaHuachuca City-Tombstone area (https://
www.census.gov). All of these
communities are near or within the
vicinity of historical or extant northern
Mexican gartersnake populations.
Road Construction, Use, and
Maintenance in the United States.
Roads cover approximately one percent
of the land area in the United States, but
negatively affect 20 percent of the
habitat and biota in the United States
(Angermeier et al. 2004, p. 19). Roads
pose unique threats to herpetofauna
(reptiles and amphibians) and
specifically to species like the northern
Mexican gartersnake, its prey base, and
the habitat where it occurs through: (1)
Fragmentation, modification, and
destruction of habitat; (2) an 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 and/
or inhibition of reproduction; (7)
contributions of pollutants to riparian
and aquatic communities; and (8)
population sinks through direct
mortality (Rosen and Lowe 1994, pp.
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146–148; Waters 1995, p. 42; 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).
Construction and maintenance of
roads and highways near riparian areas
can be a source of sediment and
pollutants (Waters 1995, p. 42; Wheeler
et al. 2005, pp. 145, 148–149). Sediment
can adversely affect fish populations
used as prey by the northern Mexican
gartersnake by (1) interfering with
respiration; (2) reducing the
effectiveness of visually-based hunting
behaviors; and (3) filling in interstitial
spaces of the substrate which reduces
reproduction and foraging success of
fish interfering with respiration, and
restricting reproduction and foraging of
fish. Excessive sediment also fills in
intermittent pools required for
amphibian prey reproduction and
foraging. Fine sediment pollution in
streams impacted by highway
construction without the use of
sediment control structures was 5 to 12
times greater than control streams.
Sediment can lead to several effects in
resident fish species used by northern
Mexican gartersnakes as prey species,
which can ultimately cause the northern
Mexican gartersnake’s increased direct
mortality, reduced reproductive success,
lower overall abundance, lower species
diversity, and reductions in food base as
documented by Wheeler et al. (2005, p.
145). The underwater foraging ability of
northern Mexican gartersnakes can also
be directly compromised by excessive
turbidity caused by sedimentation of
water bodies. Metal contaminants,
including iron, zinc, lead, cadmium,
nickel, copper, and chromium, are
bioaccumulative) and are associated
with highway construction and use
(Foreman and Alexander 1998, p. 220;
Hopkins et al. 1999, p. 1260; Campbell
et al. 2005, p. 241; Wheeler et al. 2005,
pp. 146–149). 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 and lead
to adverse health affects.
Several studies have addressed the
effects of bioaccumulative substances on
watersnakes. We find these studies
relevant because watersnakes and
gartersnakes have very similar life
histories and prey bases and therefore,
the effects from contamination of their
habitat from bioaccumulative agents are
expected to have similar effects.
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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 food item, the
central stoneroller (fish) (Campostoma
anomalum). Metals, in trace amounts,
affect the structure and function of the
liver and kidneys of vertebrates and may
also act as neurotoxins, affecting
nervous system function (Rainwater et
al. 2005, p. 670). Metals may also be
sequestered in the skin of reptiles, but
this effect is tempered somewhat by
ecdysis (the regular shedding or molting
of the skin) (Burger 1999, p. 212).
Hopkins et al. (1999, p. 1261) found that
metals may even interfere with
metabolic rates of banded watersnakes
(Nerodia fasciata), altering the
allocation of energy between
maintenance and reproduction,
reducing the efficiency of energy stores,
and forcing individuals to forage more
often, which increases activity costs (the
energy expended in hunting which
effects the net nutritional intake of an
organism) and predation risk.
Snakes of all species are particularly
vulnerable to mortality when they
attempt to cross roads. There are several
reasons for this phenomenon. First, all
snakes are thigmotherms (animals that
derive heat from warm surfaces), which
often compels them to slow down or
even stop and rest on road surfaces that
have been warmed by the sun as they
attempt to cross (Rosen and Lowe 1994,
p. 143). Additionally, many species of
snakes are active when traffic densities
are greatest, as is the case with
gartersnakes, which are generally
diurnal (active during daylight hours)
(Rosen and Lowe 1994, p. 147). 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, which highlights the
seasonal variability in surface activity of
this snake, and many other species of
reptiles. Perhaps the most common
factor in road mortality of snakes is the
propensity for drivers to intentionally
run over snakes, which generally make
easy targets because they usually cross
roads at a perpendicular angle (Klauber
1956, p. 1026; Langley et al. 1989, p. 47;
Shine et al. 2004, p. 11). This driving
behavior is exacerbated by the general
animosity that humans have toward
snakes in general in modern-day society
(Ernst and Zug 1996, p. 75; Green 1997
pp. 285–286). In fact, Langley et al.
(1989, p. 47) conducted an experiment
on the propensity for drivers to hit
reptiles on the road using turtle and
snake models and found that many
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people have a greater desire to hit a
snake on the road than any other
animal; several drivers actually stopped
and backed-over the snake mimic to
ensure it was dead. Roe et al. (2006, p.
161) conclude that mortality rates due to
roads are higher in vagile (mobile)
species, such as gartersnakes (active
hunters), than those of more sedentary
species, such as the North American pit
vipers in the genera Agkistrodon,
Sistrurus, and Crotalus, which more
commonly employ sit-and-wait foraging
strategies. Roads that bisect wetland
communities also act as mortality sinks
in the dispersal or migratory movements
of snakes (Roe et al. 2006, p. 161). The
effect of road mortality of snakes
becomes most significant in the case of
small, highly fragmented populations
where the chance removal of mature
females from the population may
appreciably degrade the viability of a
population.
Roads create easy access to areas
previously infrequently visited or
inaccessible to humans, increasing the
frequency and significance of
anthropogenic threats to riparian areas
and fragmenting the landscape, which
may genetically isolate herpetofaunal
populations (Rosen and Lowe 1994, pp.
146–148; Andrews and Gibbons 2005,
p. 772).
While snakes of all species may suffer
direct mortality from attempting to cross
roads, Andrews and Gibbons (2005, pp.
777–779) found that many individuals
of small, diurnal snake species avoid
open areas (e.g., roads) instinctively in
order to lower predation rates, which
represents a different type of threat from
roads. Shine et al. (2004, p. 9) found
that the common gartersnake typically
changed direction when encountering a
road. These avoidance behaviors by
individuals aversive to crossing roads
affect movement patterns and may
ultimately affect reproductive output
within populations (Shine et al. 2004,
pp. 9, 17–19). This avoidance behavior
has been observed in the common
gartersnake (Thamnophis sirtalis), a
sister taxon to the Mexican gartersnake
with similar life histories and behavior
(Shine et al. 2004, p. 9). In our
discussion and as evidenced by the
literature we reviewed on the effect of
roads on snake movements, we
acknowledge the individuality of snakes
in their behaviors towards road
crossings in that roads may affect a
snake’s movement behavior by a variety
of means and that generalizing these
resultant behaviors does not adequately
address this variability.
In addition to altering the movement
patterns of some snakes, roads can
interfere with the male gartersnake’s
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olfactory-driven ability to follow the
pheromone trails left by receptive
females (Shine et al. 2004, pp. 17–18).
This effect to the male’s ability to trail
females may exacerbate the effects of
low population density and
fragmentation that affect several species
of snakes, including the northern
Mexican gartersnake. Furthermore,
roads can facilitate an increase in the
distance traveled by male snakes
seeking receptive females, which
increases exposure to predation and
subsequently increases mortality rates
(Shine et al. 2004, pp. 18–19). Although
the northern Mexican gartersnake was
not the subject of the 2004 Shine et al.
study, similar responses can be
expected in the northern Mexican
gartersnake because its life history is
similar to the, study’s subject species
(i.e., the common gartersnake).
Roads tend to adversely affect aquatic
breeding anuran (frog and/or toad)
populations more so than other species
due to their activity patterns, population
structures, and preferred habitats (Hels
and Buchwald 2001, p. 331). Carr and
Fahrig (2001, pp. 1074–1076) found that
populations of highly mobile anuran
species such as leopard frogs (Rana
pipiens) were affected more
significantly than more sedentary
species and that population persistence
can be at risk depending on traffic
densities, which may adversely affect
the prey base for northern Mexican
gartersnakes because leopard frogs are a
primary prey species.
Recreation in the United States. As
discussed above, population growth
trends are expected to continue into the
future. Expanding population growth
leads to higher recreational use of
riparian areas. Riparian areas located
near urban areas are vulnerable to the
effects of increased recreation with
predictable changes in the type and
intensity of land use following
residential development. An example of
such an area within the existing
distribution of the northern Mexican
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 neonates.
Increased human visitation of occupied
habitat also increases the potential for
human-gartersnake interactions, which
frequently does not bode well for
snakes, as it often leads to their capture,
injury, or death of the snake due to the
lay person’s fear of snakes (Rosen and
Schwalbe 1988, p. 43; Ernst and Zug
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1996, p. 75; Green 1997, pp. 285–286;
Nowak and Santana-Bendix 2002,
p. 39).
Groundwater Pumping, Surface Water
Diversions, and Drought in the United
States. Increased urbanization and
population growth results in an increase
in the demand for water and, therefore,
water development projects. Collier et
al. (1996, p. 16) mention that water
development projects are one of two
main causes of decline of native fish in
the Salt and Gila rivers of Arizona.
Municipal water use in central Arizona
has increased by 39 percent in the last
8 years (American Rivers 2006). 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. The hydrologic
connection between groundwater and
surface flow of intermittent and
perennial streams is becoming better
understood. 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 desiccation 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). Finally, complete
disconnection of the aquifer and the
stream results in strong negative effects
to riparian vegetation (Webb and Leake
2005, p. 309). If complete disconnection
occurs, the hyporheic zone could be
adversely affected. The hyporheic zone
can promote ‘‘hot spots’’ of productivity
where groundwater upwelling occurs by
producing nitrates that can enhance the
growth of vegetation, but its significance
is contingent upon its activity and
extent of connection with the
groundwater (Boulton et al. 1998, p. 67;
Boulton and Hancock 2006, pp. 135,
138). Changes to the duration and
timing of upwelling can potentially lead
to localized extinctions in biota
(Boulton and Hancock 2006, p. 139).
To varying degrees, the effects of
groundwater pumping on surface water
flow and riparian communities have
been observed in the Santa Cruz, San
Pedro, and Verde rivers as a result of
groundwater demands of Tucson, Sierra
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Vista, and the rapidly growing Prescott
Valley, respectively (Stromberg et al.
1996, pp. 113, 124–128; Rinne et al.
1998, p. 9; Voeltz 2002, pp. 45–47, 69–
71). 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 being currently
dominated by woody species more
tolerant of declining water tables due to
their associated deeper rooting depths.
The full effects of largescale
groundwater pumping associated with
the proposed Big Chino Water Ranch
Project and its associated 30-mile (48
km), 36-in (91-cm) diameter pipeline
have yet to be realized in the Verde
River (McKinnon 2006c). This
groundwater pumping and inter-basin
transfer project is projected to deliver
2.8 billion gallons of groundwater
annually from the Big Chino sub-basin
aquifer to the rapidly growing area of
Prescott Valley for municipal use
(McKinnon 2006c). The Big Chino subbasin provides 86 percent of the
baseflow to the upper Verde River
(American Rivers 2006; McKinnon
2006a). The potential for this project to
obtain funding and approval for
implementation has placed the Verde
River on American River’s ‘‘Ten Most
Endangered Rivers List (of 2006)’’
(American Rivers 2006). This potential
reduction or loss of baseflow in the
Verde River could seasonally dry up
large reaches and/or adversely affect the
riparian community and the suitability
of the habitat for extant populations of
the northern Mexican gartersnake and
its prey species in that area.
Within the Verde River watershed,
and particularly within the Verde Valley
where the northern Mexican gartersnake
remains extant, several other activities
continue to threaten surface flows
(Rinne et al. 1998, p. 9; 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, which may have supported
the northern Mexican gartersnake
(Girmendock and Young 1993, pp. 45–
47; Sullivan and Richardson 1993, pp.
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38–39; Paradzick et al. 2006, pp. 104–
110). Groundwater pumping in Tonto
Creek regularly eliminates surface flows
during parts of the year (Abarca and
Weedman 1993, p. 2). The upper Gila
River is also threatened by diversions
and water allocations. In New Mexico,
a proposed water project that resulted
from a landmark Gila River water
settlement in 2004 allows New Mexico
the right to withhold 4.5 billion gallons
of surface water every year (McKinnon
2006d). If this proposed water diversion
project is implemented, in dry years,
currently perennial reaches of the upper
Gila River will dry completely which
removes all suitability of this habitat for
the northern Mexican gartersnakes and
a host of other riparian and aquatic
species (McKinnon 2006d).
Further evidence of the threat of
groundwater depletion can be found in
the management activities of the
Arizona Department of Water Resources
(ADWR). ADWR manages water
supplies in Arizona and has established
five Active Management Areas (AMA)
across the state (ADWR 2006). An AMA
is established by ADWR when an area’s
water demand has exceeded the
groundwater supply and an overdraft
has occurred. Geographically, all five
AMAs overlap the historical
distribution of the northern Mexican
gartersnake in Arizona and provide
further evidence of the role groundwater
pumping has had and continues to have
on historical and occupied northern
Mexican gartersnake habitat. Such
overdrafts are capable of adversely
impacting surface water flow of streams
that are hydrologically connected to the
aquifer under stress and are often
exacerbated by the ever-growing number
of surface water diversions for various
purposes.
In order to accommodate the needs of
rapidly growing rural and urban
populations, surface water is commonly
diverted to serve many industrial and
municipal uses. These diversions have
dewatered large reaches of once
perennial or intermittent streams,
adversely affecting northern Mexican
gartersnake habitat throughout its range
in Arizona and New Mexico. Many
tributaries of the Verde River are
permanently or seasonally dewatered by
diversions for agriculture (Paradzick et
al. 2006, pp. 104–110).
The effects of the water withdrawals
discussed above may be exacerbated by
the current, long-term drought facing
the arid southwestern United States.
Philips and Thomas (2005) provided
streamflow records that indicate that the
drought Arizona experienced between
1999 and 2004 was the worst drought
since the early 1940s and possibly
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earlier. Ongoing drought conditions
have depleted recharge of aquifers and
decreased baseflows in the region.
While drought periods have been
relatively numerous in the arid
Southwest according to recorded history
from the mid-1800s to the present, the
effects of anthropogenic threats on
riparian and aquatic communities have
compromised the ability of these
communities to function under the
additional stress of prolonged drought
conditions. Holycross et al. (2006, pp.
52–53) recently documented the effects
of drought on northern Mexican
gartersnake habitat in the vicinity of
Arcosante along the Agua Fria River and
at Big Bug Creek where the streams were
completely dry and therefore unsuitable
northern Mexican gartersnake habitats.
Improper Livestock Grazing in the
United States. Poorly managed 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; Waters 1995, pp. 22–24; Pearce et
al. 1998, p. 307; Belsky et al. 1999, p.
1). Livestock grazing, as a resource use
on public and private lands, has more
than doubled quantitatively in 50 years;
the number of cattle being grazed in the
western United States increased from
25.5 million head in 1940, to 54.4
million head in 1990 (Belsky et al. 1999,
p. 3).
Effects of improper livestock
management on riparian and aquatic
communities have spanned from early
settlement to modern day. Some
historical accounts of riparian area
conditions in Arizona elucidate early
effects of poor livestock management.
Cheney et al. (1990, pp. 5, 10) provide
historical accounts of the early adverse
effects of improper livestock
management in the riparian zones and
adjacent uplands of the Tonto National
Forest and in south-central Arizona.
These accounts describe the removal of
riparian trees for preparation of
livestock use and substantial changes to
flow regimes accentuated by observed
increases in runoff and erosion rates.
Such accounts of riparian conditions
within the historical distribution of the
northern Mexican gartersnake in
Arizona contribute to the understanding
of when declines in abundance and
distribution may have occurred and the
causes for subsequent fragmentation of
populations and widespread
extirpations.
In the recent past, riparian and
aquatic communities have been
negatively impacted by poor livestock
management (e.g., overgrazing,
uncontrolled access to riparian areas,
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improper pasture rotation, no
monitoring of use, etc.) within several
watersheds that the northern Mexican
gartersnake historically occupied, and
in some cases, poor livestock
management may constitute the greatest
impact to riparian vegetation. The
specific ways in which improper
livestock grazing can adversely affect
northern Mexican gartersnakes and
contribute to their decline is discussed
below. Watersheds where improper
grazing has been documented as a
contributing factor of northern Mexican
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; Girmendock
and Young 1997, p. 47; Voeltz 2002, pp.
45–81; Krueper et al. 2003, pp. 607,
613–614; Holycross et al. 2006, pp. 52–
61; McKinnon 2006d, 2006e; Paradzick
et al. 2006, pp. 90–92). Holycross et al.
(2006, pp. 53–55, 58) recently
documented adverse effects from
improper livestock grazing on northern
Mexican gartersnake habitat along the
Agua Fria from EZ Ranch to Bloody
Basin Road, along Dry Creek from Dugas
Road to Little Ash Creek, along Little
Ash Creek from Brown Spring to Dry
Creek, along Sycamore Creek in the
vicinity of its confluence with the Verde
River, and on potential northern
Mexican gartersnake habitat along Pinto
Creek at the confluence with the West
Fork of Pinto Creek. In southeastern
Arizona, there have been observations of
effects to the vegetative community
suggesting that livestock grazing
activities continue to adversely affect
extant populations of northern Mexican
gartersnakes by reducing or eliminating
cover required by the northern Mexican
gartersnake for thermoregulation,
protection from predation, and foraging
(Hale 2001, pp. 32–34, 50, 56).
Poor livestock management causes a
decline in diversity, abundance, and
species composition of riparian
herpetofauna communities from direct
or indirect threats to the prey base, the
habitat, or to the northern Mexican
gartersnake itself from: (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; and (5) a rise
in water temperatures to levels lethal to
larval stages of amphibian and fish
development (Szaro et al. 1985, p. 362;
Schulz and Leininger 1990, p. 295;
Belsky et al. 1999, pp. 8–11). Improper
livestock grazing may also lead to
desertification (the process of becoming
arid land or desert as a result of land
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mismanagement or climate change) due
to a loss in soil fertility from erosion
and gaseous emissions spurred by a
reduction in vegetative ground cover
(Schlesinger et al. 1990, p. 1043). Stock
tanks may facilitate the spread of
nonnative species when nonnative
species of fish, amphibians, and crayfish
are intentionally or unintentionally
stocked by anglers and private
landowners (Rosen et al. 2001, p. 24).
Specific attributes of ecosystems, such
as composition, function, and structure,
have been documented as being altered
by improper livestock management
through a variety of means including:
(1) Decreasing the density and biomass
of individual species, reducing species
richness, and changing biological
community organization; (2) interfering
with nutrient cycling and ecological
succession; and (3) changing vegetation
stratification, contributing to soil
erosion, and decreasing availability of
water to biotic communities (Fleischner
1994, p. 631).
The management of stock tanks is an
important consideration for northern
Mexican gartersnakes. Stock tanks can
be intermediary ‘‘stepping stones’’ in
the dispersal of nonnative species from
larger source populations to new areas
(Rosen et al. 2001, p. 24). Additionally,
dense bank and aquatic vegetation is an
important habitat characteristic for the
northern Mexican gartersnake that can
be affected if the impoundment is
poorly managed, which may lead to
trampling or overgrazing of the bankside
vegetation. Poor management may also
favor nonnative predators of the
northern Mexican gartersnake (Rosen
and Schwalbe 1988, pp. 47, 32).
Alternatively, well-managed stock tanks
can provide habitat suitable for northern
Mexican gartersnakes both structurally
and in terms of prey base, especially
when the tank remains devoid of
nonnative species while supporting
native prey species; provides adequate
vegetation cover; and provides reliable
water sources in periods of prolonged
drought. Given these benefits of wellmanaged stock tanks, we believe wellmanaged stock tanks may be an
important component to northern
Mexican gartersnake conservation.
A key to proper livestock management
appears to be increasing the distribution
of cattle across the entire grazing space.
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
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poorly managed cattle to remain within
or adjacent to riparian communities.
Trimble and Mendel (1995, p. 243)
stated that ‘‘Cows, unlike sheep, appear
to love water and spend an inordinate
amount of time together lounging in
streams and ponds, especially in
summer (surface-active season for
reptiles and amphibians), sometimes
going in and coming out several times
in the course of a day.’’ Expectedly, this
behavior is more pronounced in more
arid regions (Trimble and Mendel 1995,
p. 243). In one rangeland study, it was
concluded that 81 percent of the
vegetation that was removed by cattle
was from a riparian area which
amounted to only two percent of the
total grazing space (Trimble and Mendel
1995, p. 243). Another study reported
that grazing rates were 5 to 30 times
higher in riparian areas than on the
uplands which may be due in part to
several factors: (1) Higher forage volume
and palatability of species in riparian
areas; (2) water availability; (3) the close
proximity of riparian areas to the best
upland grazing sites; and (4)
microclimatic features such as cooler
temperatures and shade (Trimble and
Mendel 1995, p. 244).
The northern Mexican gartersnake
uses riparian herbaceous vegetation for
cover, thermoregulation, and foraging.
Clary and Webster (1989, p. 1) noted
that excessive grazing and trampling
from poor livestock management can
affect riparian and stream communities
by reducing or eliminating this
vegetation, causing channel aggradation
or degradation, causing widening or
incisement of stream channels, and
changing streambank morphology, with
the cumulative result of lowering
corresponding water tables. In support
of findings made by Fleischner (1994,
pp. 631–632), these effects can largely
be attributed to the tendency of
livestock in the arid Southwest to spend
a disproportionately longer time in
riparian areas than in upland range
pasture (5–30 times longer,
comparatively), which leads to
overgrazing of the riparian vegetation
(Clary and Medin 1990, p. 1). However,
even when livestock’s access to riparian
areas is restricted, poor livestock
management in the uplands leads to soil
compaction and decreased filtering
capacity of vegetation. These effects
increase the speed and amount of runoff
from the uplands, which contributes
heightened, unnatural amounts of
sediment in aquatic habitat. This
damages the suitability of that habitat
and fills in pools, which affects their
permanency and suitability for many
prey species of the northern Mexican
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gartersnake (Sartz and Tolsted 1974, p.
354; Weltz and Wood 1986, pp. 367–
368; Orodho et al. 1990, p. 9; Trimble
and Mendel 1995, pp. 235–236; Pearce
et al. 1998, p. 302). The response of
riparian herbaceous vegetation after the
removal of cattle was documented as
dramatic, with a four to six fold increase
in density, as observed in the upper San
Pedro River (Krueper et al. 2003, pp.
607, 613–614). Schulz and Leininger
(1990, p. 295) also remarked that
riparian ecosystems can improve
quickly when livestock are removed.
As stated previously, dense vegetative
cover is an essential component to
habitat suitable for the northern
Mexican gartersnake for several reasons
(Szaro et al. 1985, p. 364; Rosen and
Schwalbe 1988, p. 47). The removal or
severe alteration of this habitat
component significantly affects the
foraging success and heightens the
predation risk of the northern Mexican
gartersnake. Small, isolated populations
of northern Mexican gartersnakes that
use stock tanks as refugia may be
extirpated within 1 year of vegetation
removal (Rosen and Schwalbe 1988, p.
33). Northern Mexican gartersnake
populations that occur in isolated
wetlands or stock tanks are not likely to
recolonize naturally (i.e. without
reestablishment efforts) once extirpated
due to the species’ tendency to avoid
long overland movements (Rosen and
Schwalbe 1988. p. 33).
Szaro et al. (1985, p. 360) assessed the
effects of improper livestock
management on the same stream on a
sister taxon. They 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 accumulates
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.
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Direct mortality of amphibian species,
in all life stages, from being trampled by
livestock has been documented in the
literature (Bartelt 1998, p. 96; Ross et al.
1999, p. 163). The resultant extirpation
risk of amphibian populations as a prey
base for northern Mexican gartersnakes
by direct mortality is governed by the
relative isolation of the amphibian
population, the viability of that
population, and the propensity for
stochastic events such as wildfires.
Livestock grazing within habitat
occupied by northern Mexican
gartersnakes can result in direct
mortality of individual gartersnakes as
observed in a closely related taxon on
the Apache-Sitgreaves National Forest.
In that instance, a black-necked
gartersnake (Thamnophis cyrtopsis
cyrtopsis) had apparently been killed by
trampling hoof action of cattle along the
shore of a stock tank within an actively
grazed allotment (Chapman 2005). This
event was not observed first-hand, but
was supported by postmortem photo
documentation of the physical injuries
to the specimen and the location of the
carcass among a dense cluster of hoof
tracks along the shoreline of the stock
tank. It is also unlikely that a predator
would kill the snake and leave it
uneaten. While this type of direct
mortality of gartersnakes has long been
suspected by agency biologists and
academia, this may be the first recorded
observation of direct mortality of a
gartersnake due to livestock trampling.
We expect this type of direct mortality
to be uncommon but significant in the
instance of a fragmented population
with a skewed age-class distribution and
low to no recruitment as currently
observed in many northern Mexican
gartersnake populations in the United
States. In these circumstances, the loss
of one or more adults, most notably
reproductive females, may lead directly
to extirpation of the species from a
given site with no expectation of
recolonization.
Our analysis of the best available
scientific and commercial information
available indicates that adverse effects
from improper livestock management on
the northern Mexican gartersnake, its
habitat, and its prey base can be
significant. However, we recognize that
well-managed grazing can occur with
limited effects to this species when
management emphasis is directed to
moderated access restrictions for
occupied habitat combined with the use
of remote drinkers (containerized water
sources supplied by water pumped from
a nearby source) as well as other
livestock management protocols that
lessen the effect of vegetation
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disturbance and removal adjacent to
occupied habitat by increasing the
distribution of cattle across an
allotment. Lastly, as previously stated,
we also recognize the value of wellmanaged stock tanks in the conservation
of northern Mexican gartersnakes.
Catastrophic Wildfires in the United
States. Low-intensity fire has been a
natural disturbance factor in forested
landscapes for centuries, and lowintensity fires were common in
southwestern forests prior to European
settlement (Rinne and Neary 1996, pp.
135–136). Rinne and Neary (1996, p.
143) discuss the current effects of fire
management policies on aquatic
communities in Madrean-type
ecosystems in the southwestern United
States. They 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 devastating wildfires. The
effects of these catastrophic wildfires
include the removal of vegetation, the
degradation of watershed condition,
altered stream hydrographs, and
increased sedimentation of streams.
These effects can harm fish
communities, as observed in the 1990
Dude Fire, in which corresponding ash
flows decimated some fish populations
in Dude Creek and the East Verde River
(Voeltz 2002, p. 77). These effects can
significantly lessen the prey base for
northern Mexican gartersnakes and
could lead to direct mortality in the case
of fires that are within occupied habitat.
Fire has also become an increasingly
significant threat in lower elevation
communities as well. Esque and
Schwalbe (2002, pp. 180–190) discuss
the effect of wildfires in the upper and
lower subdivisions of Sonoran
desertscrub where the northern Mexican
gartersnake historically occurred. The
widespread invasion of nonnative
annual grasses, such as brome species
(Bromus sp.) and Mediterranean grasses
(Schismus sp.), appear to be largely
responsible for altered fire regimes that
have been observed in these
communities, which are not adapted to
fire (Esque and Schwalbe 2002, p. 165).
In areas comprised entirely of native
species, ground vegetation density is
mediated by barren spaces that do not
allow fire to carry itself across the
landscape. However, in areas where
nonnative grasses have become
established, the fine fuel load is
continuous, and fire is capable of
spreading quickly and efficiently (Esque
and Schwalbe 2002, p. 175). After
disturbances such as fire, brome grasses
may exhibit dramatic population
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explosions, which hasten their effect on
native vegetative communities.
Additionally, with increased fire
frequency, these population explosions
ultimately lead to a type-conversion of
the vegetative community from
desertscrub to grassland (Esque and
Schwalbe 2002, pp. 175–176). Fires
carried by the fine fuel loads created by
nonnative grasses often burn at
unnaturally high temperatures, which
may result in soils becoming
hydrophobic (water repelling),
exacerbate sheet erosion, and contribute
large amounts of sediment to receiving
water bodies, thereby affecting the
health of the riparian community (Esque
and Schwalbe 2002, pp. 177–178). The
siltation of isolated, remnant pools in
intermittent streams has significant
effects on lower-elevation species, as
observed in lowland leopard frogs and
native fish, important prey species for
northern Mexican gartersnakes (Esque
and Schwalbe 2002, p. 190).
Undocumented Immigration and
International Border Enforcement and
Management in the United States.
Undocumented immigrants attempt to
cross the International border from
Mexico into the United States in areas
historically or currently occupied by the
northern Mexican gartersnake. This
method of immigration and the
corresponding efforts to enforce U.S.
border laws and policies have been
occurring for many decades with
increasing intensity and have resulted
in unintended adverse effects to biotic
communities in the border region.
During the warmest months of the year,
many attempted border crossings occur
in riparian areas that serve to provide
shade, water, and cover. Increased U.S.
border enforcement efforts that began in
the early 1990s in California and Texas
have resulted in concentrated levels of
attempted undocumented immigrant
crossings into Arizona (Segee and
Neeley 2006, p. 6).
Riparian habitats that historically
supported or may currently support
northern Mexican gartersnakes in the
San Bernardino National Wildlife
Refuge, the San Pedro River corridor,
the Santa Cruz River corridor, the lower
Colorado River corridor, and along
many smaller streamside and canyon
bottom areas within Cochise, Santa
Cruz, and Pima counties have high
levels of undocumented immigrant
traffic (Segee and Neeley 2006,
Executive Summary, pp. 10–12, 21–23).
Use of new roads and trails from
immigration and enforcement activities,
as well as the construction, use, and
maintenance of enforcement
infrastructure (i.e., fences, walls, and
lighting systems), leads to compaction
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of streamside soils, and the destruction
and removal of riparian vegetation
necessary as cover for the northern
Mexican gartersnake. These activities
also serve as a source of additional
sediment to streams that affect their
suitability as habitat for prey species of
the northern Mexican gartersnake and
affect the suitability and availability of
pool habitats by filling them in with
sediment. Riparian areas along the
upper San Pedro River have been
impacted by out of control fires that
undocumented immigrants likely
started to keep warm and/or prepare
food (Segee and Neeley 2006, p. 23).
There also remains the threat of pursuit,
capture, and death of northern Mexican
gartersnakes when they are encountered
by undocumented immigrants and
border enforcement personnel in high
use areas due to the snake’s stigma in
society (Rosen and Schwalbe 1988, p.
43; Ernst and Zug 1996, p. 75; Green
1997, pp. 285–286; Nowak and Santana
Bendix 2002, p. 39).
The wetland habitat within the San
Bernardino National Wildlife Refuge has
been adversely affected by
undocumented immigration. It is
estimated that approximately 1,000
undocumented immigrants per month
use these important wetlands for
bathing, drinking, and other uses during
their journey northward. These
activities can contaminate the water
quality of the wetlands and lead to
reductions in the prey base for the
northern Mexican gartersnake, as well
as increase exposure of the snake to
humans, and thereby increase direct
mortality rates (Rosen and Schwalbe
1988, p. 43; Ernst and Zug 1996, p. 75;
Green 1997, pp. 285–286; Nowak and
Santana-Bendix 2002, p. 39; Segee and
Neeley 2006, pp. 21–22). In addition,
numerous observations of littering and
destruction of vegetation and wildlife
occur annually throughout the San
Bernardino National Wildlife Refuge,
which adversely affect the quality and
quantity of vegetation as habitat for the
northern Mexican gartersnake (USFWS
2006, p. 95).
There remains the possibility that
adverse effects to riparian communities
may increase in the future as land
access and infrastructure restrictions in
sensitive wildlife areas may be relaxed
according to proposed policy changes
that aim to boost border enforcement
activities in these currently roadless
areas and as concentrated enforcement
efforts in urban locations funnel more
undocumented immigrant traffic to
remote wilderness areas (Segee and
Neeley 2006, pp. 15–16).
Habitat Threats in Mexico. Threats to
northern Mexican gartersnake habitat in
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Mexico include the intentional and
unintentional introductions of
nonnative species, improper livestock
grazing, urbanization and development,
water diversions and groundwater
pumping, loss of vegetation cover and
deforestation, erosion, and pollution, as
well as impoundments and dams that
have modified or destroyed riparian and
aquatic communities within Mexico in
areas where the species occurred
historically (Conant 1974, p. 471;
Contreras Balderas and Lozano 1994, p.
384; va Landa et al. 1997, p. 316; Miller
et al. 2005, pp. 60–61; Abarca 2006). We
experienced difficulty finding specific
information documenting that
populations of northern Mexican
gartersnakes in Mexico are directly
affected by these threats which is
problematic in a rangewide analysis
given that approximately 70 to 80
percent of the historic distribution of
the northern Mexican gartersnake
occurs in Mexico. We did, however,
find enough information to provide
some refined discussion of smaller
geographic areas within Mexico, and
acknowledge that many of the threats
that affect the northern Mexican
gartersnake in the United States also
occur in Mexico and could affect the
northern Mexican gartersnake in similar
ways but at potentially varying
intensities.
Conant (2003, p. 4) noted
anthropogenic threats to seven
fragmented, endemic subspecies of
Mexican gartersnake in the
Transvolcanic Belt Region of southern
Mexico, which extends from southern
Jalisco eastward through the state of
´
Mexico to central Veracruz which
comprises a small proportion of the
subspecies’ range. Although Conant
(2003) addresses threats to a small
percentage of the historic distribution,
many of these rural land uses are
regionally ubiquitous and therefore
these threats can be extrapolated to the
surrounding vicinity of the distribution
of these seven recently described
subspecies of the Mexican gartersnake
in Mexico. Some of these threats
included water diversions, pollution
(e.g., discharge of raw sewage),
sedimentation of aquatic habitats, and
eutrophication (increase of dissolved
nutrients and decrease of dissolved
oxygen) of lentic (still water) habitats.
Conant (2003, p. 4) expressed great
concern that while many of these threats
were evident during his field work in
the 1960s, they are ‘‘continuing with
increased velocity.’’
Water pollution, dams, groundwater
pumping, and impoundments were
identified by Miller et al. (2005, pp. 60–
61) as significant threats to aquatic
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biota. 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 [where the northern Mexican
gartersnake is distributed] such as the
´
Rıo Grande de Santiago below
´
Guadalajara (Jalisco) and Rıo Colorado
downstream of Hoover (Boulder) Dam,
have simply been destroyed by
pollution and river alteration.’’ Near
´
Torreon, Coahuila, where the northern
Mexican gartersnake was historically
distributed, groundwater pumping has
resulted in flow reversal, which has
driedup many local springs, drawn
arsenicladen water, further
contaminated the area, and resulted in
adverse human health effects in that
area. Severe water pollution from
untreated domestic waste is evident
downstream of large Mexican cities, and
inorganic pollution from nearby
industrialized areas and agricultural
irrigation return flow has dramatically
affected aquatic communities (Miller et
al. 2005, p. 60). Miller et al. (2005, p. 61)
provides an excerpt from Soto Galera et
al. (1999) addressing the threats to the
´
Rıo Lerma (Mexico’s longest river)
where the northern Mexican gartersnake
was historically distributed: ‘‘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 Rıo Lerma basin matches or exceeds
the worst cases reported for comparably
sized basins elsewhere in the world.’’
Several rivers within the historic
distribution of the northern Mexican
gartersnake have been impounded and
dammed throughout Mexico, resulting
in habitat modification and the
dispersal and establishment of
nonnative species. The damming and
´
modification of the Rıo Colorado, where
the northern Mexican gartersnake was
distributed, has facilitated the
replacement of the entire native fishery
with nonnative species (Miller et al.
2005, p. 61). Nonnative species continue
to pose significant threats in the decline
of native, often endemic, prey species of
the northern Mexican gartersnake in
several regions of Mexico, as discussed
further in Factor C below (Miller et al.
2005, p. 60).
Miller et al. (2005) does provide some
locality specific information on the
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status and threats of freshwater fishes
and riparian and aquatic communities
in specific waterbodies throughout
Mexico that historically overlapped, or
are adjacent to, the historic distribution
of the northern Mexican gartersnake: the
´
Rıo Grande (dam construction, p. 78);
´
the Rıo Bravo (extirpations, pp. 82, 112);
´
headwaters of the Rıo Lerma
(extinction/rediscovery, nonnatives,
pollution, dewatering, pp. 60, 105, 197);
´
Lago de Chapala and its outlet to the Rıo
Grande de Santiago (major declines, p.
106); medium-sized streams throughout
the Sierra Madre Occidental (localized
extirpations, logging, dewatering, pp.
´
109, 177, 247); the Rıo Conchos
´
(extirpations, p. 112); the rıos Casas
´
Grandes, Santa Marıa, del Carmen, and
Laguna Bustillos (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
´
(nonnatives, pp. 148, Plate 61); the Rıo
´
Colorado (nonnatives, p. 153); the rıos
´
Fuerte and Culiacan (logging, p. 177);
canals, ponds, lakes in the endorheic
´
(closed) Valle de Mexico (nonnatives,
extirpations, pollution, pp. 197, 281);
´
the Rıo Verde Basin (dewatering,
nonnatives, extirpations, Plate 88); the
´
Rıo Mayo (dewatering, nonnatives, p.
´
247); the Rıo Papaloapan (pollution, p.
252); lagos de Zacapu and Yuriria
´
(habitat destruction, p. 282); and the Rıo
´
Panuco Basin (nonnatives, p. 295).
Conant (1974, pp. 486–489) described
significant threats to northern Mexican
gartersnake habitat within its historical
distribution in various locations in
western Chihuahua, Mexico, and within
the Rio Concho system where it is
known to occur. These threats
specifically included impoundments,
diversions, and purposeful
introductions of largemouth bass,
common carp, and bullfrogs. We discuss
the threats from nonnative species
introductions below in our discussion of
Factor C. McCranie and Wilson (1987,
p. 2) discuss threats to the pine-oak
communities of higher elevation
habitats in the Sierra Madre Occidental,
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, especially if the
road is paved as has been the case with
(Mexican) Highway 40 through southern
Durango. We feel fortunate to have
worked in an area of this country of
rapid population growth that is all too
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fast disappearing.’’ In Mexico, as
compared to the United States, there is
believed to be a delay in the magnitude
and significance of adverse effects to
riparian communities, but it is believed
that threats to riparian and aquatic
communities that have been observed in
Arizona as described below are
currently occurring with increasing
significance in several regions across
Mexico within the historic distribution
of the northern Mexican gartersnake
(Conant 1974, pp. 471, 487–489;
Contreras Balderas and Lozano 1994,
pp. 379–381; va Landa et al. 1997,
p. 316; Miller et al. 2005, p. 60–61;
Abarca 2006; Rosen 2006).
Collectively, the impacts described
above are expected to continue as a
result of Mexico’s expanding role as an
economical labor force for international
manufacturing under the North
American Free Trade Agreement
(NAFTA) and the subsequent increase
in population size, economic growth
and development, and infrastructure.
Mexico’s human population grew 700
percent from 1910 to 2000 (Miller et al.
2005, p. 60). More recently, Mexico’s
population increased by 245 percent
from 1950 to 2002, and is projected to
grow by another 28 percent by 2025
(EarthTrends 2005). As of 1992, Mexico
had the second highest gross domestic
product in Latin America at 5.8 percent,
following Brazil (DeGregorio 1992,
p. 60). As a result of NAFTA, the
number of maquiladoras (export
assembly plants) is expected to increase
by as many as 3,000 to 4,000 (Contreras
Balderas and Lozano 1994, p. 384). To
accommodate Mexico’s increasing
population, rural areas are largely
devoted to food production based on
traditional methods, which has led to
serious losses in vegetative cover and
soil erosion (va Landa et al. 1997,
p. 316). To increase forage and stocking
rates for livestock production in the arid
lowlands of northern Mexico, African
buffelgrass (Pennisetum ciliare) was
widely introduced in Mexico and has
´
spread on its own (Burquez-Montijo et
al. 2002, p. 131). Buffelgrass invasions
pose a serious threat to native arid
ecosystems because buffelgrass prevents
germination of native species, competes
for water, crowds out native vegetation,
and creates fine fuels in vegetation
communities not adapted to fire; in such
native arid ecosystems, buffelgrass has
caused many changes, including severe
´
soil erosion (Burquez-Montijo et al.
2002, pp. 135, 138). Erosion affects the
suitability of habitat for northern
Mexican gartersnakes and their prey
species. Recent estimates indicate that
80 percent of Mexico is affected by soil
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erosion with the most serious erosion
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) (va Landa et al. 1997, p. 317), the
states in which the northern Mexican
gartersnake historically occurred.
The threats to riparian and aquatic
communities in Mexico (such as the
intentional and unintentional
introductions of nonnative species,
improper livestock grazing, urbanization
and development, water diversions and
groundwater pumping, loss of
vegetation cover and deforestation,
erosion, pollution, impoundments, and
dams) vary in their significance both
geographically and ecologically, based
on geographical distribution of land
management activities and urban
centers, but are expected to continue
into the future. Threats that affect the
amount of water within an occupied
area directly affect its suitability to
northern Mexican gartersnakes. Threats
that alter the vegetation of occupied
habitat reduce the habitat’s suitability as
cover for protection from predators, as
a foraging area, and as an effective
thermoregulatory site. Nonnative
species, explained further in our Factor
C discussion, compete with the northern
Mexican gartersnake for prey as well as
prey on juvenile and sub-adult northern
Mexican gartersnakes, which hampers
the recruitment of young snakes into the
population and lessens the viability of
that population over time. However,
because specific and direct survey
information is significantly limited
concerning the presence and potential
effect of these threats to the subspecies
in Mexico, this discussion is based on
extrapolation of how we understand
these threats to affect the subspecies in
the United States. Furthermore, the
subspecies was historically distributed
in several regions within Mexico that
have remained roadless and isolated,
thus suggesting that the severity of
threats may be less than that found
within the range in United States where
lands have greater past and current
economic pressures such as grazing and
development. As such we can not
conclude that the subspecies is likely to
become endangered throughout its range
in Mexico. Although we acknowledge
that these threats are affecting the
subpecies in the United States, we have
determined that the portion of the
subspecies’ range in the United States
does not constitute a significant portion
of the range of the subspecies or a DPS.
Therefore, on the basis of the best
available information, we determine
that it is not likely that the northern
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Mexican gartersnake will become an
endangered species within the
foreseeable future based on threats
under this factor.
B. Overutilization for commercial,
recreational, scientific, or educational
purposes
The northern Mexican gartersnake
may not be collected in the United
States without special authorization by
the Arizona Game and Fish Department
or the New Mexico Department of Game
and Fish. We have found no evidence
that current or historical levels of lawful
or unlawful field collecting of northern
Mexican gartersnakes has played a
significant role in the decline of this
species. The Arizona Game and Fish
Department recently produced field
identification cards for distribution that
provide information to assist with the
field identification of each of Arizona’s
five native gartersnake species as well as
guidance on submitting photo vouchers
for university museum collections.
Additionally, universities such as
Arizona State University and the
University of Arizona recently began to
accept photo voucher record, versus
physical specimens, in their respective
museum collections. We believe these
measures further reduce the necessity
for field biologists to collect physical
specimens (unless discovered
postmortem) for locality voucher
purposes and therefore further reduce
impacts to vulnerable populations from
formal biological field investigations
and field specimen collections. We were
unable to obtain any information about
the effect of overutilization for
commercial, recreational, scientific, or
educational purposes in Mexico.
Specific discussion of the regulatory
protections for the northern Mexican
gartersnake is provided under Factor D
‘‘Inadequacy of Existing Regulatory
Mechanisms’’ below.
C. Disease or Predation
Disease
Disease in northern Mexican
gartersnakes has not yet been
documented as a specific threat in the
United States or Mexico. However,
because little is known about disease in
wild snakes, it is premature to conclude
that there is no disease threat that could
directly affect remaining northern
Mexican gartersnake populations (Rosen
2006).
Disease and nonnative parasites have
been implicated in the decline in the
prey base of the northern Mexican
gartersnake. The outbreak of chytrid
fungus (of the genus Batrachochytrium)
has been identified as a chief causative
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agent in the significant declines of many
of the native ranid frogs and other
amphibian species, and regional
concerns exist for the native fish
community due to nonnative parasites
such as the Asian tapeworm
(Bothriocephalus achelognathi) in
southeastern Arizona (Rosen and
Schwalbe 1997, pp. 14–15; 2002c, pp.
1–19; Morell 1999, pp. 728–732; Sredl
and Caldwell 2000, p. 1; Hale 2001, pp.
32–37; Bradley et al. 2002, p. 206). The
chytrid fungus 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 the chytrid fungus
a serious threat to amphibian diversity.
In Arizona, chytrid infections have been
reported in several northern Mexican
gartersnake native prey species (Morell
1999, pp. 731–732; Sredl and Caldwell
2000, p. 1; Hale 2001, pp. 32–37;
Bradley et al. 2002, p. 207; USFWS
2002a, pp. 40802–40804). Declines of
native prey species of the northern
Mexican gartersnake from chytrid
infections have contributed to the
decline of this species in the United
States. However, we do not have
specific information regarding potential
impacts of chytrid infections on
northern Mexican gartersnake native
prey species in Mexico.
We also note that in a pure culture
(uncontaminated growth medium), the
fungus Batrachochytrium can grow on
boiled snakeskin (keratin), which
indicates the potential for the fungus to
live saprobically (obtaining nutrients
from non-living organic matter,
commonly dead and decaying plant or
animal matter, by absorbing soluble
organic compounds) on gartersnake skin
in the wild if other components of the
ecosystem limit the growth of
competing bacteria and oomycetes (a
taxonomic group of fungi that produce
oospores such as the genera Pythium,
Phytophthora, and Aphanomyces)
(Longcore et al. 1999, p. 227). While the
genus Batrachochytrium has been
grown on snakeskin in the laboratory,
no reports of the organism on reptilian
hosts in the wild have been
documented. We anticipate diligence in
monitoring the status of incidence of
this disease in this species in the wild
for early detection purposes should this
potential threat come to fruition in wild
populations of northern Mexican
gartersnakes.
Nonnative Species Interactions
A host of native predators prey upon
northern Mexican gartersnakes
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including birds of prey, other snakes
[kingsnakes (Lampropeltis sp.),
whipsnakes (Masticophis sp.), etc.],
wading birds, raccoons (Procyon lotor),
skunks (Mephitis sp.), and coyotes
(Canis latrans) (Rosen and Schwalbe
1988, p. 18). However, nonnative
species, such as the bullfrog, the
northern (virile) (Orconectes virilis) and
red swamp (Procambarus clarki)
crayfish, and numerous species of exotic
sport and bait fish species continue to
be the most prominent threat to the
northern Mexican gartersnake and to its
prey base from direct predation,
competition, and modification of habitat
in the United States and potentially in
Mexico (Conant 1974, pp. 471, 487–489;
Meffe 1985, pp. 179–185; Rosen and
Schwalbe 1988, pp. 28, 32; 1997, p. 1;
Bestgen and Propst 1989, pp. 409–410;
Clarkson and Rorabaugh 1989, pp. 531,
535; Marsh and Minckley 1990, p. 265;
Stefferud and Stefferud 1994, p. 364;
Rosen et al. 1995, pp. 257–258; 1996b,
pp. 2, 11–13; 2001, p. 2; Degenhardt et
al. 1996, p. 319; Fernandez and Rosen
1996, pp. 8, 23–27; Weedman and
Young 1997, pp. 1, Appendices B, C;
Inman et al. 1998, p. 17; Rinne et al.
1998, pp. 4–6; Fagan et al. 2005, pp. 34,
34–41; Olden and Poff 2005, pp. 82–87;
Unmack and Fagan 2004, p. 233; Miller
et al. 2005, pp. 60–61; Abarca 2006;
Brennan and Holycross 2006, p. 123;
Holycross et al. 2006, pp. 13–15; Rosen
and Melendez 2006, p. 54).
Nonnative Species Interactions in the
United States. Nonnative species
represent serious threats to the northern
Mexican gartersnake through
competition for prey, direct predation,
and alteration of habitat. Riparian and
aquatic communities have been
dramatically impacted by a shift in
species’ composition. Specifically,
riparian and wetland communities have
experienced a shift from being
historically dominated by native fauna
to being increasingly occupied by an
expanding assemblage of nonnative
plant and animal species that have been
intentionally or accidentally introduced,
or have colonized new areas from
neighboring occupied localities. For
example, nonnative shrub species in the
genus Tamarix have been widely
introduced throughout the western
States and appear to thrive in regulated
river systems (Stromberg and Chew
2002, pp. 210–213). Tamarix invasions
may result in habitat alteration from
potential effects to water tables, changes
to canopy and ground vegetation
structures, and increased fire risk,
which hasten the demise of native
cottonwood and willow communities
and affect the suitability of the
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vegetation component to northern
Mexican gartersnake habitat (Stromberg
and Chew 2002, pp. 211–212; USFWS
2002b, p. H–9).
Declines in the Northern Mexican
Gartersnake Anuran Prey Base in the
United States. The decline of the
northern Mexican gartersnake within its
historical and extant distribution was
subsequent to the declines in its prey
base (native amphibian and fish
populations) from introductions of
nonnative bullfrogs, crayfish, and
numerous species of exotic sport and
bait fish as documented in an extensive
body of literature (Nickerson and Mays
1970, p. 495; Hulse 1973, p. 278; Vitt
and Ohmart 1978, p. 44; Meffe 1985, pp.
179–185; Ohmart et al. 1988, pp. 143–
147; Rosen and Schwalbe 1988, pp. 28–
31; 1997, pp. 8–16; Bestgen and Propst
1989, pp. 409–410; Clarkson and
Rorabaugh 1989, pp. 531–538; Marsh
and Minckley 1990, p. 265; Sublette et
al. 1990, pp. 112, 243, 246, 304, 313,
318; Stefferud and Stefferud 1994, p.
364; Holm and Lowe 1995, p. 5; Rosen
et al. 1995, pp. 251, 257–258; 1996a, pp.
2–3; 1996b, p. 2; 2001, p. 2; Sredl et al.
1995a, pp. 7–8; 1995b, pp. 8–9; 1995c,
pp. 7–8; 2000, p. 10; Degenhardt et al.
1996, p. 319; Fernandez and Rosen
1996, pp. 8–27; Drost and Nowak 1997,
p. 11; Weedman and Young 1997, pp. 1,
Appendices B, C; Inman et al. 1998, p.
17; Rinne et al. 1998, pp. 4–6; Turner et
al. 1999, p. 11; Nowak and Spille 2001,
p. 11; Bonar et al. 2004, p. 3; Fagan et
al. 2005, pp. 34, 34–41; Olden and Poff
2005, pp. 82–87; Holycross et al. 2006,
pp. 13–15, 52–61; Brennan and
Holycross 2006, p. 123). The northern
Mexican gartersnake is particularly
vulnerable to a loss in native prey
species (Rosen and Schwalbe 1988, p.
20). Rosen et al. (2001, pp. 10, 13, 19)
examined this issue in detail and
proposed a hypothesis involving two
reasons for the decline in northern
Mexican gartersnakes following the loss
or decline in the native prey base: (1)
The northern Mexican gartersnake is
unlikely to increase foraging efforts at
the risk of increased predation; and (2)
the species needs substantial food
regularly to maintain its weight and
health. If forced to forage more often for
smaller prey items, a reduction in
growth and reproductive rates will
result (Rosen et al. 2001, pp. 10, 13).
Native ranid frog species such as
lowland leopard frogs, northern leopard
frogs, and federally threatened
Chiricahua leopard frogs have all
experienced significant declines
throughout their distribution in the
Southwest, partially due to predation
and competition with nonnative species
(Clarkson and Rorabaugh 1989, pp. 531,
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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 and
without corrective action, predicted that
the Chiricahua leopard frog will be
extirpated from this region. 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 community and
that native frog populations in another
19 sites (33 percent) had been
completely displaced by invading
bullfrogs.
Declines in the native leopard frog
populations in Arizona have
significantly contributed to declines in
the northern Mexican gartersnake, as a
primary native predator. Scotia Canyon
in the Huachuca Mountains of
southeastern Arizona is a location
where corresponding declines between
leopard frog and northern Mexican
gartersnake populations has 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 apparently extirpated
by the early 1990s (Holm and Lowe
1995, pp. 45–46). Northern Mexican
gartersnakes in low numbers were
observed in decline during the early
1980s with low capture rates remaining
through the early 1990s (Holm and
Lowe 1995, pp. 27–35). Surveys
documented further decline in 2000
(Rosen et al. 2001, pp. 15–16). A former
stronghold for the northern Mexican
gartersnake, the San Bernardino
National Wildlife Refuge has also been
affected by correlative declines between
leopard frog and northern Mexican
gartersnake populations (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).
Declines of leopard frog populations,
often correlated with nonnative species
introductions (but also with the spread
of chytridiomycosis, symptomatic
disease caused by the chytrid fungus,
and habitat modification and
destruction), has not just occurred
throughout southeastern Arizona, but
throughout much of the U.S.
distribution of the northern Mexican
gartersnake based on survey data
(Nickerson and Mays 1970, p. 495; Vitt
and Ohmart 1978, p. 44; Ohmart et al.
1988, p. 150; Rosen and Schwalbe 1988,
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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). Specifically,
Holycross et al. (2006, pp. 53–57, 59)
recently documented extirpations of the
northern Mexican gartersnake’s native
leopard frog prey base at several
currently 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
watershed) in the vicinity of the Forest
Service Cabin, at the Page Springs and
Bubbling Ponds fish hatchery along Oak
Creek, Sycamore Creek (Verde River
watershed) 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.’’
Rosen et al. (2001, p. 22) concluded
that the presence and expansion of
nonnative predators (mainly bullfrogs,
crayfish, and green sunfish) are the
primary causes of decline in northern
Mexican gartersnakes in southeastern
Arizona. Specifically, the authors
identified the expansion of bullfrogs
into the Sonoita grasslands (the
threshold to the Canelo Hills) and the
introduction of crayfish into Lewis
Springs as being of particular concern in
terms of future recovery efforts for the
northern Mexican gartersnake. It should
also be noted that Rosen et al. (2001,
Appendix I) documented the decline of
several native fish species in several
locations visited, further affecting the
prey base of northern Mexican
gartersnakes. Rosen et al. (1995, pp.
252–253) sampled 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 aquatic and
semi-aquatic vertebrate species detected
were nonnative. The most commonly
encountered nonnative species was the
bullfrog (Rosen et al. 1995, p. 254).
Declines in the Northern Mexican
Gartersnake Native Fish Prey Base in
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the United States. Native fish species
such as the federally endangered Gila
chub, petitioned roundtail chub, and
federally endangered Gila topminnow
are among the primary prey species for
the northern Mexican gartersnake
(Rosen and Schwalbe 1988, p. 18).
Similar to bullfrogs, predatory
nonnative fish species such as
largemouth bass also prey upon juvenile
northern Mexican gartersnakes.
Additionally both nonnative sport and
bait compete with the northern Mexican
gartersnake in terms of its native fish
and native anuran prey base. 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 gartersnakes). Holycross et al.
(2006, pp. 53–55) recently documented
significantly depressed or extirpated
native fish prey bases for the northern
Mexican gartersnake along the Agua
Fria in the vicinity of Table Mesa Road
and the Little Grand Canyon Ranch,
along Dry Creek from Dugas Road to
Little Ash Creek, along Little Ash Creek
from Brown Spring to Dry Creek, along
Sycamore Creek (Agua Fria watershed)
in the vicinity of the Forest Service
Cabin, and along Sycamore Creek
(Verde River watershed) in the vicinity
of its confluence with the Verde River
north of Clarkdale.
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 captured in the
listing rules of 13 native species listed
under the Act whose historical ranges
overlap with the historical distribution
of the northern Mexican gartersnake.
These native fish species were likely
prey species for the northern Mexican
gartersnake, including: bonytail chub
(Gila elegans, 45 FR 27710, April 23,
1980), Yaqui catfish (Ictalurus pricei, 49
FR 34490, August 31, 1984), 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), humpback chub (Gila
cypha, 32 FR 4001, March 11, 1967),
Gila chub (Gila intermedia, 70 FR
66663, November 2, 2005), Colorado
pikeminnow (Ptychocheilus lucius, 32
FR 4001, March 11, 1967), spikedace
(Meda fulgida, 51 FR 23769, July 1,
1986), loach minnow (Tiaroga cobitis,
51 FR 39468, October 28, 1986),
razorback sucker (Xyrauchen texanus,
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56 FR 54957, October 23, 1991), desert
pupfish (Cyprinodon macularius, 51 FR
10842, March 31, 1986), and Gila
topminnow (Poeciliopsis occidentalis
occidentalis, 32 FR 4001, March 11,
1967)]. In total within Arizona, 19 of 31
(61 percent) of native fish species are
listed under the Act. Arizona ranks the
highest of all 50 States in the percentage
of native fish species at risk (85.7
percent, Stein 2002, p. 21).
Fragmentation of extant listed native
fish populations is exacerbating the
decline of these species and may
preclude their recovery as well as
continue to affect their role in the prey
base of northern Mexican gartersnakes.
Fagan et al. (2005, pp. 34–41) examined
the correlation between fragmentation of
extant distributions and the relative risk
of extinction of any given species. They
found the strongest correlation to risk of
extinction due to fragmentation of fish
populations occurred at the
intermediate to large spatial scales,
which geographically correspond to
tributaries and river basins (Fagan et al.
2005, p. 38). At this range in spatial
scale, the effects of dam building, water
diversions, and introduced nonnatives
appear to be significant factors
exacerbating the fragmentation by acting
as barriers to the exchange of genetic
material among listed fish populations
(Fagan et al. 2005, pp. 38–39).
Olden and Poff (2005, p. 75) stated
that environmental degradation and the
proliferation of nonnative fish species
threaten the endemic and unique fish
faunas of the American Southwest. The
fastest expanding nonnative species are
red shiner (Cyprinella lutrensis), fathead
minnow (Pimephales promelas), green
sunfish (Lepomis cyanellus), largemouth
bass (Micropterus salmoides), western
mosquitofish, and channel catfish
(Ictalurus punctatus). 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 (Micropterus
dolomieue), have been introduced into
formerly and currently occupied
northern Mexican gartersnake habitat
(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, Appendices B, C; Voeltz
2002, p. 88; Bonar et al. 2004, pp. 1–
108).
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Several authors have identified both
the presence of nonnative fish species as
well as their deleterious effects on
native species within Arizona. 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
influence in the lower reaches where
the northern Mexican gartersnake is
considered extant. At the Gisela
sampling point, four of six sampling
attempts resulted in no fish captured; of
the 41 fish captured in the remaining
two attempts, 90 percent were
nonnative, including 28 fathead
minnows, 5 green sunfish, 3 red shiner,
and 1 yellow bullhead. Surveys in the
Salt River above Lake Roosevelt indicate
a decline of roundtail chub and other
natives 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 roundtail chub
populations (Voeltz 2002, p. 40).
A report provided by Bonar et al.
(2004, pp. 1–108) is the most current
and perhaps one of the most complete
assessments of native and nonnative
fish species interactions in the Verde
River mainstem. Overall, Bonar et al.
(2004, p. 57) found that nonnative fishes
were approximately 2.6 times more
dense per unit volume of river than
native fishes, and their standing crop
was approximately 2.8 times that of
native fishes per unit volume of river.
Bonar et al. (2004, p. 79) verified the
findings of Voeltz (2002, pp. 71, 88), in
stating that red shiner were the most
commonly encountered nonnative fish
species in the Verde River by almost
four-fold; they found the species to be
present throughout the Verde River
year-around, but noted the highest
numbers in the reach between Beasley
Flat to Sheep Bridge above Horseshoe
Reservoir in riffle habitats. River reaches
above Horseshoe Reservoir have
resident self-sustaining populations of
bass, green sunfish, catfish, and carp,
with a low, unstable native fish
community, which results in fewer
native fish predation observations in
sampling results for this reach (Bonar et
al. 2004, pp. 80, 87). Reaches below
Bartlett Reservoir had both high native
and nonnative fish abundance, which
resulted in more frequent observations
of nonnative predation on native fish
according to Bonar et al. (2004, p. 87).
Lastly, Bonar et al. (2004, p. 6) found
that channel and flathead catfish, green
sunfish, largemouth and smallmouth
bass, and yellow bullhead had the
highest rates of piscivory (fish
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predation) on native and nonnative fish
species in all river reaches; of these
species, largemouth bass were
documented as the most significant
predator on native fish.
Northern Mexican gartersnakes can
successfully use some nonnative
species, such as mosquitofish and red
shiner, as prey species. However, all
other nonnative species, most notably
the spiny-rayed fish, are not considered
prey species for the northern Mexican
gartersnake. These nonnative species
can be difficult to swallow due to their
body shape and spiny dorsal fins, are
predatory on juvenile gartersnakes, and
reduce the abundance of or completely
eliminate native fish populations. This
is particularly important in the wake of
a stochastic event such as flooding,
extreme water temperatures, or
excessive turbidity. Native fish are
adapted to the dramatic fluctuations in
water conditions and flow regimes and
persist in the wake of stochastic events
as a prey base for the northern Mexican
gartersnake. Nonnative fish, even
species that may be used as prey by the
northern Mexican gartersnake, generally
are ill-adapted to these conditions and
may be removed from the area
temporarily or permanently, depending
on the hydrologic connectivity to extant
populations. If an area is solely
comprised of nonnative fish, the
northern Mexican gartersnake may be
faced with nutritional stress or
starvation. The most conclusive
evidence for the northern Mexican
gartersnake’s intolerance for nonnative
fish remains in the fact that, in most
incidences, nonnative fish species
generally do not occur in the same
locations as the northern Mexican
gartersnake and its native prey species.
Bullfrog Diet and Distribution in the
United States. Bullfrogs are widely
considered one of the most serious
threats to the northern Mexican
gartersnake throughout its range (Conant
1974, pp. 471, 487–489; Rosen and
Schwalbe 1988, pp. 28–30; Rosen et al.
2001, pp. 21–22). Bullfrogs adversely
affect northern Mexican gartersnakes
through direct predation of juvenile and
sub-adults and from competition with
native prey species. Bullfrogs first
appeared in Arizona in 1926, as a result
of a systematic introduction effort by the
State Game Department (now, the
Arizona Game and Fish Department) for
the purposes of sport hunting and as a
food source. (Tellman 2002, p. 43). By
1982, the Arizona Game and Fish
Department had systematically
introduced some 682,000 bullfrog
tadpoles into streams throughout the
State (Tellman 2002, p. 43). Bullfrogs
are extremely prolific, adept at
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colonizing new areas, and may disperse
to distances of 6.8 miles (10.9 km) and
likely further within drainages (Bautista
2002, p. 131; Rosen and Schwalbe
2002a, p. 7; Casper and Hendricks 2005,
p. 582). Batista (2002, p. 131) confirmed
‘‘the strong colonizing skills of the
bullfrog and that the introduction of this
exotic species can disturb local anuran
communities.’’
Bullfrogs are voracious, opportunistic,
even cannibalistic predators that readily
attempt to consume any animal smaller
than themselves, including conspecifics
(other species within the same genus)
which can encompass 80 percent of
their diet (Casper and Hendricks 2005,
p. 543). Bullfrogs have demonstrated
astonishing variability in their diet,
which has been documented to include
vegetation, earthworms, leeches, insects,
centipedes, millipedes, spiders,
scorpions, crayfish, snails, numerous
species of larval and metamorphosed
amphibians, fish, small alligators,
turtles, lizards, numerous species of
snakes [seven genera; including six
different species of gartersnakes, two
species of rattlesnakes, and Sonoran
gophersnakes (Pituophis catenifer
affinis)], small mammals (e.g.,
chipmunks, cotton rats, shrews, mice,
and voles), numerous species of birds,
bats, muskrats, and even juvenile mink
(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, p. 544; Combs et al.
2005, p. 439; Wilcox 2005, p. 306).
Bullfrogs have been documented
throughout the State of Arizona.
Holycross et al. (2006, pp. 13–14, 52–61)
found bullfrogs at 55 percent of sample
sites in the Agua Fria watershed, 62
percent of sites in the Verde River
watershed, 25 percent of sites in the Salt
River watershed, and 22 percent of sites
in the Gila River watershed. 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
documented the presence of bullfrogs
through their survey efforts Statewide in
specific regional areas, drainages, and
disassociated wetlands that include the
Kaibab National Forest (Sredl et al.
1995a, p. 7); the Coconino National
Forest (Sredl et al. 1995c, p. 7); the
White Mountain Apache Reservation
(Hulse 1973, p. 278); Beaver Creek
(tributary to the Verde River) (Drost and
Nowak 1997, p. 11); the Watson Woods
Riparian Preserve near Prescott (Nowak
and Spille 2001, p. 11); the Tonto
National Forest (Sredl et al. 1995b, p. 9);
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the Lower Colorado River (Vitt and
Ohmart 1978, p. 44; Clarkson and DeVos
1986, pp. 42–49; Ohmart et al. 1988, p.
143); the Huachuca Mountains (Rosen
and Schwalbe 1988, Appendix I; Holm
and Lowe 1995, pp. 27–35; Sredl et al.
2000, p. 10; Rosen et al. 2001, Appendix
I); the Pinaleno Mountains region
(Nickerson and Mays 1970, p. 495); the
San Bernardino National Wildlife
Refuge (Rosen and Schwalbe 1988,
Appendix I; 1995, p. 452; 1996, pp. 1–
3; 1997, p. 1; 2002b, pp. 223–227;
2002c, pp. 31, 70; Rosen et al. 1995, p.
254; 1996b, pp. 8–9; 2001, Appendix I);
the Buenos Aires National Wildlife
Refuge (Rosen and Schwalbe 1988,
Appendix I); the Arivaca Area (Rosen
and Schwalbe 1988, Appendix I; Rosen
et al. 2001, Appendix I); Cienega Creek
drainage (Rosen et al. 2001, Appendix
I); Babocamari River drainage (Rosen et
al. 2001, Appendix I); Turkey Creek
drainage (Rosen et al. 2001, Appendix
I); O’Donnell Creek drainage (Rosen et
al. 2001, Appendix I); Audubon
Research Ranch near Elgin (Rosen et al.
2001, Appendix I); Santa Cruz River
drainage (Rosen and Schwalbe 1988,
Appendix I; Rosen et al. 2001,
Appendix I); San Rafael Valley (Rosen et
al. 2001, Appendix I); San Pedro River
drainage (Rosen and Schwalbe 1988,
Appendix I; Rosen et al. 2001,
Appendix I); Bingham Cienega (Rosen et
al. 2001, Appendix I); Sulfur Springs
Valley (Rosen et al. 1996a, pp. 16–17);
Whetstone Mountains region (Turner et
al. 1999, p. 11); Aqua Fria River
drainage (Rosen and Schwalbe 1988,
Appendix I; Holycross et al. 2006, pp.
13, 15–18, 52–53); Verde River drainage
(Rosen and Schwalbe 1988, Appendix I;
Holycross et al. 2006, pp. 13, 26–28, 55–
56); greater metropolitan Phoenix area
(Rosen and Schwalbe 1988, Appendix
I); greater metropolitan Tucson area
(Rosen and Schwalbe 1988, Appendix
I); Sonoita Creek drainage (Rosen and
Schwalbe 1988, Appendix I); Sonoita
Grasslands (Rosen and Schwalbe 1988,
Appendix I); Canelo Hills (Rosen and
Schwalbe 1988, Appendix I); Pajarito
Mountains (pers. observation, J. Servoss,
Fish and Wildlife Biologist, U.S. Fish
and Wildlife Service); Picacho Reservoir
(Rosen and Schwalbe 1988, Appendix
I); Dry Creek drainage (Holycross et al.
2006, pp. 19, 53); Little Ash Creek
drainage (Holycross et al. 2006, pp. 19,
54); Oak Creek drainage (Holycross et al.
2006, pp. 23, 54); Sycamore Creek
drainages (Holycross et al. 2006, pp. 20,
25, 54–55); Rye Creek drainage
(Holycross et al. 2006, pp. 37, 58);
Spring Creek drainage (Holycross et al.
2006, pp. 25, 59); Tonto Creek drainage
(Holycross et al. 2006, pp. 40–44, 59);
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San Francisco River drainage (Holycross
et al. 2006, pp. 49–50, 61); and the
upper Gila River drainage (Holycross et
al. 2006, pp. 45–50, 60–61).
Perhaps one of the most serious
consequences of bullfrog introductions
is their persistence in an area once they
have become established, and the
subsequent difficulty in eliminating
bullfrog populations. Rosen and
Schwalbe (1995, p. 452) experimented
with bullfrog removal at various sites on
the San Bernardino National Wildlife
Refuge in addition to a control site with
no bullfrog removal in similar habitat on
the Buenos Aires National Wildlife
Refuge. Removal of adult bullfrogs
resulted in a substantial increase in
younger age-class bullfrogs where
removal efforts were the most intensive
(Rosen and Schwalbe 1997, p. 6).
Evidence from dissection samples from
young adult and sub-adult 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 (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).
Consequently, this strategy was viewed
as being potentially ‘‘self-defeating’’ and
‘‘counter-productive’’ but required
further investigation (Rosen and
Schwalbe 1997, p. 6).
Bullfrog Effects on the Native Anuran
Prey Base for the Northern Mexican
Gartersnake in the United States.
Bullfrog introductions in the United
States and Mexico have adversely
affected the native leopard frog prey
base for northern Mexican gartersnakes
(Conant 1974, pp. 471, 487–489; Hayes
and Jennings 1986, pp. 491–492; Rosen
and Schwalbe 1988, p. 28–30; 2002b,
pp. 232–238; Rosen et al. 1995, pp. 257–
258; 2001, pp. 2, Appendix I). Different
age classes of bullfrogs within a
community can affect native ranid
populations via different mechanisms.
Juvenile bullfrogs may affect native
ranids by competition, male bullfrogs
may affect native ranids by predation,
and female bullfrogs may affect native
ranids by 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 microhabitat use, but
also suggested that an individual ranid
frog species’ physical ability to escape
influences the effect of bullfrogs on each
native ranid community.
Kupferberg (1994, p. 95) found that
where bullfrogs were present in
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California, native anurans were rare or
absent. Effects of larval bullfrogs on
native ranid frogs have also been
described in the literature. Survivorship
of larval threatened California redlegged frogs (Rana aurora) was 700
percent greater in the absence of
bullfrog larvae (Lawler et al. 1999). Bury
and Whelan (1986, pp. 9–10) implicated
bullfrog introductions in the decline of
several native ranid frogs in several
States within the western United States
including Nevada, California, Montana,
Colorado, Oregon, and Washington.
Hayes and Jennings (1986, pp. 500–501)
conclude that while bullfrog
introductions have affected the status of
native ranid frogs throughout the
western United States, the synergistic
effect of other factors, such as habitat
alteration and destruction, introduced
nonnative fishes, commercial
exploitation, toxicants, pathogens and
parasites, and acid rain, likely also
played significant roles.
Bullfrog Predation on Northern
Mexican Gartersnakes in the United
States. Sub-adult and adult bullfrogs not
only compete with the northern
Mexican gartersnake for prey items, but
directly prey upon juvenile and
occasionally sub-adult northern
Mexican 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, taken by
John Carr of the Arizona Game and Fish
Department in 1964, provides
photographic documentation of bullfrog
predation (Rosen and Schwalbe 1988, p.
29; 1995, p. 452). 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 neonate (newborn)
and juvenile age size classes due to
bullfrogs preying on young small
snakes, which ultimately leads to low
recruitment levels (reproduction and
survival of young) (Rosen and Schwalbe
1988, p. 18; Holm and Lowe 1995, p.
34).
The tails of gartersnakes are easily
broken-off through predation attempts
(tails of gartersnakes do not regenerate),
which may assist in escaping an
individual predation attempt but may
also lead to infection or compromise an
individual’s physical ability to escape
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future predation attempts or
successfully forage. The incidence of
tail breaks in gartersnakes can often be
used to assess predation pressures
within gartersnake populations. Rosen
and Schwalbe (1988, p. 22) found the
incidence of tail breaks to be
statistically higher in females than in
males. Fitch (2003, p. 212) also found
that tail breaks in the common
gartersnake occurred more frequently in
females than males and in adults more
than in juveniles. Fitch (2003, p. 212)
also 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.
Furthermore, Mushinsky and Miller
(1993, pp. 662–664) found that the
incidence of tail injury in water snakes
in the genera Nerodia and Regina
(which have similar life histories to
northern Mexican gartersnakes) was
higher in females than in males and in
adults more than juveniles. We believe
this could be explained by higher
basking rates associated with gravid
(pregnant) females that increased their
visibility to predators and that predation
on juvenile snakes generally results in
complete consumption of the animal,
which would limit observations of tail
injury in the juvenile age class. Rosen
and Schwalbe (1988, p. 22) suggested
that the indication that female northern
Mexican gartersnakes bear more injuries
is consistent with the inference that
they employ a riskier foraging strategy.
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 postinjury hibernation may play an
important role in subsequent mortality.
Ecologically significant observations
on tail injuries were made by Rosen and
Schwalbe (1988, pp. 28–31) from the
once-extant population of northern
Mexican gartersnakes on the San
Bernardino National Wildlife Refuge
where 78 percent of specimens had
broken tails with a ‘‘soft and club-like’’
terminus, which suggests repeated
injury from multiple predation attempts.
While palpating (medically examining
by touch) gravid female northern
Mexican gartersnakes, Rosen and
Schwalbe (1988, p. 28) noted bleeding
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from this region which suggested the
snakes suffered from ‘‘squeeze-type’’
injuries inflicted by adult bullfrogs.
While a sub-adult or adult northern
Mexican gartersnake may survive an
individual predation attempt from a
bullfrog while only incurring tail
damage, secondary effects from
infection of the wound can significantly
contribute to mortality of individuals.
Research on the effects of attempted
predation performed by Mushinsky and
Miller (1993, pp. 661–664) and Willis et
al. (1982, pp. 100–101) supports the
observations made by Holm and Lowe
(1995, p. 34) on the northern Mexican
gartersnake population age class
structure in Scotia Canyon in the
Huachuca Mountains of southeastern
Arizona in the early 1990s. Specifically,
Holm and Lowe (1995, pp. 33–34)
observed a conspicuously greater
number of adult snakes, in that
population than sub-adult snakes as
well as a higher incidence of tail injury
(89 percent) in all snakes captured.
Bullfrogs have been identified as the
primary cause for both the collapse of
the native leopard frog (prey base for the
northern Mexican gartersnake) and
northern Mexican gartersnake
populations on the San Bernardino
National Wildlife Refuge (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). Rosen and Schwalbe
(1988, p. 18) stated that the low
survivorship of neonates, and possibly
yearlings, due to bullfrog predation is an
important proximate cause of
population declines of this snake at the
San Bernardino National Wildlife
Refuge and throughout its distribution
in Arizona.
Effects of Crayfish on Northern
Mexican Gartersnakes in the United
States. Crayfish represent another
category of nonnative species threat as
they are a primary threat to many prey
species of the northern Mexican
gartersnake and may also prey upon
juvenile gartersnakes (Fernandez and
Rosen 1996, p. 25; Voeltz 2002, pp. 87–
88). 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 trophic
structures (food chains) in riparian and
aquatic ecosystems through their effect
on vegetative structure, stream substrate
composition, and predation on eggs,
larval, and adult forms of native
invertebrate and vertebrate species.
Crayfish fed on embryos, tadpoles,
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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).
Fernandez and Rosen (1996, pp. 6–19,
52–56) and Rosen (1987, p. 5) discussed
observations of inverse relationships
between crayfish abundance and native
herpetofauna including narrow-headed
gartersnakes (Thamnophis
rufipunctatus rufipunctatus), 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 also prey
on fish eggs and larvae (Inman et al.
1998, p. 17).
Crayfish alter the abundance and
structure of aquatic vegetation by
grazing on aquatic and semiaquatic
vegetation, which reduces the cover
needed for 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) also found that
crayfish frequently burrow into stream
banks, which leads to increased bank
erosion, stream turbidity, and siltation
of substrates. Creed (1994, p. 2098)
found that filamentous alga (Cladophora
glomerata) was at least 10-fold greater in
aquatic habitat absent crayfish.
Filamentous alga is an important
component of aquatic vegetation that
provides cover for foraging gartersnakes
as well as microhabitat for prey species.
Inman et al. (1998, p. 3) documented
nonnative crayfish as widely distributed
and locally abundant in a broad array of
natural and artificial lotic (free-flowing)
and lentic (still water) habitats
throughout Arizona, many of which
overlapped the historical and extant
distribution of the northern Mexican
gartersnake. Hyatt (undated, p. 71)
concluded that the majority of waters in
Arizona contained at least one species
of crayfish. Holycross et al. (2006, p. 14)
found crayfish in 64 percent of the
sample sites in the Agua Fria watershed;
in 85 percent of the sites in the Verde
River watershed; in 46 percent of the
sites in the Salt River watershed; and in
67 percent of the sites in the Gila River
watershed. In total, crayfish were
recently observed at 35 (61 percent) of
the 57 sites surveyed across the
Mogollon Rim (Holycross et al. 2006, p.
14).
Several other authors have
specifically documented the presence of
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crayfish in many areas and drainages
throughout Arizona, which is testament
to their ubiquitous distribution in
Arizona and their strong colonizing
abilities. These areas included the
Kaibab National Forest (Sredl et al.
1995a, p. 7); the Coconino National
Forest (Sredl et al. 1995c, p. 7); the
Watson Woods Riparian Preserve near
Prescott (Nowak and Spille 2001, p. 33);
the Tonto National Forest (Sredl et al.
1995b, p. 9); the Lower Colorado River
(Ohmart et al. 1988, p. 150; Inman et al.
1998, Appendix B); the Huachuca
Mountains (Sredl et al. 2000, p. 10); the
Arivaca Area (Rosen et al. 2001,
Appendix I); Babocamari River drainage
(Rosen et al. 2001, Appendix I);
O’Donnell Creek drainage (Rosen et al.
2001, Appendix I); Santa Cruz River
drainage (Rosen and Schwalbe 1988,
Appendix I; Rosen et al. 2001,
Appendix I); San Pedro River drainage
(Inman et al. 1998, Appendix B; Rosen
et al. 2001, Appendix I); Aqua Fria River
drainage (Inman et al. 1998, Appendix
B; Holycross et al. 2006, pp. 14, 15–18,
52–54); Verde River drainage (Inman et
al. 1998, Appendix B; Holycross et al.
2006, pp. 14, 20–28, 54–56); Salt River
drainage (Inman et al. 1998, Appendix
B; Holycross et al. 2006, pp. 15, 29–44,
56–60); Black River drainage (Inman et
al. 1998, Appendix B); San Francisco
River drainage (Inman et al. 1998,
Appendix B; Holycross et al. 2006, pp.
14, 49–50, 61); Nutrioso Creek drainage
(Inman et al. 1998, Appendix B); Little
Colorado River drainage (Inman et al.
1998, Appendix B); Leonard Canyon
Drainage (Inman et al. 1998, Appendix
B); East Clear Creek drainage (Inman et
al. 1998, Appendix B); Chevelon Creek
drainage (Inman et al. 1998, Appendix
B); Eagle Creek drainage (Inman et al.
1998, Appendix B; Holycross et al.
2006, pp. 47–48, 60); Bill Williams
drainage (Inman et al. 1998, Appendix
B); Sabino Canyon drainage (Inman et
al. 1998, Appendix B); Dry Creek
drainage (Holycross et al. 2006, pp. 19,
53); Little Ash Creek drainage
(Holycross et al. 2006, pp. 19, 54);
Sycamore Creek drainage (Holycross et
al. 2006, pp. 25, 54–55); East Verde
River drainage (Holycross et al. 2006,
pp. 21–22, 54); Oak Creek drainage
(Holycross et al. 2006, pp. 23, 54); Pine
Creek drainage (Holycross et al. 2006,
pp. 24, 55); Spring Creek drainage
(Holycross et al. 2006, pp. 25, 55); Big
Bonito Creek drainage (Holycross et al.
2006, pp. 29, 56); Cherry Creek drainage
(Holycross et al. 2006, pp. 33, 57); East
Fork Black River drainage (Holycross et
al. 2006, pp. 34, 57); Haigler Creek
drainage (Holycross et al. 2006, pp. 35,
58); Houston Creek drainage (Holycross
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et al. 2006, pp. 35–36, 58); Rye Creek
drainage (Holycross et al. 2006, pp. 37,
58); Tonto Creek drainage (Holycross et
al. 2006, pp. 40–44, 59); Blue River
drainage (Holycross et al. 2006, pp. 45,
60); Campbell Blue River drainage
(Holycross et al. 2006, pp. 46, 60); and
the Gila River drainage (Inman et al.
1998, Appendix B; Holycross et al.
2006, pp. 45–50, 61).
Bullfrog and Crayfish Eradication in
the United States. As previously noted,
nonnative species such as bullfrogs and
crayfish have proven difficult, if not
impossible, to eradicate once
established in certain environments.
Bullfrogs, for example, are particularly
damaging to, and persistent in, riparian
communities. A population of adult
bullfrogs can sustain itself even when
the native vertebrate prey base has been
severely reduced or extirpated because
adult bullfrogs are cannibalistic and
larval bullfrogs can be sustained by
grazing on aquatic vegetation (Rosen
and Schwalbe 1995, p. 452). Effective
removal of semi-aquatic nonnative
species is possible in simple,
geographically isolated systems that can
be manipulated (e.g., stock tanks);
however, it can be expensive, and
specially designed fencing is likely
needed to prevent reinvasion until
entire landscapes (e.g., an entire valley)
have been cleared of nonnative species
(Rosen and Schwalbe 2002a, p. 7; Hyatt
undated). No single method is available
to effectively remove bullfrogs or
crayfish from lotic, or complex interconnected systems (Rosen and
Schwalbe 1996a, pp. 5–8; 2002a, p. 7;
Hyatt Undated, pp. 63–71). The inability
of land managers to effectively address
the invasion of nonnative species in
such communities highlights the serious
nature of nonnative species invasions.
Hyatt (undated, p. 71) concluded that
successful eradication of crayfish in
Arizona is highly unlikely. While
potential threats to physical habitat
from human land use activities can
usually be lessened or removed
completely with adjustments to land
management practices, the concern for
the apparent irreversibility of nonnative
species invasions becomes paramount
which leaves us to conclude that
nonnative species are the greatest threat
to the northern Mexican gartersnake due
to the long-term implications.
Nonnative Fish distribution and
Community Interactions in the United
States. 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
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documented the presence of nonnative
fish at many locations. Rosen et al.
(2001, Appendix I) found nonnative fish
in the following survey locations: the
Arivaca Area; Babocamari River
drainage; O’Donnell Creek drainage;
Audubon Research Ranch (Post Canyon)
near Elgin; Santa Cruz River drainage;
Agua Caliente Canyon; Santa Catalina
Mountains; and the San Pedro River
drainage. Holycross et al. (2006, pp. 14–
15, 52–61) found nonnative fish in the
Aqua Fria River drainage; the Verde
River drainage; the Dry Creek drainage;
the Little Ash Creek drainage; the
Sycamore Creek drainage; the East
Verde River drainage; the Oak Creek
drainage; the Pine Creek drainage; the
Big Bonito Creek drainage; the Black
River drainage; the Canyon Creek
drainage; the Cherry Creek drainage; the
Christopher Creek drainage; the East
Fork Black River drainage; the Haigler
Creek drainage; the Houston Creek
drainage; the Rye Creek drainage; the
Salt River drainage; the Spring Creek
drainage; the Tonto Creek drainage; the
Blue River drainage; the Campbell Blue
River drainage; the Eagle Creek
drainage; and the San Francisco River
drainage. Other authors have
documented the presence of nonnative
fish through their survey efforts in
specific regions that include the Tonto
National Forest (Sredl et al. 1995b, p. 8)
and the Huachuca Mountains (Sredl et
al. 2000, p. 10).
Holycross et al. (2006, pp. 14–15)
found nonnative fish species while
surveying for narrow-headed and
Mexican gartersnakes in 64 percent of
the sample sites in the Agua Fria
watershed, 85 percent of the sample
sites in the Verde River watershed, 75
percent of the sample sites in the Salt
River watershed, and 56 percent of the
sample sites in the Gila River
watershed. 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 detected
in only 8 of 57 sites surveyed (14
percent) (Holycross et al. 2006, p. 14).
While the locations and drainages
identified above that are known to
support populations of nonnative fish
do not provide a thorough
representation of the status of nonnative
fish distribution Statewide in Arizona, it
is well documented that nonnative fish
have infiltrated the majority of aquatic
communities in Arizona.
Rinne et al. (1998, p. 3) documented
over a dozen species of nonnative fish
that have been stocked within the
historical distribution of the northern
Mexican gartersnake in the Verde Basin
with over 850 stocking events occurring
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in Horseshoe and/or Bartlett reservoirs
and almost 4,500 in streams (mostly
tributaries to the Verde) over the past 60
years. Rinne et al. (1998, pp. 4–6) found
that in all but the uppermost reach,
nonnatives predominated the sampling
results in the Verde River. Voeltz (2002,
p. 88) documented an ‘‘alarming trend’’
in the Verde River with the reduction of
native fish abundance corresponding
with an explosion in red shiner
populations.
Nonnative fish can also affect native
amphibian populations. 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 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 prediction by Jennings
et al. (1992, p. 503) that native
amphibian declines will lead directly to
gartersnake declines. Matthews et al.
(2002, p. 20) noted that in addition to
nonnative fish species adversely
impacting amphibian populations that
are part of the gartersnake’s prey base,
direct predation on gartersnakes by
nonnative fish also occurs. Inversely,
gartersnake predation on nonnative
species, such as centrarchids, may
physically harm the snake. Choking
injuries to northern Mexican
gartersnakes may occur from attempting
to ingest nonnative spiny-rayed fish
species (such as green sunfish and bass)
because the spines located in the dorsal
fins of these species can become lodged,
or cut into the gut tissue of the snake,
as observed in narrow-headed
gartersnakes (Nowak and SantanaBendix 2002, p. 25).
Nonnative fish invasions can
indirectly affect the health,
maintenance, and reproduction of the
northern Mexican gartersnake by
altering its foraging strategy and
foraging success. Observations made by
Dr. Phil Rosen at Finley Tank on the
Audubon Research Ranch near Elgin,
Arizona, of northern Mexican
gartersnake populations and individual
growth trends prior to the arrival of the
nonnative bullfrog, provides
information on the effects of nonnative
fish invasions and the likely nutritional
ramifications of a fish-only diet in a
species that normally has a varied diet
largely supported by amphibian prey
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items (Rosen et al. 2001, p. 19). The
more energy expended in foraging,
coupled by the reduced number of small
to medium-sized fish available in lower
densities, may lead to deficiencies in
nutrition affecting growth and
reproduction because energy is instead
allocated to maintenance and the
increased energy costs of intense
foraging activity (Rosen et al. 2001, p.
19). In contrast, a northern Mexican
gartersnake diet that includes both fish
and amphibians such as leopard frogs
provides larger prey items which reduce
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 in
juvenile snakes that were deprived of
regular feedings versus the control
group that were fed regularly at natural
frequencies. Reduced foraging success
may therefore increase mortality rates in
the juvenile size class and consequently
affect recruitment of northern Mexican
gartersnakes where their prey base has
been compromised by nonnative
species.
Nonnative fish species also facilitate
the invasion of other aquatic nonnative
species such as bullfrogs. Adams et al.
(2003, pp. 343, 349) found that the
invasion of nonnative fish species
indirectly facilitates the invasion of
bullfrogs. Survivorship of tadpoles is
increased when nonnative fish prey
upon predatory macroinvertebrates,
which reduces the densities of
predatory macroinvertebrates and
relaxes their predation rate on bullfrog
tadpoles. These findings support the
‘‘invasional meltdown’’ hypothesis,
which suggests that when positive
interactions among nonnatives are
prevalent, that community of nonnative
species can increase the probability of
further invasions (Simberloff and Von
Holle 1999, p. 21; Adams et al. 2003, pp.
343, 348–350). While mutually
facilitative interactions among
introduced species have not been
thoroughly examined, it has been
concluded that nonnatives can and do
facilitate the expansion of other
nonnative species (Simberloff and Van
Holle 1999, p. 21).
Nonnative Species in Mexico. The
native fish prey base for northern
Mexican gartersnakes has been
dramatically affected by the
introduction of nonnative species in
several regions of Mexico (Conant 1974,
pp. 471, 487–489; Miller et al. 2005, pp.
60–61; Abarca 2006). In the lower
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elevations of Mexico where northern
Mexican gartersnakes occurred
historically and may still be extant,
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
become extinct due to human activities
(Contreras Balderas and Lozano 1994,
pp. 383–384). In 1979, The American
Fisheries Society listed 69 species of
native fish in Mexico as threatened or in
danger of becoming extinct. Ten years
later that number rose to 123 species, an
increase of 78 percent (Contreras
Balderas and Lozano 1994, pp. 383–
384). Miller et al. (2005, p. 60)
concludes that some 20 percent of
Mexico’s native fish are threatened or in
danger of becoming extinct. Nonnative
species are increasing everywhere
throughout Mexico and the outlook for
this trend looks ‘‘bleak’’ for native fish
according to Miller et al. (2005, p. 61).
A number of freshwater fish populations
have been adversely affected by
nonnative species in many documented
localities, several of which were
previously noted in the discussion
under Factor A.
Bullfrogs were purposefully
introduced nationwide in a concerted
effort to establish the species in all lakes
and canal systems throughout Mexico as
a potential food source for humans
although frog legs ultimately never
gained popularity in Mexican culinary
culture (Conant 1974, pp. 487–489).
Rosen and Melendez (2006, p. 54) report
bullfrog invasions to be prevalent in
northwestern Chihuahua and
northeastern Sonora where the northern
Mexican gartersnake is thought to occur.
In many areas, native leopard frogs were
completely displaced (extirpated) where
bullfrogs were observed. Rosen and
Melendez (2006, p. 54) also
demonstrated the relationship between
fish and amphibian communities in
Sonora and western Chihuahua in that
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 addition to
bullfrog invasions, the first record in
Mexico for the nonnative Rio Grande
leopard frog was recently documented
in northwestern Sonora, Mexico where
the northern Mexican gartersnake is
considered likely extirpated (Rorabaugh
and Servoss 2006, p. 102).
Unmack and Fagan (2004, p. 233)
compared historical museum collections
of nonnative fish species from the Gila
River basin in Arizona and the
geographically small Yaqui River basin
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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 distribution,
diversity, and abundance 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 and/or range
reductions of native fish species are
expected to occur in the Yaqui Basin of
Sonora, Mexico which may have extant
populations of northern Mexican
gartersnake, as did much of the Gila
Basin before the introduction of
nonnative species. The implications of
these declines in native fish to northern
Mexican gartersnakes indicate a
potentially serious threat to the
gartersnake’s persistence in these areas.
However, because specific and direct
survey information is significantly
limited concerning the presence and
potential effect of nonnative species on
the northern Mexican gartersnake in
Mexico, this discussion is based on
extrapolation of how we understand
these threats to affect the subspecies in
the United States. Furthermore, based
on the information available concerning
the threats in Mexico we can not
conclude that the subspecies is likely to
become endangered throughout its range
in Mexico. Although we acknowledge
that these threats are affecting the
subpecies in the United States, we have
determined that the portion of the
subspecies’ range in the United States
does not constitute a significant portion
of the range of the subspecies or a DPS.
Therefore, on the basis of the best
available information, we determine
that it is not likely that the northern
Mexican gartersnake will become an
endangered species within the
foreseeable future based on threats
under this factor.
D. The Inadequacy of Existing
Regulatory Mechanisms
Currently, the northern Mexican
gartersnake is considered ‘‘State
Endangered’’ in New Mexico. In the
State of New Mexico, an ‘‘Endangered
Species’’ is defined as ‘‘any species of
fish or wildlife whose prospects of
survival or recruitment within the state
are in jeopardy due to any of the
following factors: (1) The present or
threatened destruction, modification or
curtailment of its habitat; (2)
overutilization for scientific,
commercial or sporting purposes; (3) the
effect of disease or predation; (4) other
natural or man-made factors affecting its
prospects of survival or recruitment
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within the state; or (5) any combination
of the foregoing factors’’ as per New
Mexico Statutory Authority (NMSA) 17–
2–38.D. ‘‘Take’’, defined as ‘‘means to
harass, hunt, capture or kill any wildlife
or attempt to do so’’ by 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
northern Mexican gartersnakes, only
recommendations are afforded with
respect to actions that result in
destruction or modification of habitat
(NMSA 17–2–41.C and NMAC 19.33.6)
(Painter 2005).
Prior to 2005, the Arizona Game and
Fish Department allowed for take of up
to four northern Mexican gartersnakes
per person per year as specified in
Commission Order Number 43. The
Arizona Game and Fish Department
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 Arizona Game and Fish
Department has subsequently amended
Commission Order Number 43, which
closed the season on northern Mexican
gartersnakes, effective January 2005.
Take of northern Mexican gartersnakes
is no longer permitted in Arizona
without issuance of a scientific
collecting permit as per Arizona
Administrative Code R12–4–401 et seq.
While the Arizona Game and Fish
Department can seek criminal or civil
penalties for illegal take of northern
Mexican gartersnakes, only
recommendations are afforded with
respect to actions that result in
destruction or modification of northern
Mexican gartersnake habitat.
As previously mentioned, humans
encounter gartersnake species somewhat
regularly in riparian areas used for
recreational purposes or for other
reasons. This is partially due to
gartersnakes having an active foraging
strategy as well as diurnal behavior.
Many such encounters result in the
capture, injury, or death of the
gartersnake due to the lay person’s fear
or dislike of 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). It would be very difficult for the
Arizona Game and Fish Department or
the New Mexico Department of Fish and
Game to cite lay people (who are not
reptile hobbyists or amateur
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herpetologists in specific pursuit of
herpetofauna) for such forms of take.
Consequently, while the pursuit and
intentional collection of reptiles,
including the northern Mexican
gartersnake, is regulated by these
agencies, unregulated capture,
collection, or killing likely occurs
regularly.
We are reasonably certain that the
level of illegal field collecting by the
hobbyist community is low because
gartersnakes are relatively undesirable
in amateur herpetological collections.
However, there remains the possibility
that small, isolated, and/or low-density
populations could be negatively affected
by the collection of reproductive
females (Painter 2000, p. 39; Painter
2005; Holycross 2006).
The northern Mexican gartersnake is
considered a ‘‘Candidate Species’’ in the
Arizona Game and Fish Department
draft document, Wildlife of Special
Concern (WSCA) (AGFD In Prep., p. 12).
A ‘‘Candidate Species’’ is one ‘‘whose
threats are known or suspected but for
which substantial population declines
from historical levels have not been
documented (though they appear to
have occurred)’’ (AGFD In Prep., p. 12).
The purpose of the WSCA list is to
provide guidance in habitat
management implemented by landmanagement agencies.
Neither the New Mexico Department
of Game and Fish nor the Arizona Game
and Fish Department have specified or
mandated recovery goals for the
northern Mexican gartersnake, nor has
either State developed a conservation
agreement or plan for this species.
The U.S. Bureau of Land Management
considers the northern Mexican
gartersnake as a ‘‘Special Status
Species,’’ and agency biologists actively
attempt to identify gartersnakes
observed incidentally during fieldwork
for their records (Young 2005).
Otherwise, no specific protection or
land-management consideration is
afforded to the species on Bureau of
Land Management lands.
The presence of water is a primary
habitat constituent for the northern
Mexican gartersnake. Public concern
over the inadequacy of Arizona surface
water laws to ensure that flow is
maintained perennial streams was
discussed by Arizona Republic
columnist Shaun McKinnon (2006b).
McKinnon (2006b) highlighted the fact
that because the existing water laws are
so old, they reflect a legislative
interpretation of the resource that is not
consistent with what we know today;
yet the laws have never been updated or
amended to account for this
discrepancy. For example, over 100
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years ago when Arizona’s water laws
were written, the important connection
between groundwater and surface water
was not known (McKinnon 2006b).
Furthermore, meaningful changes to
these regulations that account for the
relative scarcity of surface water are
unlikely to come about because Arizona
is so ‘‘entrenched in tradition and in
property ownership’’ and because the
threat of litigation over proposed
changes precludes such efforts
(McKinnon 2006b). McKinnon (2006b)
specifically, mentions the Gila, Salt,
Verde, Santa Cruz, and San Pedro rivers
as having habitat attributes that have
directly suffered from inadequate
surface water regulations.
The U.S. Forest Service does not
include northern Mexican gartersnake
on their ‘‘Management Indicator Species
List,’’ but it is included on the
‘‘Regional Forester’s Sensitive Species
List.’’ This means that northern Mexican
gartersnakes are ‘‘considered’’ in land
management decisions. Individual U.S.
Forest Service biologists may
opportunistically gather data on the
gartersnakes observed incidentally in
the field for their records, although it is
not required.
Activities that could adversely affect
northern Mexican gartersnakes and their
habitat continue to occur throughout
their extant distribution on U.S. Forest
Service lands. Clary and Webster (1989,
p. 1) stated that ‘‘* * * most riparian
grazing results suggest that the specific
grazing system used is not of dominant
importance, but good management is—
with control of use in the riparian area
a key item.’’ Due to ongoing constraints
in funding, staff levels, and time, and
regulatory compliance pertaining to
monitoring and reporting duties tied to
land management, proactive measures
continue to be limited. These factors
affect a land manager’s ability to employ
adaptive management procedures when
effects to sensitive species or their
habitat could be occurring at levels
greater than accounted for in regulatory
compliance mechanisms, such as in
section 7 consultation under the Act for
other listed species that may co-occur
with the northern Mexican gartersnake
in an area.
The majority of extant populations of
northern Mexican gartersnake in the
United States occur on lands managed
by the U.S. Bureau of Land Management
and U.S. Forest Service. Although both
agencies have riparian protection goals,
neither agency has specific management
plans for the northern Mexican
gartersnake.
Riparian communities are complex
and recognized as unique in the
southwestern United States but are
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highly sensitive to many anthropogenic
land uses, as evidenced by the
comparatively high number of federally
listed riparian or aquatic species. Four
primary prey species for the northern
Mexican gartersnake, the Chiricahua
leopard frog, Gila topminnow, Gila
chub, and roundtail chub, are federally
listed or were petitioned for listing.
Other listed or proposed riparian
species or their proposed or designated
critical habitat overlap the current or
historical distribution of the northern
Mexican gartersnake. Despite secondary
protections that may be afforded to the
northern Mexican gartersnake from
federally listed species and/or their
critical habitat, riparian and aquatic
communities continue to be adversely
impacted for reasons previously
discussed, contributing to the declining
status of the northern Mexican
gartersnake throughout its range in the
United States.
Throughout Mexico, the Mexican
gartersnake is federally listed at the
species level of its taxonomy as
‘‘Amenazadas,’’ or Threatened, by the
Secretaria de Medio Ambiente y
Recursos Naturales (SEMARNAT)
(SEDESOL 2001). Threatened species
are ‘‘those species, or populations of the
same, likely to be in danger of
disappearing in a short or medium time
frame, if the factors that impact
negatively their viability, cause the
deterioration or modification of their
habitat or directly diminish directly the
size of their populations continue to
operate’’ (SEDESOL 2001 [NOM–059–
ECOL–2001], p. 4). This designation
prohibits taking of the species, unless
specifically permitted, as well as
prohibits any activity that intentionally
destroys or adversely modifies its
habitat [SEDESOL 2000 (LGVS) and
2001 (NOM–059–ECOL–2001)].
Additionally, in 1988, the Mexican
Government passed a regulation that is
similar to the National Environmental
Policy Act of the United States (42
U.S.C. 4321 et seq.). This Mexican
regulation requires an environmental
assessment of private or government
actions that may affect wildlife and/or
their habitat (SEDESOL 1988
[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,
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 recently developed the
Method of Evaluation of the Risk of
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Extinction of the Wild Species in
Mexico (MER) which unifies the criteria
of decision 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 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, the Mexican
gartersnake was placed on the NOM–
059 [SEDESOL 1994 (NOM–059–ECOL–
1994), p. 46] as a threatened species as
determined by a panel of scientific
experts. However, we are uncertain of
the specific information that was used
as the basis for the listing in Mexico and
were unable to obtain any information
that was used to validate the Federal
listing of the Mexican gartersnake in
Mexico.
Our review of the existing
governmental regulatory mechanisms
that pertain to the management of the
northern Mexican gartersnake or its
habitat in the United States leads us to
conclude that the protections afforded
by existing regulations may be
insufficient to adequately address the
declining status of the subspecies in the
United States. However, the Mexican
gartersnake (inclusive of the northern
Mexican gartersnake) is considered a
Federally-threatened species in Mexico.
Although we do not have sufficient
information to analyze the efficacy of
existing regulatory mechanisms in
Mexico, the best available data does not
support the conclusion that the species
is likely to become in danger of
extinction within the foreseeable future
due to the threats posed by the other
factors. Therefore, uncertainty with
respect to the efficacy of existing
regulatory mechanisms is not
dispositive as to the listing status of the
subspecies, and it is not a threatened
species on the basis of the lack of
existing regulatory mechanisms.
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E. Other Natural or Manmade Factors
Affecting Its Continued Existence in the
United States
Marcy’s checkered gartersnake
(Thamnophis marcianus marcianus)
may have ecological implications in the
decline and future conservation of the
northern Mexican gartersnake in
southern Arizona. Marcy’s checkered
gartersnake is a semi-terrestrial species
that is able to co-exist to some degree
with riparian and aquatic nonnative
predators. This is largely due to its
ability to forage in more terrestrial
habitats, specifically in the 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 bullfrogs, nonnative sportfish,
and crayfish also occur, which increases
not only the encounter rate between the
species but also the juvenile mortality
rate of the northern Mexican
gartersnake. Marcy’s checkered
gartersnake is a potential benefactor of
this scenario. As northern Mexican
gartersnake numbers decline within a
population, space becomes available for
occupation by checkered gartersnakes.
Marcy’s checkered gartersnake
subsequently maintains pressure on the
carrying capacity (the maximum
number of a given species that an area
can maintain based upon available
resources) for an area and could
potentially accelerate the decline of the
northern Mexican gartersnake (Rosen
and Schwalbe 1988, p. 31).
Rosen et al. (2001, pp. 9–10)
documented the occurrence of Marcy’s
checkered gartersnakes out-competing
and replacing northern Mexican
gartersnakes at the San Bernardino
National Refuge and surrounding
habitats of the Black Draw. They
suspected that the drought from the late
1980s through the late 1990s played a
role in the degree of competition for
aquatic resources, provided an
advantage to the more versatile Marcy’s
checkered gartersnake, and expedited
the decline of the northern Mexican
gartersnake. The ecological relationship
between these two species, in
combination with other factors
described above that have adversely
affected the northern Mexican
gartersnake prey base and the suitability
of occupied and formerly occupied
habitat, may be contributing to the
decline of this species.
We were unable to obtain any
information on other natural or
manmade factors affecting the
continued existence of the northern
Mexican gartersnake in Mexico.
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Finding
We have carefully examined the best
scientific and commercial information
available regarding the past, present,
and future threats faced by the northern
Mexican gartersnake. We reviewed the
petition, information available in our
files, other published and unpublished
information submitted to us during the
public comment period following our
90-day petition finding and consulted
with recognized northern Mexican
gartersnake experts and other Federal,
State, and Mexican resource agencies.
Because specific and direct survey
information is significantly limited
concerning the presence and potential
effect of the threats discussed in this
finding to the subspecies in Mexico,
much of our discussion is based on
extrapolation of how we understand
these threats to affect the subspecies in
the United States. Furthermore, based
on the information available concerning
the threats in Mexico we can not
conclude that the subspecies is likely to
become endangered throughout its range
in Mexico. Although we acknowledge
that several threats are affecting the
subpecies in the United States, we have
determined that the portion of the
subspecies’ range in the United States
does not constitute a significant portion
of the range of the subspecies or a DPS.
On the basis of the best scientific and
commercial information available, we
determine that it is not likely that the
northern Mexican gartersnake is likely
to become an endangered species within
the foreseeable future and that listing of
the northern Mexican gartersnake
throughout its range in the United States
and Mexico based on its rangewide
status is not warranted.
In making this finding, we
respectfully acknowledge that the
Mexican government has found
Thamnophis eques to be in danger of
disappearance in the short-or mediumterm future in their country from the
destruction and modification of its
habitat and/or from the effects of
shrinking population sizes and has
therefore listed the species as
Threatened, under the listing authority
of SEMARNAT (SEDESOL 2001).
However, as discussed at length in
Factor D above, we also note that the
level of information required to list a
species in Mexico may not be as
rigorous as that required to list a species
in the United States under the
Endangered Species Act. Our
conclusion that listing is not warranted
under the Act is based on: (1) The
apparent differences in listing protocols;
(2) the significantly limited amount of
information available on the status of
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and threats to the northern Mexican
gartersnake in Mexico in comparison to
our knowledge of the same in the
United States; and most importantly (3)
the relatively large percentage (70 to 80
percent) of the subspecies’ historic
distribution in Mexico for which we
have little to no information about with
respect to status and threats.
In making this Finding, we also
recognize there have been declines in
the distribution and abundance of the
northern Mexican gartersnake within its
distribution in the United States which
are primarily attributed to individual
and community interactions with
nonnative species that occur in every
locality where northern Mexican
gartersnakes have been documented in
the United States. As discussed in
Factor C above, the documented
mechanisms for which nonnative
interactions occur include: (1) Direct
predation on northern Mexican
gartersnakes by nonnative species; and
(2) the effects of a diminished prey base
via nonnative species preying upon and
competing with native prey species
(Meffe 1985, pp. 179–185; Rosen and
Schwalbe 1988, pp. 28–31; 1995, p. 452;
2002b, pp. 223–227; Bestgen and Propst
1989, pp. 409–410; Clarkson and
Rorabaugh 1989, pp. 531, 535; Marsh
and Minckley 1990, p. 265; Stefferud
and Stefferud 1994, p. 364; Rosen et al.
1995, pp. 257–258; 1996, pp. 2, 11–12;
2001, pp. 2, 21–22; Degenhardt et al.
1996, p. 319; Fernandez and Rosen
1996, pp. 21–33; Weedman and Young
1997, pp. 1, Appendices B, C; Inman et
al. 1998, p. 17; Rinne et al. 1998, pp. 4–
6; Fagan et al. 2005, pp. 38–39; Olden
and Poff 2005, pp. 82–87; Holycross et
al.2006, pp. 12–15; Brennan and
Holycross 2006, p. 123). However, we
again note that the portion of the
historic distribution of the northern
Mexican gartersnake in the United
States represents approximately 20 to 30
percent of its rangewide distribution.
Furthermore, we were unable to obtain
substantial information regarding the
status of the northern Mexican
gartersnake in Mexico (representing
approximately 70 to 80 percent of its
rangewide distribution).
Throughout the range of the northern
Mexican gartersnake, but most
accurately within its distribution in the
United States, literature documents the
cause and effect relationship of
disturbances to the trophic structure
(food chain) of native riparian and
aquatic communities. The substantial
decline of primary native prey species,
such as leopard frogs and native fish,
has contributed significantly to the
decline of a primary predator, the
northern Mexican gartersnake. In this
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respect, the northern Mexican
gartersnake is considered an indicator
species, or a species that can be used to
gauge the condition of a particular
habitat, community, or ecosystem. The
synergistic effect of nonnative species
both reducing the prey base of, and
directly preying upon, northern
Mexican gartersnakes has placed
significant pressure upon the viability
and sustainability of extant northern
Mexican gartersnake populations and
has led to significant fragmentation and
risks to the continued viability of extant
populations. The evolutionary biology
of the northern Mexican gartersnake,
much like that of native fish and
leopard frogs, has left the species
without adaptation to and defenseless
against the effect of nonnative species
invasions.
We further recognize that in addition
to the deleterious effects of nonnative
species invasions, the decline of the
northern Mexican gartersnake has been
exacerbated by historical and ongoing
threats to its habitat in the United
States. The threats identified and
discussed above in detail in Factor A,
‘‘The Present or Threatened Destruction,
Modification, or Curtailment of its
Habitat or Range,’’ effectively
summarize our knowledge of the current
and future status of its riparian and
aquatic habitat in the United States.
Chiefly, these threats include: (1) The
modification and loss of ecologically
valuable cienegas (Hendrickson and
Minckley 1984, p. 161; Stromberg et al.
1996, p. 113); (2) urban and rural
development (Medina 1990, p. 351;
Girmendock and Young 1997, pp. 45–
47; Voeltz 2002, p. 88; Wheeler et al.
2005, pp. 153–154); (3) road
construction, use, and maintenance
(Rosen and Lowe 1994, pp. 143, 146–
148; Waters 1995, p. 42; Carr and Fahrig
2001, pp. 1074–1076; Hels and
Buchwald 2001, p. 331; Smith and Dodd
2003, pp. 134–138; Angermeier et al.
2004, p. 19; Shine et al. 2004, pp. 9, 17–
19; Andrews and Gibbons 2005, p. 772;
Wheeler et al. 2005, pp. 145, 148–149;
Roe et al. 2006, pp. 163–166); (4) human
population growth (Girmendock and
Young 1993, p. 47; American Rivers
2006; Arizona Republic, March 16,
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2006); (5) groundwater pumping,
surface water diversions, and drought
(Abarca and Weedman 1993, p. 2;
Girmendock and Young 1993, pp. 45–
52; Sullivan and Richardson 1993, pp.
35–42; Stromberg et al. 1996, pp. 124–
127; Boulton et al. 1998, pp. 60–62;
Rinne et al. 1998, pp. 7–11; Voeltz 2002,
p. 88; Philips and Thomas 2005; Webb
and Leake 2005, pp. 307–308; American
Rivers 2006; Boulton and Hancock 2006,
p. 139); (6) improper livestock grazing
(Sartz and Tolsted 1974, p. 354;
Kauffman and Krueger 1984, pp. 433–
434; Szaro et al. 1985, pp. 361–363;
Weltz and Wood 1986, p. 367–368;
Clary and Webster 1989, pp. 1–3; Clary
and Medin 1990, pp. 1–6; Orodho et al.
1990, p. 9; Fleischner 1994; pp. 631–
632; Trimble and Mendel 1995, p. 233;
Waters 1995, pp. 22–24; Girmendock
and Young 1997, p. 47; Pearce et al.
1998, p. 302; Belsky et al. 1999, p. 1;
Voeltz 2002, p. 88; Krueper et al. 2003,
pp. 607, 613–614); (7) catastrophic
wildfire and wildfire in non-fire
adapted communities (Rinne and Neary
1996, p. 135; Esque and Schwalbe 2002,
pp. 165, 190); and (8) undocumented
immigration and international border
enforcement and management activities
(Segee and Neeley 2006, pp. 5–7;
USFWS 2006, pp. 91–105).
In our discussion under Factors A
through E above, we have provided a
comprehensive, in-depth analysis of all
known threats that have or continue to
affect the status of the northern Mexican
gartersnake in the United States,
including those which have not yet been
documented but where potential effects
exist. As a result of our assessment, we
note that certain land use activities such
as road construction and use, direct
mortality from livestock grazing,
undocumented immigration and
international border enforcement and
management activities, and some types
of development, pose a more significant
risk to highly fragmented, low density
populations of northern Mexican
gartersnakes. As noted on several
occasions above, in these types of
situations where the viability of a
known northern Mexican gartersnake
population is clearly at risk, the loss of
a single reproductive female due to
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these threats is of concern. However,
these types of threats are less significant
to the northern Mexican gartersnake
when the status of these at-risk
populations improves through the
implementation of conservation
activities. We also remain optimistic
that our local, State, and Federal
partners in wildlife conservation will be
proactive in monitoring populations and
implementing conservation measures to
ensure that apparent declines of the
northern Mexican gartersnake in the
United States are reversed and that this
species remains a member of our native
riparian and aquatic communities. But
we do not rely upon any future
conservation actions in making this
finding.
Notwithstanding our extensive
discussion of the past and ongoing
threats affecting this species, and the
evidence of range contraction within the
United States, neither the existence of
the threats nor past range contraction
means that a species meets the
definition of a threatened or endangered
species under the Act. Based on our
evaluation of the best available data, we
conclude that the northern Mexican
gartersnake is not likely to become an
endangered species in all or a
significant portion of its range in the
foreseeable future.
References Cited
A complete list of all references cited
in this document is available upon
request from the Field Supervisor at the
Arizona Ecological Services Office (see
ADDRESSES section).
Author
The primary author of this document
is the Arizona Ecological Services Office
(see ADDRESSES section).
Authority: The authority for this action is
the Endangered Species Act of 1973, as
amended (16 U.S.C. 1531 et seq.).
Dated: September 14, 2006.
H. Dale Hall,
Director, Fish and Wildlife Service.
[FR Doc. 06–7784 Filed 9–25–06; 8:45 am]
BILLING CODE 4310–55–P
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[Federal Register Volume 71, Number 186 (Tuesday, September 26, 2006)]
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[Pages 56228-56256]
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[FR Doc No: 06-7784]
[[Page 56227]]
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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; 12-Month Finding on a
Petition To List the Northern Mexican Gartersnake (Thamnophis eques
megalops) as Threatened or Endangered With Critical Habitat; Proposed
Rule
Federal Register / Vol. 71, No. 186 / Tuesday, September 26, 2006 /
Proposed Rules
[[Page 56228]]
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DEPARTMENT OF THE INTERIOR
Fish and Wildlife Service
50 CFR Part 17
Endangered and Threatened Wildlife and Plants; 12-Month Finding
on a Petition To List the Northern Mexican Gartersnake (Thamnophis
eques megalops) as Threatened or Endangered With Critical Habitat
AGENCY: Fish and Wildlife Service, Interior.
ACTION: Notice of 12-month petition finding.
-----------------------------------------------------------------------
SUMMARY: We, the U.S. Fish and Wildlife Service (Service), announce a
12-month finding on a petition to list the northern Mexican gartersnake
(Thamnophis eques megalops) as threatened or endangered with critical
habitat under the Endangered Species Act of 1973, as amended (Act). The
petitioners provided three listing scenarios for consideration by the
Service: (1) Listing the United States population as a Distinct
Population Segment (DPS); (2) listing Thamnophis eques megalops
throughout its range in the United States and Mexico based on its
rangewide status; or (3) listing Thamnophis eques megalops throughout
its range in the United States and Mexico based on its status in the
United States. After thorough analysis and review of all available
scientific and commercial information, we find that listing of the
subspecies, under any of the three scenarios, is not warranted. Of the
three listing scenarios specified above, we found scenario two provided
the most rigorous evaluation of the status of the northern Mexican
gartersnake and herein provide detailed discussion of our conclusions
in that context. We also provide additional discussion of our
evaluation of scenarios (1) listing the United States population as a
DPS and (3) listing Thamnophis eques megalops throughout its range in
the United States and Mexico based on its status in the United States.
DATES: The finding announced in this document was made on September 26,
2006.
ADDRESSES: The complete supporting file for this finding is available
for inspection, by appointment, during normal business hours at the
Arizona Ecological Services Office, 2321 West Royal Palm Road, Suite
103, Phoenix, AZ 85021-4951. Please submit any new information,
materials, comments, or questions concerning this species or this
finding to the above address.
FOR FURTHER INFORMATION CONTACT: Steve Spangle, Field Supervisor,
Arizona Ecological Services Office (see ADDRESSES) 602-242-0210.
SUPPLEMENTARY INFORMATION:
Background
Section 4(b)(3)(B) of the Act (16 U.S.C. 1531 et seq.), requires
that, for any petition to revise the Lists of Threatened and Endangered
Wildlife and Plants that contains substantial scientific and commercial
information that listing may be warranted, we make a finding within 12
months of the date of receipt of the petition on whether the petitioned
action is (a) not warranted, (b) warranted, or (c) warranted, but that
the immediate proposal of a regulation implementing the petitioned
action is precluded by other pending proposals to determine whether any
species is threatened or endangered, and expeditious progress is being
made to add or remove qualified species from the Lists of Endangered
and Threatened Wildlife and Plants. Section 4(b)(3)(C) of the Act
requires that a petition for which the requested action is found to be
warranted but precluded be treated as though resubmitted on the date of
such finding, i.e., requiring a subsequent finding to be made within 12
months. Each subsequent 12-month finding will be published in the
Federal Register.
On December 19, 2003, we received a petition dated December 15,
2003, requesting that we list the northern Mexican gartersnake as
threatened or endangered, and that we designate critical habitat
concurrently with the listing. The petition, submitted by the Center
for Biological Diversity, was clearly identified as a petition for a
listing rule and contained the names, signatures, and addresses of the
requesting parties. Included in the petition was supporting information
regarding the species' taxonomy and ecology, historical and current
distribution, present status, and actual and potential causes of
decline. We acknowledged the receipt of the petition in a letter to Mr.
Noah Greenwald, dated March 1, 2004. In that letter, we also advised
the petitioners that, due to funding constraints in fiscal year (FY)
2004, we would not be able to begin processing the petition at that
time.
On May 17, 2005, the petitioners filed a complaint for declaratory
and injunctive relief, challenging our failure to issue a 90-day
finding in response to the petition as required by 16 U.S.C.
1533(b)(3)(A) and (B). In a stipulated settlement agreement, we agreed
to submit a 90-day finding to the Federal Register by December 16,
2005, and if positive, submit a 12-month finding to the Federal
Register by September 15, 2006 [Center for Biological Diversity v.
Norton, CV-05-341-TUC-CKJ (D. Az)]. The settlement agreement was signed
and adopted by the District Court of Arizona on August 2, 2005.
On December 13, 2005, we made our 90-day finding that the petition
presented substantial scientific information indicating that listing
the northern Mexican gartersnake (Thamnophis eques megalops) may be
warranted, but we did not discuss the applicability of any of the three
listing scenarios that were provided in the petition. The finding and
our initiation of a status review was published in the Federal Register
on January 4, 2006 (71 FR 315). We are required, under the court-
approved stipulated settlement agreement, to submit to the Federal
Register our 12-month finding pursuant to the Act [16 U.S.C.
1533(b)(3)(B)] on or before September 15, 2006. This notice constitutes
our 12-month finding for the petition to list the northern Mexican
gartersnake as threatened or endangered.
Previous Federal Actions
The Mexican gartersnake (Thamnophis eques) (which included the
subspecies) was placed on the list of candidate species as a Category 2
species in 1985 (50 FR 37958). Category 2 species were those for which
existing information indicated that listing was possibly appropriate,
but for which substantial supporting biological data to prepare a
proposed rule were lacking. In the 1996 Candidate Notice of Review
(February 28, 1996; 61 FR 7596), the use of Category 2 candidates was
discontinued, and the northern Mexican gartersnake was no longer
recognized as a candidate. In addition, on January 4, 2006, we
published a 90-day finding on a petition to list the northern Mexican
gartersnake (71 FR 315), as discussed above.
Biology
Species Description. The northern Mexican gartersnake may occur
with other native gartersnake species and can be difficult for people
without herpetological expertise to identify. With a maximum known
length of 44 inches (in) (112 centimeters (cm)), it ranges in
background color from olive to olive-brown to olive-gray with three
stripes that run the length of the body. The middle dorsal stripe is
yellow and darkens toward the tail. The pale yellow to light-tan
lateral stripes distinguish the Mexican gartersnake from other
sympatric (co-occurring) gartersnake species because a portion of the
lateral
[[Page 56229]]
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 and the olive-gray ventrolateral fields. A
conspicuous, light-colored crescent extends behind the corners of the
mouth. The two dark brown to black blotches that occur behind the head
of several gartersnake species may be diffuse or absent in the Mexican
gartersnake. The coloration of the venter is bluish-gray or greenish-
grey. The dorsolateral scalation is keeled, the anal plate is single,
and there are eight or nine upper labial scales (Rosen and Schwalbe
1988, p. 4; Rossman et al. 1996, pp. 171-172).
Taxonomy. The northern Mexican 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), but also
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 that have been described in the
gartersnake genus Thamnophis (Rossman et al. 1996, p. xvii-xviii). De
Queiroz et al. (2002, p. 323) identified two large overlapping clades
(related taxonomic groups) of gartersnakes that they called the
``Mexican'' and ``widespread'' clades which were supported by allozyme
and mitochondrial DNA genetic analyses. Thamnophis eques is a member of
the ``widespread'' clade and is most closely related taxonomically to,
although genetically and phenotypically distinct from, the checkered
gartersnake (Thamnophis marcianus) (De Queiroz and Lawson 1994, p.
217).
Rossman et al. (1996, p. 175) noted that the current specific name
eques was not applied at the time of the original description of the
holotype because the specimen was mistakenly identified as a black-
necked gartersnake (Thamnophis cyrtopsis). In recent history and 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). T. eques displays considerable phenotypic variability
(variation in its physical appearance) across its distribution, and all
subspecific descriptions under T. eques have been based on
morphometrics or morphological characters. The subspecies T. e. eques
and T. e. megalops are distinguished by average differences in sub-
caudal scale counts, while T. e. virgatenuis is distinguished from T.
e. megalops based on having a darker background color and a narrower
vertebral stripe (Rossman et al. 1996, p. 175). Rossman et al. (1996,
p. 175) also noted that the discontinuous distributions of high-
elevation and low-elevation T. e. virgatenuis and T. e. megalops,
respectively, are ``zoogeographically peculiar and unique among
gartersnakes.''
Rossman et al. (1996, p. 172) describe the distribution of T. e.
eques as occurring from southern Nayarit eastward along the Transverse
Volcanic Axis to west-central Veracruz, and identified an additional
disjunct population in central Oaxaca. T. e. virgatenuis is distributed
in three isolated, high-elevation populations in southwestern Durango
and in west-central and northwestern Chihuahua (Rossman et al. 1996, p.
172).
In 2003, an additional seven new subspecies were identified under
T. eques: (1) T. e. cuitzeoensis; (2) T. e. patzcuaroensis; (3) T. e.
inspiratus; (4) T. e. obscurus; (5) T. e. diluvialis; (6) T. e.
carmenensis; and (7) T. e. scotti (Conant 2003, p. 3). These seven new
subspecies were described based on morphological differences in
coloration and pattern; have high endemism (degree of restriction to a
particular area) with 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). We are not aware of any challenges
within the scientific literature of the validity of current taxonomy of
any of the 10 subspecies of T. eques.
The most widely distributed of the 10 subspecies under Thamnophis
eques is the northern Mexican gartersnake (Thamnophis eques megalops),
which is the only subspecies that occurs in the United States and the
entity we address in this finding. In Mexico, T. e. megalops
historically occurred throughout the Sierra Madre Occidental south to
Guanajuato, and east across the Mexican Plateau to Hidalgo, which
comprised approximately 85 percent of the total rangewide distribution
of the species (Rossman et al. 1996, p. 173). Robert Kennicott first
described the northern Mexican gartersnake in 1860, as Eutenia megalops
from the type locality of Tucson, Arizona (Rosen and Schwalbe 1988, p.
2). In 1951, Dr. Hobart Smith renamed the subspecies with its current
scientific name (Rosen and Schwalbe 1988, p. 3). A summary of this
species' lengthy taxonomic history can be found in Rosen and Schwalbe
(1988, pp. 2-3). Several common names have been applied to the northern
Mexican gartersnake in the United States over the years, such as the
Arizona ribbon snake, the Emory's gartersnake, and the Arizona
gartersnake (Rosen and Schwalbe 1988, p. 2).
In summary, while the taxonomic history of Thamnophis eques is
robust, we found no indication in the significant body of taxonomic
literature we reviewed that its current taxonomy is in doubt or in any
way invalid (Rosen and Schwalbe 1988, pp. 2-3; De Queiroz and Lawson
1994, pp. 215-217; Liner 1994, p. 107; Rossman et al. 1996, pp. 171,
175; Conant 2003, p. 6; Crother et al. 2000, p. 72; 2003, p. 202; De
Queiroz et al. 2002, p. 327).
Habitat. 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). The northern
Mexican gartersnake is considered a riparian obligate (restricted to
riparian areas when not engaged in dispersal behavior) and occurs
chiefly in the following general habitat types: (1) Source-area
wetlands [e.g., cienegas (mid-elevation wetlands with highly organic,
reducing (basic, or alkaline) soils), stock tanks (small earthen
impoundment), etc.]; (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; Arizona Game and Fish Department
2001). Vegetation characteristics vary based on the type of habitat.
For example, in source-area wetlands, dense vegetation consists of knot
grass (Paspalum distichum), spikerush (Eleocharis), bulrush (Scirpus),
cattail (Typha), deergrass (Muhlenbergia), sacaton (Sporobolus),
Fremont cottonwood (Populus fremontii), Goodding's willow (Salix
gooddingii), and velvet mesquite (Prosopis velutina) (Rosen and
Schwalbe 1988, pp. 14-16).
In riparian woodlands consisting of cottonwood and willow or
gallery forests of broadleaf and deciduous species along larger rivers,
the northern Mexican gartersnake may be observed in mixed grasses along
the bank or in the shallows (Rossman et al. 1996, p. 176; Rosen and
Schwalbe 1988, p. 16). Within and adjacent to the Sierra Madre
Occidental in Mexico, it occurs in montane woodland, Chihuahuan
desertscrub, mesquite-grassland, and Cordillera Volc[aacute]nica
montane woodland (McCranie and Wilson 1987, pp. 14-17).
[[Page 56230]]
In small streamside riparian habitat, this snake is often
associated with Arizona sycamore (Platanus wrightii), sugar leaf maple
(Acer grandidentatum), velvet ash (Fraxinus velutina), Arizona cypress
(Cupressus arizonica), Arizona walnut (Juglans major), Arizona alder
(Alnus oblongifolia), alligator juniper (Juniperus deppeana), Rocky
Mountain juniper (J. scopulorum), and a number of oak species (Quercus
spp.) (McCranie and Wilson 1987, pp. 11-12; Cirett-Galan 1996, p. 156).
Behavior, Prey Base, and Reproduction. The northern Mexican
gartersnake is surface active at ambient 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. The northern
Mexican gartersnake is an active predator and is believed to heavily
depend upon a native prey base (Rosen and Schwalbe 1988, pp. 18, 20).
Generally, its diet consists predominantly of amphibians and fishes,
such as adult and larval native leopard frogs [e.g., lowland leopard
frog (Rana yavapaiensis) and Chiricahua leopard frog (Rana
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 Schwalbe 1988, p. 18).
Auxiliary prey items may also include young Woodhouse's toads (Bufo
woodhousei), treefrogs (Family Hylidae), earthworms, deermice
(Peromyscus maniculatus), 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). To a much lesser extent, this snake's diet may include nonnative
species, including juvenile fish, larval and juvenile bullfrogs, and
mosquitofish (Gambusia affinis) (Holycross et al. 2006, p. 23).
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
ovoviviparous (eggs develop and hatch within the oviduct of the
female). Mating occurs in April and May in their northern distribution
followed by the live birth of between 7 and 26 neonates (newly born
individuals) (average is 13.6) in July and August (Rosen and Schwalbe
1988, p. 16). Approximately half of the sexually mature females within
a population reproduce in any one season (Rosen and Schwalbe 1988, p.
17).
Distribution
Historical Distribution. The United States comprises the northern
portion of the northern Mexican gartersnake's distribution. Within the
United States, the northern Mexican gartersnake historically occurred
predominantly in Arizona with a limited distribution in New Mexico that
consisted of scattered locations throughout the Gila and San Francisco
headwater drainages in western Hidalgo and Grant counties (Price 1980,
p. 39; Fitzgerald 1986, Table 2; Degenhardt et al. 1996, p. 317;
Holycross et al. 2006, pp. 1-2). Fitzgerald (1986, Table 2) provided
museum records for the following historical localities for northern
Mexican gartersnakes in New Mexico: (1) Mule Creek; (2) the Gila River,
5 miles (mi) ( 8 kilometers (km)) east of Virden; (3) Spring Canyon;
(4) the West Fork Gila River at Cliff Dwellings National Monument; (5)
the Tularosa River at its confluence with the San Francisco River; (6)
the San Francisco River at Tub Spring Canyon; (7) Little Creek at
Highway 15; (8) the Middle Box of Gila River at Ira Ridge; (9) Turkey
Creek; (10) Negrito Creek; and (11) the Rio Mimbres.
Within Arizona, the historical distribution of the northern Mexican
gartersnake ranged from 130 to 6,150 ft (40 to 1,875 m) in elevation
and spread variably based on the relative permanency of water and the
presence of suitable habitat. In Arizona, the northern Mexican
gartersnake historically occurred within several perennial or
intermittent drainages and disassociated wetlands that included: (1)
The Gila River; (2) the Lower Colorado River from Davis Dam to the
International Border; (3) the San Pedro River; (4) the Santa Cruz River
downstream from the International Border; (5) the Santa Cruz River
headwaters/San Rafael Valley and adjacent montane canyons; (6) the Salt
River; (7) the Rio San Bernardino from International Border to
headwaters at Astin Spring (San Bernardino National Wildlife Refuge);
(8) Agua Fria River; (9) the Verde River; (10) Tanque Verde Creek in
Tucson; (11) Rillito Creek in Tucson; (12) Agua Caliente Spring in
Tucson; (13) the downstream portion of the Black River from the Paddy
Creek confluence; (14) the downstream portion of the White River from
the confluence of the East and North forks; (15) Tonto Creek from the
mouth of Houston Creek downstream to Roosevelt Lake; (16) Cienega Creek
from the headwaters to the ``Narrows'' just downstream of Apache
Canyon; (17) Pantano Wash (Cienega Creek) from Pantano downstream to
Vail; (18) Potrero Canyon/Springs; (19) Audubon Research Ranch and
vicinity near Elgin; (20) Upper Scotia Canyon in the Huachuca
Mountains; (21) Arivaca Creek; (22) Arivaca Cienega; (23) Sonoita
Creek; (24) Babocomari River; (25) Babocamari Cienega; (26) Barchas
Ranch, Huachuca Mountain bajada; (27) Parker Canyon Lake and
tributaries in the Canelo Hills; (28) Big Bonito Creek; (29) Lake
O'Woods, Lakeside area; (30) Oak Creek from Midgley Bridge downstream
to the confluence with the Verde River; and (31) Spring Creek above the
confluence with Oak Creek (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; Rosen 2006; Holycross 2006).
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 (De Queiroz and Smith 1996, p. 155); however, any
populations of northern Mexican gartersnakes that may have historically
occurred in Nevada pertained directly to the Colorado River and are
likely extirpated.
Within Mexico, northern Mexican gartersnakes historically occurred
within the Sierra Madre Occidental and the Mexican Plateau in the
Mexican states of Sonora, Chihuahua, Durango, Coahila, Zacatecas,
Guanajuato, Nayarit, Hidalgo, Jalisco, San Luis Potos[iacute],
Aguascalientes, Tlaxacala, Puebla, M[eacute]xico, Veracruz, and
Quer[eacute]taro, which comprises approximately 70 to 80 percent of its
historical rangewide distribution (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).
Status in the United States. Holycross et al. (2006, p. 12)
included the northern Mexican gartersnake as a target species at 33
sites surveyed within drainages along the Mogollon Rim. A total of 874
person-search hours and 63,495 trap-hours were devoted to that effort,
which resulted in the capture of 23 snakes total in 3 (9 percent) of
the sites visited. This equates to approximately 0.03 snakes observed
per person-search hour and 0.0004 snakes captured per trap-hour over
the entire effort. For comparison, a population of northern Mexican
gartersnakes at Page Springs, Arizona,
[[Page 56231]]
that we consider stable yielded 0.22 snakes observed per person-search
hour and 0.004 snakes captured per trap-hour (an order of magnitude
higher) (Holycross et al. 2006, p. 23). Survey sites were selected
based on the existence of historical records for the species or sites
where the species may occur based on habitat suitability within the
historical distribution of the species. Holycross et al. (2006, p. 12)
calculated the capture rates for the northern Mexican gartersnake as
12,761 trap-hours per snake and 49 person-search hours per snake.
Northern Mexican gartersnakes were found at 2 of 11 (18 percent)
historical sites and 1 of 22 (4 percent) sites where the species was
previously unrecorded (Holycross et al. 2006, p. 12). When compared
with extensive survey data in Rosen and Schwalbe (1988, Appendix I),
these data demonstrate dramatic declines in both capture rates and the
total number of populations of the species in areas where multiple
surveys have been completed over time. However, these data may be
affected by differences in survey efforts and drought.
In 2000, Rosen et al. (2001, Appendix I) resurveyed many sites in
southeastern Arizona that were historically known to support northern
Mexican gartersnake populations during the early to mid-1980s, and also
provided additional survey data collected from 1993-2001. Rosen et al.
(2001, pp. 21-22) reported their results in terms of increasing,
stabilized, or decreasing populations of northern Mexican gartersnakes.
Three sites (San Bernardino National Wildlife Refuge, Finley Tank
at the Audubon Research Ranch near Elgin, and Scotia Canyon in the
Huachuca Mountains) were intensively surveyed and yielded mixed
results. The northern Mexican gartersnake population on the San
Bernardino National Wildlife Refuge experienced ``major, demonstrable
declines'' to near or at extirpation over the span of a decade. That
population is now considered extirpated (Radke 2006). The status of the
population at Finley Tank is uncertain. Scotia Canyon was the last area
intensively resurveyed by Rosen et al. (2001, pp. 15-16). In comparing
this information with survey data from Holm and Lowe (1995, pp. 27-35),
northern Mexican gartersnake populations in this area suggest a
possible decline from the early 1980s, as evidenced by low capture
rates in 1993 and even lower capture rates in 2000.
The remaining 13 sites in southeastern Arizona resurveyed by Rosen
et al. (2001, pp. 21-22) also yielded mixed results. Population trend
information is difficult to ascertain given the variability of survey
sample design and effort used by Rosen et al. (2001). However, the
survey results suggested population increases at one site (lower
Cienega Creek), possible stability at two sites (lower San Rafael
Valley, Arivaca), and negative trends at many other sites [Empire-
Cienega Creek, Babocomari, Bog Hole, O'Donnell Creek, Turkey Creek
(Canelo), Post Canyon, Lewis Springs (San Pedro River), San Pedro River
near Highway 90, Barchas Ranch Pond (Huachuca Mountain bajada), Heron
Spring, Sharp Spring, and Elgin-Sonoita windmill well site (San Rafael
Valley)] (Rosen et al. 2001, pp. 21-22). While this survey effort could
not confirm any specific extirpations of northern Mexican gartersnake
populations on a local scale in southeastern Arizona, most sites
yielded no snakes during resurvey (Rosen et al. 2001, Appendix I).
Our analysis of the best available data on the status of the
northern Mexican gartersnake distribution in the United States
indicates that its distribution has been significantly reduced in the
United States, and it is now considered extirpated from New Mexico
(Nickerson and Mays 1970, p. 503; Rosen and Schwalbe 1988, pp. 25-26,
Appendix I; Holm and Lowe 1995, pp. 27-35; Sredl et al. 1995b, pp. 2,
9-10; 2000, p. 9; Rosen et al. 2001, Appendix I; Painter 2005, 2006;
Holycross et al. 2006, p. 66; Brennan and Holycross 2006, p. 123; Radke
2006; Rosen 2006; Holycross 2006). Fitzgerald (1986, pp. 9-10) visited
33 localities of potential habitat for northern Mexican gartersnakes in
New Mexico in the Gila River drainage and was unable to confirm its
existence at any of these sites. The New Mexico Department of Game and
Fish State Herpetologist, Charles Painter, provided several causes that
have synergistically contributed to the decline of northern Mexican
gartersnakes in New Mexico, including bullfrog and nonnative fish
introductions, modification and destruction of habitat, commercial
exploitation, direct human-inflicted harm, and fragmentation of
populations. The last known observation of the northern Mexican
gartersnake in New Mexico occurred in 1994 on private land (Painter
2000, p. 36; Painter 2005).
Our analysis of the best available information indicates that the
northern Mexican gartersnake has likely been extirpated from a large
portion of its historical distribution in the United States. We define
a population as ``likely extirpated'' when there have been no northern
Mexican gartersnakes reported for a decade or longer at a site within
the historical distribution of the species, despite at least minimal
survey efforts, and natural recovery at the site is not expected due to
the presence of known threats. The perennial or intermittent stream
reaches and disassociated wetlands where the northern Mexican
gartersnake has likely been extirpated include: (1) The Gila River; (2)
the Lower Colorado River from Davis Dam to the International Border;
(3) the San Pedro River; (4) the Santa Cruz River downstream from the
International Border at Nogales; (5) the Salt River; (6) the Rio San
Bernardino from International Border to headwaters at Astin Spring (San
Bernardino National Wildlife Refuge); (7) the Agua Fria River; (8) the
Verde River upstream of Clarkdale; (9) the Verde River from the
confluence with Fossil Creek downstream to its confluence with the Salt
River; (10) Tanque Verde Creek in Tucson; (11) Rillito Creek in Tucson;
(12) Agua Caliente Spring in Tucson; (13) Potrero Canyon/Springs; (14)
Babocamari Cienega; (15) Barchas Ranch, Huachuca Mountain bajada; (16)
Parker Canyon Lake and tributaries in the Canelo Hills; and (17) Oak
Creek at Midgley Bridge (Rosen and Schwalbe 1988, pp. 25-26, Appendix
I; 1997, pp. 16-17; Rosen et al. 2001, Appendix I; Brennan and
Holycross 2006, p. 123; Holycross 2006; Holycross et al. 2006, pp. 15-
51, 66; Radke 2006; Rosen 2006). Information pertaining to the cause or
causes of extirpation of these sites is summarized in Table 1 below.
Conversely, our review of the best available information indicates
the northern Mexican gartersnake is likely extant in a fraction of its
historical range in Arizona. We define populations as ``likely extant''
when the species is expected to reliably occur in appropriate habitat
as supported by recent museum records and/or recent (i.e., less than 10
years) reliable observations. The perennial or intermittent stream
reaches and disassociated wetlands where we conclude northern Mexican
gartersnakes remain extant include: (1) The Santa Cruz River/Lower San
Rafael Valley (headwaters downstream to the International Border); (2)
the Verde River from the confluence with Fossil Creek upstream to
Clarkdale; (3) Oak Creek at Page Springs; (4) Tonto Creek from the
mouth of Houston Creek downstream to Roosevelt Lake; (5) Cienega Creek
from the headwaters downstream to the ``Narrows'' just downstream of
Apache Canyon; (6) Pantano Wash (Cienega Creek) from Pantano downstream
to Vail; (7) Upper Scotia Canyon in the Huachuca Mountains; and (8) the
Audubon Research Ranch and vicinity near Elgin
[[Page 56232]]
(Rosen et al. 2001, Appendix I; Caldwell 2005; Brennan and Holycross
2006, p. 123; Holycross 2006; Holycross et al. 2006, pp. 15-51, 66;
Rosen 2006).
The current status of the northern Mexican gartersnake is unknown
in several areas in Arizona where the species is known to have
historically occurred. We base this determination on mostly historical
museum records for locations where survey access is restricted, survey
data are unavailable or insufficient, and/or current threats could
preclude occupancy. The perennial or intermittent stream reaches and
disassociated wetlands where the status of the northern Mexican
gartersnake remains uncertain include: (1) The downstream portion of
the Black River drainage from the Paddy Creek confluence; (2) the
downstream portion of the White River drainage from the confluence of
the East and North forks; (3) Big Bonito Creek; (4) Lake O'Woods near
Lakeside; (5) Spring Creek above the confluence with Oak Creek; (6) Bog
Hole Wildlife Area; (7) Upper 13 Tank, Patagonia Mountain bajada; (8)
Babocamari River; and (9) Arivaca Cienega (Rosen and Schwalbe 1988,
Appendix I; Rosen et al. 2001, Appendix I; Brennan and Holycross 2006,
p. 123; Holycross 2006; Holycross et al. 2006, pp. 15-51; Rosen 2006).
In summary, after consultation with species' experts and land
managers, and based upon our analysis of the best available scientific
and commercial data, we conclude that the northern Mexican gartersnake
has been extirpated from 85 to 90 percent of its historical
distribution in the United States.
Status in Mexico. Throughout this finding, and due to the
significantly limited amount of available literature that addresses the
status of and threats to extant populations of the northern Mexican
gartersnake in Mexico, we rely in part on (1) information that
addresses the status of and threats to both riparian and aquatic
biological communities within the historical distribution of the
northern Mexican gartersnake in Mexico; and (2) information that
addresses the status of and threats to native freshwater fish within
the historical distribution of the northern Mexican gartersnake in
Mexico, which we use as ecological surrogates due to their similar
habitat requirements and their role as important prey species utilized
by the northern Mexican gartersnake. Observations on the status of
riparian and aquatic communities in Mexico are available but limited in
comparison to our knowledge of these communities in the United States.
The current distribution of the northern Mexican gartersnake in Mexico
is also not well understood, although its status is believed to be in
decline in many areas due to historical and continuing threats to its
habitat and prey base, as discussed below. A large number of springs
have dried up in several Mexican states within the distribution of the
northern Mexican gartersnake, namely, Chihuahua, Durango, Coahila, and
San Luis Potos[iacute] (Contreras Balderas and Lozano 1994, p. 381).
Contreras Balderas and Lozano (1994, p. 381) also stated that several
streams and rivers throughout Mexico and within the distribution of the
northern Mexican gartersnake have dried up or become intermittent due
to overuse of surface and groundwater supplies. We further acknowledge
that northern Mexican gartersnakes were historically distributed in
several regions within Mexico that have remained roadless and isolated
and, according to the information we were able to obtain regarding the
status of the northern Mexican gartersnake in Mexico, few ecological
investigations have occurred in these areas due to their remote nature
and the logistical difficulties that face research in such areas.
However, Mexican biologists Ramirez Bautista and Arizmendi (2004, p. 3)
were able to provide general information on the principal threats to
northern Mexican gartersnake habitat in Mexico which included the
dessication of wetlands, improper livestock grazing, deforestation,
wildfires, and urbanization. In addition, nonnative species, such as
bullfrogs and sport and bait 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). Given the lack of specific data on the status of the northern
Mexican gartersnake in Mexico, we cannot conclude with any degree of
certainty its overall status in Mexico.
Northern Mexican Gartersnake Distinct Population Segment
In the petition to list the northern Mexican gartersnake, the
petitioners specified several listing options for our consideration,
including listing northern Mexican gartersnake in the United States as
a DPS. Under the Act, we must consider for listing any species,
subspecies, or DPSs of vertebrate species/subspecies, if information is
sufficient to indicate that such action may be warranted. To implement
the measures prescribed by the Act and its Congressional guidance, we
developed a joint policy with the National Oceanic and Atmospheric
Administration (NOAA) Fisheries entitled Policy Regarding the
Recognition of Distinct Vertebrate Population (DPS Policy) to clarify
our interpretation of the phrase ``distinct population segment of any
species of vertebrate fish or wildlife'' for the purposes of listing,
delisting, and reclassifying species under the Act (61 FR 4721;
February 7, 1996). Under our DPS policy, we consider three elements in
a decision regarding the status of a possible DPS as endangered or
threatened under the Act. The elements are: (1) The population
segment's discreteness from the remainder of the taxon to which it
belongs; (2) the population segment's significance to the taxon to
which it belongs; and (3) the population segment's conservation status
in relation to the Act's standards for listing (i.e., when treated as
if it were a species, is the population segment endangered or
threatened?). Our policy further recognizes it may be appropriate to
assign different classifications (i.e., threatened or endangered) to
different DPSs of the same vertebrate taxon (61 FR 4721; February 7,
1996).
Discreteness
The DPS policy's standard for discreteness requires an entity given
DPS status under the Act to be adequately defined and described in some
way that distinguishes it from other populations of the species. A
population segment may be considered discrete if it satisfies either
one of the following conditions: (1) Marked separation from other
populations of the same taxon resulting from physical, physiological,
ecological, or behavioral factors, including genetic discontinuity; or
(2) populations delimited by international boundaries within which
differences in control of exploitation, management of habitat,
conservation status, or regulatory mechanisms exist that are
significant in light of 4(a)(1)(D) of the Act.
Marked Separation from Other Populations of the Same Taxon as a
Consequence of Physical, Physiological, Ecological or Behavioral
Factors. We do not have any information to indicate that a marked
separation exists between the United States and Mexico that would
distinguish populations of northern Mexican gartersnake in the United
States from those in Mexico. There is no information to indicate that a
marked separation exists as a result of physical, physiological,
ecological, or behavioral factors.
There has been no genetic analysis completed for the northern
Mexican gartersnake. Thus, we have no information to indicate that
genetic differences exist.
[[Page 56233]]
Populations Delimited by International Boundaries Within Which
Differences in Control of Exploitation, Management of Habitat,
Conservation Status, or Regulatory Mechanisms Exist that are
Significant. In terms of the conservation status of the northern
Mexican gartersnake, despite the significantly limited amount of
monitoring and/or survey data for the northern Mexican gartersnake in
Mexico, we believe there is a higher probability that the subspecies is
fairing better overall in Mexico in terms of having more total
populations, because a larger percentage of the overall range of the
subspecies (approximately 70 to 80 percent of it historical
distribution) occurs in Mexico. However, we have no information to
indicate that the populations on either side of the United States-
Mexico border have a more stable or better conservation status.
We recognize that differences in management regulatory protection
of northern Mexican gartersnake populations may exist between
populations within Mexico and those within the United States. These
differences primarily pertain to protections afforded to occupied
habitat. In Mexico, any activity that intentionally destroys or
adversely modifies occupied northern Mexican gartersnake habitat is
prohibited [SEDESOL 2000 (LGVS) and 2001 (NOM-059-ECOL-2001)]. Neither
the Arizona Game and Fish Department or the New Mexico Department of
Game and Fish can offer protections to occupied habitat. Instead, these
agencies regulate take in the form of lethal or live collection of
individuals which is prohibited in both states. However, any
conclusions that may be drawn with reference to differences in
management across the United States-Mexico border are largely
speculative due to the lack of information available as to the efficacy
and protections of these regulations in practice. Because we determine
in the following section that populations of the northern Mexican
gartersnake in the United States are not significant to the subspecies
as a whole, we need not address further the ``discreteness'' test of
the DPS policy. For further information on regulatory considerations,
please see our discussion under Factor D below.
Significance
Under our DPS policy, a population segment must be significant to
the taxon to which it belongs. The evaluation of ``significance'' may
address, but is not limited to, (1) evidence of the persistence of the
discrete population segment in an ecological setting that is unique for
the taxon; (2) evidence that loss of the population segment would
result in a significant gap in the range of the taxon; (3) evidence
that the population segment represents the only surviving natural
occurrence of a taxon that may be more abundant elsewhere as an
introduced population outside its historic range; and (4) evidence that
the discrete population segment differs markedly from other populations
of the species in its genetic characteristics.
Ecological Setting. Throughout its rangewide distribution, the
northern Mexican gartersnake occurs at elevations from 130 to 8,497 ft
(40 to 2,590 m) (Rossman et al. 1996, p. 172). The northern Mexican
gartersnake is considered a riparian obligate (restricted to riparian
areas when not engaged in dispersal behavior) and occurs chiefly in the
following general habitat types in both the United States and Mexico:
(1) Source--area wetlands [e.g., cienegas (mid-elevation wetlands with
highly organic, reducing (basic, or alkaline) soils), stock tanks
(small earthen impoundment), etc.]; (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; Arizona Game and Fish
Department 2001). Based on this information, we determine that
populations of the northern Mexican gartersnake in Arizona do not
occupy an ecological setting differing enough from populations that
occur in Mexico to be considered unique for the subspecies.
Gap in the Range. The Service can determine that a gap in a taxon's
range caused by the potential loss of a population would be significant
based on any relevant considerations. One factor which may support such
a determination is whether the loss of a geographic area amounts to a
substantial reduction of a taxon's range and this reduction is
biologically important. The United States comprised the most northern
portion of the northern Mexican gartersnake's range and constituted
approximately 20-30 percent of its rangewide historical distribution.
Because we do not currently know exactly what the status of the
northern Mexican gartersnake is in Mexico at this time, we are unable
to ascertain what percentage of extant populations occur in the United
States as compared to Mexico. However, this is not sufficient evidence
to support a determination that loss of the northern Mexican
gartersnake in the United States represents a substantial reduction in
the subspecies' range based on the geographic area which would be lost.
Furthermore, no area that is uniquely biologically significant to the
northern Mexican gartersnake is located within the United States as
compared to Mexico.
Another factor relevant to determining whether a gap is significant
is the biological significance of the number of total individuals of
the taxon in the population that may be lost. Although we have no data
on the absolute numbers of northern Mexican gartersnakes in the United
States or Mexico, the best available science suggests that there are
far more individuals in Mexico than in the United States, based on the
more extensive range in Mexico and the current low density and number
of extant populations in the United States. Therefore, we have no
information to indicate that the loss of between 8 and 17 populations
of northern Mexican gartersnakes known in the United States is
biologically significant to the taxon as a whole.
In conclusion, we have determined that the gap in the range of the
northern gartersnake that would be caused by the loss of the United
States population would not be significant because: (1) Loss of the
United States population would not constitute a substantial and
biologically important reduction of the range of the subspecies; (2)
the loss of the individuals in the United States would not be
biologically significant to the subspecies; and (3) we have not
identified any other reason why loss of the United States population
would result in a significant gap in the range of the subspecies.
Marked Differences in Genetic Characteristics. Within the
distribution of every species there exists a peripheral population, an
isolate or subpopulation of a species at the edge of the taxon's range.
Long-term geographic isolation and loss of gene flow between
populations is the foundation of genetic changes in populations
resulting from natural selection or change. Evidence of changes in
these populations may include genetic, behavioral, and/or morphological
differences from populations in the rest of the species' range. We have
no information to indicate that genetic differences exist between
populations of the northern Mexican gartersnake at the northern portion
of its range in the United States from those in Mexico. Therefore,
based on the genetic information currently available, the northern
Mexican gartersnake in the United States should not be considered
biologically or ecologically significant based simply on
[[Page 56234]]
genetic characteristics. Biological and ecological significance under
the DPS policy is always considered in light of Congressional guidance
(see Senate Report 151, 96th Congress, 1st Session) that the authority
to list DPS's be used ``sparingly'' while encouraging the conservation
of genetic diversity.
Whether the Population Represents the Only Surviving Natural
Occurrence of the Taxon. As part of a determination of significance,
our DPS policy suggests that we consider whether there is evidence that
the population represents the only surviving natural occurrence of a
taxon that may be more abundant elsewhere as an introduced population
outside its historic range. The northern Mexican gartersnake in the
United States is not the only surviving natural occurrence of the
subspecies. Consequently, this factor is not applicable to our
determination regarding significance.
Conclusion
Following a review of the available information, we conclude that
the northern Mexican gartersnake in the United States is not
significant to the remainder of the subspecies. We made this
determination based on the best available information, which does not
demonstrate that (1) these populations persist in an ecological setting
that is unique for the subspecies; (2) the loss of these populations
would result in a significant gap in the range of the subspecies; and
(3) these populations differ markedly from populations of northern
Mexican gartersnake in Mexico in their genetic characteristics, or in
other considerations that might demonstrate significance. Further,
available information does not demonstrate that the life history and
behavioral characteristics of the northern Mexican gartersnake in the
United States is unique to the subspecies. Therefore, on the basis of
the best scientific and commercial information available, we find that
proposing to list a DPS for the northern Mexican gartersnake in the
United States is not warranted; these populations do not meet the
definition of a distinct population segment. We are not addressing the
third prong of the DPS policy (i.e. the population segment's
conservation status in relation to the Act's standards for listing)
since we find that the United States portion of the range of the
northern Mexican gartersnake does not qualify as a listable entity
pursuant to our DPS policy, as discussed above.
Significant Portion of the Range
In the petition to list the northern Mexican gartersnake, the
petitioners also requested that we consider listing the species
throughout its range based on its status in the United States. As
required by the Act, we have considered in this finding whether the
northern Mexican gartersnake is in danger of extinction ``in all or a
significant portion of its range'' as defined in the terms ``threatened
species'' and ``endangered species'' pursuant to section 3 of the Act.
In order to determine if Arizona constitutes a significant portion of
the range of the subspecies, we evaluate whether threats in this
geographic area imperil the viability of the subspecies as a whole due
to any biological importance of this portion of the subspecies range.
Based upon the best scientific information available, we find that the
extant populations in the United States are not considered a stronghold
for the subspecies, they do not represent core or important breeding
habitat, we are not aware of any unique genetic or behavioral
characteristics, and we are not aware that threats in this portion of
its range threaten the whole subspecies with extinction. Therefore, we
determine that the extant populations of the northern Mexican
gartersnake in Arizona do not constitute a significant portion of the
range of the subspecies because there is no particular characteristic
to any segment within this portion of its range that would render it
biologically more significant to the taxon as a whole than other
portions of its current range.
We note that the court in Defenders of Wildlife v. Norton, 258 F.3d
1136 (9th Cir. 2001), appeared to suggest that a species could be in
danger of extinction in a significant portion of its range if there is
a ``major geographical area'' in which the species is no longer viable
but once was. Although we do not necessarily agree with the court's
suggestion, we have determined that the historical range of the
subspecies within the United States does not constitute a ``major
geographical area'' in this context. The portion of the northern
Mexican gartersnake's historical range in United States (20 to 30
percent) constitutes a small percentage of the total range of the
subspecies.
The petitioners also requested that we consider listing the species
throughout its range based on its rangewide status. Below we respond to
the petitioners request through our analysis of the five listing
factors for the United States and Mexico.
Summary of Factors Affecting the Northern Mexican Gartersnake
Section 4 of the Act (16 U.S.C. 1533), and implementing regulations
at 50 CFR 424, set forth procedures for adding species to the Federal
Lists of Endangered and Threatened Wildlife and Plants. Under section
4(a) of the Act, we may list a species on the basis of any of five
factors, as follows: (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. In making this finding, information
regarding the status of, and threats to, the northern Mexican
gartersnake in relation to the five factors provided in section 4(a)(1)
of the Act is discussed below and summarized in Table 1 below.
Table 1.--Summary of Northern Mexican Gartersnake Status and Threats by
Population in United States
[All locations in Arizona unless otherwise specified.]
------------------------------------------------------------------------
Regional historical/
Population locality Current status current threats
------------------------------------------------------------------------
Gila River.................... Extirpated....... Considered extirpated
by nonnatives,
improper grazing,
recreation,
development,
groundwater pumping,
diversions,
channelization,
dewatering, road
construction/use,
wildfire,
intentional harm,
dams, prey base
reductions.
Gila and San Francisco Extirpated....... Considered extirpated
Headwaters in New Mexico. by nonnatives,
improper grazing,
recreation, prey
base reductions.
Lower Colorado River from Extirpated....... Considered extirpated
Davis Dam to International by nonnatives, prey
Border. base reductions,
recreation,
development, road
construction/use,
borderland security/
undocumented
immigration,
intentional harm,
dams.
[[Page 56235]]
San Pedro River in United Extirpated....... Considered extirpated
States. by nonnatives, prey
base reductions,
improper grazing,
groundwater pumping,
road construction/
use, borderland
security/
undocumented
immigrants,
intentional harm.
Santa Cruz River downstream of Extirpated....... Considered extirpated
the Nogales area of the by nonnatives, prey
International Border. base reductions,
improper grazing,
development,
groundwater pumping,
diversions,
channelization, road
construction/use,
borderland security/
undocumented
immigrants,
intentional harm,
contaminants.
Salt River.................... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
diversions,
wildfire,
channelization, road
construction/use,
intentional harm,
dams.
Rio San Bernardino from Extirpated....... Considered extirpated
International Border to by nonnatives, prey
headwaters at Astin Spring base reductions,
(San Bernardino National borderland security/
Wildlife Refuge). undocumented
immigration,
intentional harm,
competition with
Marcy's checkered
gartersnake.
Agua Fria River............... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
development,
recreation, dams,
road construction/
use, wildfire,
intentional harm.
Verde River upstream of Extirpated....... Considered extirpated
Clarkdale. by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
diversions,
channelization, road
construction/use,
intentional harm.
Verde River from the Extirpated....... Considered extirpated
confluence with the Salt by nonnatives, prey
upstream to Fossil Creek. base reductions,
improper grazing,
recreation,
groundwater pumping,
diversions,
channelization, road
construction/use,
wildfire,
development,intentio
nal harm, dams.
Potrero Canyon/Springs........ Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing.
Tanque Verde Creek in Tucson.. Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
road construction/
use, intentional
harm.
Rillito Creek in Tucson....... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
road construction/
use, intentional
harm.
Agua Caliente Spring in Tucson Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
road construction/
use, intentional
harm.
Babocamari Cienega............ Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing.
Barchas Ranch, Huachuca Extirpated....... Considered extirpated
Mountain bajada. by nonnatives, prey
base reductions,
improper grazing,
borderland security/
undocumented
immigration,
intentional harm.
Parker Canyon Lake and Extirpated....... Considered extirpated
tributaries in the Canelo by nonnatives, prey
Hills. base reductions,
improper grazing,
recreation, road
construction/use,
borderland security/
undocumented
immigration,
intentional harm,
dams.
Oak Creek at Midgley Bridge... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
intentional harm.
Santa Cruz River/Lower San Extant........... Nonnatives, prey base
Rafael Valley (headwaters reductions, improper
downstream to International grazing, borderland
Border). security/
undocumented
im