Endangered and Threatened Wildlife and Plants; Listing the Blue-throated Macaw, 61208-61219 [2013-24215]

Agencies

• Fish and Wildlife Service
• DEPARTMENT OF THE INTERIOR

[Federal Register Volume 78, Number 192 (Thursday, October 3, 2013)]
[Rules and Regulations]
[Pages 61208-61219]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: 2013-24215]


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DEPARTMENT OF THE INTERIOR

Fish and Wildlife Service

50 CFR Part 17

[Docket No. FWS-R9-ES-2012-0034; 450 003 0115]
RIN 1018-AY68


Endangered and Threatened Wildlife and Plants; Listing the Blue-
throated Macaw

AGENCY: Fish and Wildlife Service, Interior.

ACTION: Final rule.

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SUMMARY: We, the U.S. Fish and Wildlife Service (Service), are listing 
the blue-throated macaw (Ara glaucogularis) as endangered under the 
Endangered Species Act of 1973, as amended (Act). This species is 
endemic to a small area in Bolivia, and there are estimated to be fewer 
than 500 individuals remaining in the wild. Its status remains tenuous 
despite conservation efforts. Threats to the species include: lack of 
reproductive success (loss of nestlings) due to nest failure, which 
primarily is caused by competition for nest sites and predation by 
larger avian species; and the lack of suitable, available habitat in 
addition to its small population size.

DATES: This final rule is effective November 4, 2013.

ADDRESSES: This final rule is available on the Internet at https://www.regulations.gov under Docket No. FWS-R9-ES-2012-0034. Comments and 
materials we received, as well as supporting documentation used in the 
preparation of this rule, are available for public inspection, by 
appointment, during normal business hours at: U.S. Fish and Wildlife 
Service, 4401 N. Fairfax Drive, Suite 400, Arlington, VA 22203.

FOR FURTHER INFORMATION CONTACT: Janine Van Norman, Chief, Branch of 
Foreign Species, Endangered Species Program, U.S. Fish and Wildlife 
Service, 4401 North Fairfax Drive, Room 420, Arlington, VA 22203; 
telephone 703-358-2171. If you use a telecommunications device for the 
deaf (TDD), call the Federal Information Relay Service (FIRS) at 800-
877-8339.

SUPPLEMENTARY INFORMATION:

Background

    The Endangered Species Act of 1973, as amended (Act) (16 U.S.C. 
1531 et seq.), is a law that was passed to prevent extinction of 
species by providing measures to help alleviate the loss of species and 
their habitats. Before a plant or animal species can receive the 
protection provided by the Act, it must first be added to one of the 
Federal Lists of Endangered and Threatened Wildlife and Plants. Section 
4 of the Act and its implementing regulations at part 424 of title 50 
of the Code of Federal Regulations (CFR) set forth the procedures for 
adding species to these lists.

Previous Federal Actions

    We received the petition to list this species on May 6, 1991, from 
Alison Stattersfield, of the International Council for Bird 
Preservation (ICBP). That petition requested that we list 53 foreign 
birds under the Act, including the blue-throated macaw, which is the 
subject of this final rule. We took several actions on this petition. 
On December 16, 1991, we published a positive 90-day finding and 
announced the initiation of a status review of the species included in 
the 1991 petition (56 FR 65207). On March 28, 1994, we published a 
document that served as our 12-month finding on the 1991 petition (59 
FR 14496). In that document, we announced our finding that listing 38 
species from the 1991 petition, including the blue-throated macaw, was 
warranted but precluded because of other, higher priority listing 
actions. The blue-throated macaw was assigned

[[Page 61209]]

a listing priority number (LPN) of 2. Species are assigned LPNs based 
on the magnitude and immediacy of threats, as well as their taxonomic 
status. A lower LPN corresponds to a higher priority to determine a 
listing status. An LPN of 2 reflects threats that are both imminent and 
high in magnitude, as well as the taxonomic classification of the blue-
throated macaw as a full species. In the May 3, 2011, Annual Notice of 
Review, we announced that listing was warranted but precluded for 20 
foreign species, including the blue-throated macaw.
    On January 10, 2013, we issued a proposed rule (78 FR 2239) to add 
the blue-throated macaw as endangered to the Federal List of Endangered 
and Threatened Wildlife.

Summary of Comments

    We base this rule on a review of the best scientific and commercial 
information available, including all information we received during the 
public comment period. In the January 10, 2013, proposed rule (78 FR 
2239), we requested that all interested parties submit information that 
might contribute to development of a final rule. The public comment 
period was open for 60 days, ending March 11, 2013. We also contacted 
appropriate scientific experts and organizations, and invited them to 
comment on the proposed listing in accordance with our peer review 
policy, described in the section below. We received 23 comments from 
members of the public including peer reviewer; these comments are 
available at https://www.regulations.gov under Docket No. FWS-R9-ES-
2012-0034).

Peer Review

    In accordance with our policy, ``Notice of Interagency Cooperative 
Policy for Peer Review in Endangered Species Act Activities,'' that was 
published on July 1, 1994 (59 FR 34270), we sought the expert opinion 
of three appropriate independent specialists regarding this rule. The 
purpose of such review is to ensure listing decisions are based on 
scientifically sound data, assumptions, and analysis. We sent copies of 
the proposed rule to the peer reviewers immediately following 
publication in the Federal Register. We invited these peer reviewers to 
comment, during the public comment period, on the specific assumptions 
and the data that were the basis for our conclusions regarding the 
proposal to list this species as endangered under the Act. We received 
comments from three peer reviewers.
    We reviewed all comments we received for substantive issues and new 
information regarding the proposed listing of this species; we address 
those comments below. Comments that provided support or opposition 
without substantive information were noted, but will not be addressed 
in this final rule. Some of the commenters did not appear to understand 
the criteria for listing under the Act. Therefore, we are providing 
clarification below. The following summarizes the comments we received 
and our responses.
    (1) Comment: Many commenters, while not opposed to the listing of 
the species, asked for a special rule under section 4(d) of the Act 
(also called a ``4(d) rule'') that would allow interstate trade of the 
species to occur.
    Response: Section 4(d) of the Act allows the Service to develop a 
special rule to apply the prohibitions of section 9 or to provide 
measures that are necessary and advisable to provide for the 
conservation of threatened species. A special rule cannot be 
promulgated for a species that is listed as endangered under the Act. 
Because we determined that listing the blue-throated macaw as 
endangered under the Act is appropriate, we are not able to develop a 
4(d) rule for this species. That said, not all interstate trade is 
prohibited under the ESA. Sale; offer for sale; and delivery, receipt, 
carrying, transport, or shipment in interstate or foreign commerce in 
the course of a commercial activity are prohibited. Interstate trade 
that is not sale, offer for sale, or in the course of a commercial 
activity is not regulated.
    (2) Comment: Several commenters, including individual bird breeders 
and the American Federation of Aviculture, objected to our finding, but 
did not provide new information relevant to the determination (for the 
specific content of these comments, see https://www.regulations.gov 
under Docket No. FWS-R9-ES-2012-0034).
    Response: We thank all the commenters for their interest in the 
conservation of this species and thank those commenters who provided 
information for our consideration in making this listing determination. 
Under section 4(b) of the Act, the Service is required to make listing 
determinations solely on the basis of the best scientific and 
commercial data available after conducting a review of the status of 
the species. When we published our proposed rule, we opened a public 
comment period during which we requested any additional information on 
the blue-throated macaw. In making this listing determination, we 
reviewed the best available scientific and commercial information, we 
contacted species experts, and we diligently searched for the most 
current information on this species. Therefore, we have obtained and 
considered the ``best scientific and commercial data available'' in our 
listing determination. After careful consideration, we conclude that 
this species meets the definition of an endangered species under the 
Act.

Effects of This Rule

Commercial Use

    The Act does not prohibit intrastate (within a State or U.S. 
territory) sale, offer for sale, or certain other intrastate activities 
of an endangered species. But, among other things, it does prohibit 
interstate (between States and U.S. territories) sale, offer for sale, 
and certain other activities such as transport in the course of a 
commercial activity of endangered species. If a person in the course of 
a commercial activity can demonstrate that such sale or other 
commercial use enhances the propagation or survival of the species, or 
that it is for scientific research, he or she may apply for a permit 
for these activities.
    Because interstate commercial use of endangered species is 
generally prohibited, if you wish to sell or otherwise commercially use 
your macaw(s), you would have to either sell the bird(s) to someone who 
resides within your home State, commercially use the bird within your 
State, or apply for a permit for interstate sale or commercial use of 
your bird(s). In addition, to be in compliance with the Act, any 
advertisements for the sale of your birds should include a statement 
that no sale involving parties from another state can be consummated 
until a permit has been obtained from the Service.

Captive Breeding

    The Service does not regulate captive breeding of listed species. 
This means that you are not prohibited from continuing to breed these 
birds. However, the Act does prohibit interstate and foreign sales, 
certain other interstate and foreign commercial activities, imports, 
and exports without a Service permit. Therefore, if you intend to sell 
any progeny, you will either need to sell them within the State the 
birds were bred to someone residing in the same State or, if intending 
to sell the birds outside the State where they were bred, you will need 
to obtain a Service permit. In addition, to be in compliance with the 
Act and its implementing regulations at 50 CFR Part

[[Page 61210]]

17, any advertisements for the sale of your birds should include a 
statement that no sale involving parties from another state can occur 
until a permit has been obtained from the Service. For more information 
on obtaining such a permit, see https://www.fws.gov/permits.

Personal Pets

    The Act does not restrict ownership of your personal pet or moving 
your personal pet across State lines for noncommercial purposes. There 
are no restrictions on traveling with or transporting legally obtained 
endangered species within the United States for your own personal use. 
No permit is required for you to travel or transport your pet macaw(s) 
within the United States, provided you are not selling or otherwise 
engaging in a commercial activity with the bird.

Summary of Changes From Proposed Rule

    This final rule incorporates changes to our proposed listing based 
on the comments we received and newly available scientific and 
commercial information. Peer reviewers generally commented that the 
proposed rule was thorough and comprehensive. There were different 
views on what the historical threats to the species were and 
differences in thoughts on the magnitude of the various factors 
currently affecting the species. For example, some peer reviewers and 
commenters indicated that illegal removal from the wild for the pet 
trade was the most significant factor affecting the species and that 
habitat loss and competition for nest sites had less of an effect on 
the species than predation. Others questioned the degree of the effect 
that botflies have on the species. There are very few individuals 
studying and working closely with this species, and we made our 
determinations based on the best available scientific and commercial 
information. None of the information collected during the comment 
period changed our final listing determination. A list of literature 
used in finalizing this determination and comments we received are 
available at https://www.regulations.gov under Docket No. FWS-R9-ES-
2012-0034.
    The most significant change is that, based on recent surveys, the 
population of this species appears to be greater than was previously 
believed. Recent surveys conducted by the Armonia Association and the 
Loro Parque Fundaci[oacute]n indicate that the wild population of the 
blue-throated macaw is likely between 350 to 400 individuals (Waugh 
2013, pers. comm.; Lebbin 2013, pers. comm.; Hennessey 2013, pers. 
comm.); including between 190 to 225 mature individuals (Waugh 2013, 
pers. comm.). Additionally, a population viability analysis on the 
blue-throated macaw was conducted and published in late 2012 (Strem and 
Bouzat 2012, pp. 12-24). It was not available at the time we were 
developing the proposed listing determination; however, this 
information is incorporated into this final listing determination.
    We also note that providing separate legal status to captive 
specimens of protected species is not permissible under the ESA.

Species Information

Taxonomy

    The taxonomic status of this species was disputed until fairly 
recently. The blue-throated macaw was previously considered an aberrant 
form of the blue-and-yellow macaw (A. ararauna), but these two species 
are known to occur sympatrically (in the same location) without 
interbreeding (Kyle 2007a; del Hoyo et al. 1997). Common names in 
Spanish for the blue-throated macaw include guacamayo barba azul and 
guacamayo caninde. Both BirdLife International (BLI) and the Integrated 
Taxonomic Information System (ITIS) recognize the blue-throated macaw 
as Ara glaucogularis. ITIS (https://www.itis.gov) is a database 
maintained by a partnership of U.S., Canadian, and Mexican federal 
government agencies, other organizations, and taxonomic specialists to 
provide taxonomic information. Therefore, we accept the species as Ara 
glaucogularis.

Population

    As of 1998, the species was known to occur in eight locations, and 
the total species' population was believed to be 100 to 150 individuals 
(Loro Parque Fundaci[oacute]n (LPF) 2002, p. 13). In October 2004, a 
new, small population was found at Santa Rosa, 100 kilometers (km) (62 
miles (mi)) west of what was believed to be the western-most edge of 
the species' range (LPF 2012; Herrera et al. 2007, p. 18). Biologists 
surveying for this species in 2004 found more birds than in previous 
surveys by searching outside known population locations in specific 
habitat types believed to support the blue throated macaw (palm groves 
and forested islands) (Herrera et al. 2007, p. 18). In 2007, a 
population of approximately 25 individuals was found one hour south of 
Trinidad (Kyle 2007a, p. 6). Also in 2007, a flock of approximately 70 
birds was observed near the Rio Mamor[eacute] (Asociaci[oacute]n 
Armon[iacute]a), in the vicinity of where the Barba Azul Nature Reserve 
is now located. Population surveys conducted between 2004 and 2008 by 
Asociaci[oacute]n Armon[iacute]a and LPF indicate that there are now 
likely between 350 to 400 individuals (Waugh 2013, pers. comm.).
    We note that there are likely more than 1,000 individual blue-
throated macaws held in captivity worldwide according to the 2011 North 
American Regional Studbook (Anderson 2011, p. 4).

Species Description

    Blue-throated macaws have a blue throat; a bare, white face 
containing identifiable blue-streaks; dark grey irises; and a large 
black bill (Anderson 2011, p. 4; Kyle 2007b, p. 16). Its forehead is 
also blue, and there is a lack of contrast between its remiges (large 
flight feathers on the wing) and upperwing covert (outer) feathers. 
This species is approximately the same size (85 centimeters (cm) or 33 
inches) as the blue-and-yellow macaw. However, the blue-throated macaw 
is not as competitive as the blue-and-yellow macaw in obtaining nesting 
cavities (Kyle 2007a). Male blue-throated macaws are larger than 
females at about 800 grams (1.76 pounds), and females weigh 
approximately 600 grams (1.32 pounds) (Kyle 2007b, p. 16).
    Blue-throated macaws, like other parrot species, are monogamous and 
tend to mate for life (Strem and Bouzat 2012, pp. 12-13). There is also 
a significant investment in the care for their young; blue-throated 
macaws are not fully independent of their parents for a full year 
(Berkunsky 2010, p. 5). Therefore, some breeding pairs may not produce 
nestlings every breeding season. The blue-throated macaw forms its 
nests in large tree cavities; its preferred nesting tree is the 
motac[uacute] palm (Attalea phalerata), which is native to Bolivia, 
Brazil, and Peru. The northern population of blue-throated macaws 
breeds between August to November, and the southern population breeds 
between November to March (Berkunsky 2012, pers. comm.; Kyle 2007a). 
The southern population, an hour south of Trinidad, tends to breed 
around the same time as the more commonly found blue-and-yellow macaw. 
This overlap of breeding seasons adds to competition for nest sites.
    Blue-throated macaws are sexually mature between 6 and 8 years of 
age (Strem 2008; Kyle 2007a, p. 6). Females lay one to three eggs per 
clutch (generally one clutch per year is produced), and the eggs 
incubate for 26 days. One to three hatchlings are raised, depending on 
food availability (BLI 2010; Kyle 2007a). Nestlings fledge at

[[Page 61211]]

between 13 and 14 weeks. Blue-throated macaws are seen traveling mostly 
in pairs but also have been seen in a large flock of between 70 and 100 
individuals (Herrera 2012, pers. comm.; Macleod et al. 2009, p. 15; 
Waugh 2007a, p. 53).

Diet

    This species seeks areas where palm fruits and suitable nesting 
cavities are readily available (Herrera et al. 2007, pp. 18-24). It 
feeds on fruits of approximately 12 species of trees (Kyle 2007a, pp. 
1-10). There are 84 species of palms in Bolivia (Moraes et al. 2001, p. 
234) and approximately 11 palm species within the blue-throated macaw's 
range. Blue-throated macaws prefer the fleshy part of the fruit, or 
mesocarp, of motac[uacute] and also Mauritia flexuosa (royal palms or 
carandai-guaz[uacute]), as well as Acrocomia aculeata (common names 
include: coyoli palm, gru-gru palm, macaw palm, acrocome, Coyolipalme, 
amankayo, corojo, corozo, baboso, tucuma, and totai) (Herrera 2007, p. 
20; Yamashita and M. de Barros 1997, p. 144; Jordan and Munn 1993; 
https://www.ars-grin.gov; https://www.pacsoa.org.au). The macaws first 
puncture the apex of the mesocarp and remove the outer layer (Yamashita 
and M. de Barros 1997, p. 144). The motac[uacute] continually produces 
fruit throughout the year. Between 80 and 90 percent of motac[uacute] 
palms produce fruits all year, but the peak is between July and 
December (LPF 2003, p. 21; Moraes et al. 1996, p. 424). Motac[uacute] 
is believed to be pollinated by beetles in the Mystrops genus (Moraes 
et al. 1996, p. 425). The same palm tree may produce at any one time 
between three and five racemes (flowering stalks, each with fruits in a 
different stage of development ripeness) (Yamashita and M. de Barros 
1997, p. 144).
    The species has also been observed at clay licks (Kyle 2007a, p. 
2), which are clay banks where the birds consume soil or minerals; 
however, the reason for the clay consumption remains unclear.

Range and Habitat Description

    The blue-throated macaw is endemic to the tropical savanna 
ecoregion of north-central Bolivia in the Department of Beni (Strem and 
Bouzat 2012, p. 13; LPF 2010; Kingsbury 2010, p. 8). This ecoregion is 
approximately 160,000 square kilometers (km\2\) (61,776 square miles 
(mi\2\)). (See Appendix A in Docket No. FWS-R9-ES-2012-0034 at https://www.regulations.gov for a map of the region (hereinafter referred to as 
``Appendix A'')). Within this region, the blue-throated macaw is found 
both in groups and in widely dispersed isolated pairs within an area 
estimated to be between 2,508 and 12,900 km\2\ (968 and 4,981 mi\2\) 
(Waugh 2013, pers. comm.; Strem and Bouzat 2012, p. 12; LPF 2012; BLI 
2012; Hesse 2000, p. 104). The species is found at elevations between 
200 and 300 meters (m) (656 and 984 feet (ft)) (Yamashita and M. de 
Barros 1997, p. 144; Brace et al. 1995). The blue-throated macaw's 
habitat was occupied by humans for thousands of years before European 
colonization (Erickson 2000, p. 2). Its habitat consists of lowlands in 
an area known as Llanos (plains) de Mojos, also known as Llanos de 
Moxos (LPF 2010; Mayle et al. 2007, p. 301; Yamashita and M. de Barros 
1997, p. 141). See Appendix A for a photo representing the flooded 
habitat. The Llanos de Mojos is a wide savannah plain with poor 
drainage and, in the wet season, is extremely susceptible to flooding. 
The floods cover large areas of the plains, and the area may remain 
flooded for 5 to 7 months in some areas. These plains include parts of 
the river basins of the It[eacute]nez, Mamor[eacute], Beni, and Madre 
de Dios Rivers (see Appendix A for a map; Yamashita and M. de Barros 
1997, p. 144).
    The blue-throated macaw's habitat has progressively diminished over 
thousands of years and its habitat is now primarily restricted to small 
``islands'' of suitable habitat within privately owned cattle pastures 
(see Appendix A for a photo illustrating these islands; Milpacher 2012, 
pers. comm.; Kingsbury 2010, p. 72; Berkunsky 2008, p. 4; Kyle 2007a, 
p. 4; Kyle 2006, p. 7; LPF 2003, p. 6). The species has been observed 
in flocks of up to 100 birds in the Barba Azul Nature Reserve (Waugh 
2013, pers. comm). The blue-throated macaw is believed to occur on 
ranches adjacent to the Barba Azul Nature Reserve, Ranches Las Gamas, 
Los Patos, Pelotal, and Juan Latino, but the status of the species is 
unclear in these areas (Kingsbury 2010, p. 89). In other parts of the 
species' range, the species is believed to occur on the ranches Elsner 
with Esp[iacute]ritu, San Rafael, and the Estancia El Dorado; however, 
to the best of our knowledge, these are privately managed, and the 
species is not being monitored on the ranches.

Palm Islands

    Palm-dominated forest islands form the blue-throated macaw's 
primary habitat. These ``islands'' are on elevated terrain and are 
sometimes referred to as ``alturas'' (high ground). The islands were 
primarily formed as mounds resulting from prehistoric human existence 
in this region (Erickson 2008, pp. 168-169). The lowlands are 
frequently inundated by water due to the flooding of nearby rivers (see 
Appendix A). Historically, human cultures manipulated the water flow to 
create plains that were higher and subsequently drier (Erickson 2008, 
pp. 168-169). The mounds are common throughout the savannas and 
wetlands of Bolivia; there may be as many as 10,000 of these mounds or 
islands in Bolivia (Erickson 2008, p. 169). They have been found to 
vary in size from a few hectares to many square kilometers (Erickson 
2008, pp. 168-169; Yamashita and M. de Barros 1997, p. 144). Most are 
raised less than one meter and are often surrounded by ponds or moat-
like ditches (Erickson 2008, pp. 168-169). Typically, these islands are 
surrounded by seasonally flooded grasslands; are between 0.2 and 1.0 
hectare (ha) (0.49 to 2.47 acre (ac)) in size; and are approximately 
130 to 235 m (426 to 771 ft) above sea level (Kingsbury et al. 2010, p. 
71; Yamashita and M. de Barros 1997, p. 144).
    Besides motac[uacute], palm species found on these islands are 
typically Syagrus botryophora (sumuqu[eacute]) and Astrocaryum vulgare 
(chontilla), interspersed with semi-deciduous emergent trees such as 
Enterolobium spp. (no common name (NCN)), Sterculia striata (NCN) and 
Tabebuia spp. (roble), and the Curupau tree (Anadenanthera colubrina) 
(also known as yopo, vilca, huilco, wilco, cebil, or angico) (Kyle 
2005, p. 7). Some trees such as Ceiba pentandra (mapajo or kapok tree) 
and Hura crepitans (common names include catahua, Ochoo, arbol del 
diablo, acacu, monkey's dinner-bell, habillo, ceiba de leche, sandbox 
tree, possum wood, dynamite tree, ceiba blanca, assacu, and posentri) 
can reach more than 40 m (131 ft) in height.
    The motac[uacute] palms may have survived on the mound islands for 
various reasons: their value to human cultures, their resistance to 
burning, and their ecological suitability to the microclimate. 
Motac[uacute] is not only vital to the life history of blue-throated 
macaws; it also has local, commercial, and ecosystem importance (Kyle 
2005, p. 3; Moraes et al. 1996, pp. 424-425). This species of palm is 
used in the local community as thatch for housing, which can last up to 
7 years. Its fruit is consumed by humans and various other species; 
parts of the palm tree are used to make baskets and brooms; and palm 
oil is sold commercially (Zambrana et al. 2007, p. 2785; Moraes et al. 
1996, pp. 425-426).

[[Page 61212]]

Significance of Palm Islands to Blue-Throated Macaws

    Habitat favored by blue-throated macaws contains tall, mature trees 
in areas with continuous motac[uacute] palm fruit production (Yamashita 
and M. de Barros 1997, p. 145). Densities of motac[uacute], the blue-
throated macaw's preferred nesting and feeding source, vary greatly. In 
the 1997 Yamashita and M. de Barros study, macaws were only observed in 
areas where motac[uacute] represented more than 60 percent of the 
trees.
    Natural cavities in dead or decaying trees (usually motac[uacute] 
palms) are the primary source of nesting sites for this species. Blue-
throated macaws prefer dead trees that have cavities with a minimum 
internal diameter of 30 cm (11.8 inches) for nesting, and, therefore, 
the tree must have a diameter at breast height of 60 cm (23.6 inches) 
or greater (see Appendix A for a picture representing a tree cavity; 
Yamashita and M. de Barros 1997, p. 145).

Factors Affecting the Species

    Section 4 of the Act, and its implementing regulations at 50 CFR 
part 424, set forth the procedures for adding species to the Federal 
Lists of Endangered and Threatened Wildlife and Plants. Under section 
4(a)(1) of the Act, we may list a species based on any of the following 
five factors: (A) The present or threatened destruction, modification, 
or curtailment of its habitat or range; (B) overutilization for 
commercial, recreational, scientific, or educational purposes; (C) 
disease or predation; (D) the inadequacy of existing regulatory 
mechanisms; and (E) other natural or manmade factors affecting its 
continued existence. Listing actions may be warranted based on any of 
the above factors, singly or in combination. We considered all of these 
factors in determining that the blue-throated macaw qualifies as an 
endangered species. Each of these factors is considered and evaluated 
in this document.
    In analyzing threats to a species, the Service focuses its analysis 
on threats acting upon wild specimens within the native range of the 
species because the goal of the Act is survival and recovery of the 
species in its native ecosystems. We do not separately analyze 
``threats'' to captive-held specimens because the statutory five 
factors are not well-suited to consideration of specimens in captivity 
and captive-held specimens are not eligible for separate consideration 
for listing. But we do consider the extent to which specimens held in 
captivity create, contribute to, reduce, or remove threats to the 
species.

Loss of Palm Islands Due to Habitat Conversion

    Within the past few hundred years, the blue-throated macaw lost 
much of its remaining habitat due to conversion of palm forests to 
pasture for cattle grazing. Cattle are not native to Bolivia; they were 
introduced to Bolivia in the 1600s. After the Second World War, cattle 
ranching and the associated burning of pastures began significantly 
impacting the landscape (Robison et al. 2000, p. 61). The macaw's 
preferred habitat is now limited to a few small, isolated islands of 
suitable habitat that are surrounded by these cattle ranches (Gilardi 
2012, pers. comm.). During the flooding season, which can occur for up 
to 6 months of a year, cattle take refuge on the motac[uacute] palm 
islands because the islands are drier due to their higher elevation 
(LPF 2003, p. 33). In general, there is no direct conflict between the 
cattle themselves and blue-throated macaws, but cattle can degrade 
their habitat by trampling. Adding to habitat loss, in the preferred 
habitat of the blue-throated macaw where these motac[uacute] palms 
remain (within privately owned cattle ranches), local ranchers 
typically burn the pastures annually (Berkunsky 2008, p. 4; del Hoyo 
1997). This type of burning results in almost no recruitment of native 
palm trees, which are vital to the ecological needs of the blue-
throated macaw (Yamashita and M. de Barros 1997, p. 144). The reduction 
in habitat (reduced availability of motac[uacute] palms) and lack of 
recruitment of motac[uacute] palms is a concern for in the future for 
blue-throated macaws because it takes several years for motac[uacute] 
palms to be able to produce fruit and to develop into a size suitable 
for nesting cavities.
    As mitigation, local conservation efforts are not only planting 
trees that provide food for blue-throated macaws, they are also 
conducting educational efforts directed towards land owners within the 
range of the blue-throated macaw. Additionally, the Barba Azul Nature 
Reserve is currently expanding (to 11,000 ha) (27,181 ac) to include 
adjacent ranches where the blue-throated macaw is believed to breed. 
The land newly incorporated into the protected area has more palm 
islands with better forest (Waugh 2013, pers. comm.). However, projects 
designed to provide additional habitat for this species are in the 
early stages of development and it is too early to evaluate the 
effectiveness of these efforts.
    The lack of nesting cavities (suitable habitat) is often a limiting 
factor for bird species that depend on these cavities for nesting 
(Sandoval and Barrantes 2009, p. 75; Kyle 2006, p. 8). To raise their 
young, blue-throated macaws require specific nesting cavities that 
provide protection from predation and flooding. Additionally, many 
different species compete for these increasingly rare nest sites. The 
loss of suitable trees is one factor that has resulted in increased 
competition from other species for these nesting cavities. The impact 
of habitat loss is compounded by extreme weather events and contributes 
to other factors that affect blue-throated macaws, such as an increase 
in vulnerability to predation and competition for nests.

Nest Failure

    Nest failure (the failure of nestlings to survive to fledgling 
stage) continues for various reasons, despite intensive conservation 
efforts (Berkunsky 2010, p. 4; Kyle 2006, p. 8). Some of the causes of 
nest failure include: predation, infestation by botflies (parasites in 
the Philornis genus), exposure to severe weather events such as 
flooding, and competition for food and shelter with other species such 
as bees (Berkunsky 2010, pp. 4-5). Many nestlings die in early 
developmental stages, often due to starvation (due to lack of food or 
parental neglect, exposure to cold temperatures, or flooding (Kyle 
2007a, pp. 1-10). If parents do not have access to enough nutritional 
food sources, some nestlings are neglected so that their other 
nestlings will survive. Nestlings can also fall out of collapsed trees 
before they have fledged. During five field seasons of closely 
observing nest sites, 43 percent of the active nests (30 active nests) 
were predated (Berkunsky 2008, p. 5; Kyle 2007a, pp. 7-8). See 
additional discussion below under the Exposure to Extreme Weather 
Events section.

Predation

    Predation is a key factor limiting this species' population growth 
in some areas of its range (Kyle 2007a, pp. 3, 6-7; Kyle 2006, p. 8). 
During one season of observation, all nestlings within three nests of 
seven active blue-throated macaw nests were lost to predation (Kyle 
2007a, pp. 6-8). Because the species has such a small population size 
with likely fewer than 500 individuals remaining in the wild, losses 
such as this have a significant effect on the status of the species as 
a whole. Predators of the blue-throated macaw include:
     Toco toucan (Ramphastos toco),
     Crane hawk (Geranospiza caerulescens),

[[Page 61213]]

     Great-horned owl (Bubo virginianus), and
     Southern crested caracara (Caracara plancus, a bird of 
prey).
    The blue-throated macaw's habitat of sparse, palm-forested islands 
scattered among natural grasslands, increases the species' 
vulnerability to nest predation (Kyle 2007a, pp. 6-7). Tree nest 
cavities chosen by blue-throated macaws tend to be visible to other 
avian species flying overhead. In addition to nesting on palm islands, 
blue-throated macaws are also known to nest in isolated palms in open 
fields, which are even more exposed than nests on palm islands (Herrera 
et al. 2007, p. 20). All of the species that predate on adult blue-
throated macaws, eggs, or nestlings have large distributions and are 
commonly found at the habitat islands used by blue-throated macaws 
(Kyle 2007a, pp. 6-7). Great horned owls have been seen at many sites 
where blue-throated macaws are nesting (Kyle 2007a, p. 6). These owls, 
native to South America, have a vast range, are the most widely 
distributed owl in South America, and occupy a variety of habitats 
including open forest, farmland, and grassland.
    Because blue-throated macaw nests may be concentrated in these 
small ``islands'' of trees within cattle pastures, they are more easily 
located by predators than species that nest in a continuous forest 
setting. To discourage and mitigate the effects of predation, some 
conservation activities being conducted include the monitoring and 
discouragement of predators from attacking blue-throated macaw nests. 
These efforts are intensive. In one case, where it appeared the nest 
tree was collapsing, the tree was monitored all night by conservation 
staff (Kyle 2007a, p. 9). Often trees containing active nests are 
monitored in this way if persistent predation has been observed. The 
mitigation efforts are helpful if nestlings can survive until they are 
at least 300 grams (0.66 pounds), they have a greater chance of 
survival (Kyle 2007a, p. 7). However, these mitigation projects are in 
the early stages of development and it is too early to evaluate the 
effectiveness of these efforts.
    Botfly parasites can also cause mortality of nestlings and have 
been observed in blue-throated macaw nestlings. During some parts of 
their life cycle, botflies live subcutaneously, and feed on macaw 
tissue (Olah et al. in press; Wunderle Jr. and Arendt 2011, p. 39). 
Botflies significantly reduce the energy available for nestling growth 
and development (Uhazy and Arendt 1986 in Wunderle Jr. and Arendt 2011, 
p. 39) and can contribute to reduced fitness and in some cases death of 
nestlings. In one study of avian nestlings, botfly parasitism caused 56 
percent of mortalities, while egg and chick losses from nest predators 
and competitors accounted for less than 10 percent of reproductive 
failures (Arendt 2000 in Wunderle Jr. and Arendt 2011, p. 39).

Exposure to Extreme Weather Events

    Because this species has a small population, the blue-throated 
macaw is also vulnerable to natural catastrophic events such as 
flooding, drought, and other stochastic disturbances (Strem and Bouzat 
2012, p. 12; Kyle 2006, pp. 5-6). Bolivia is described as a 
``climatically volatile region'' and is one of the countries in the 
world most affected by natural disasters in recent years (Oxfam 
International 2009, p. 5). This species' habitat experiences extreme 
changes over the course of a year.
    For many months of the year, the blue-throated macaw's habitat is 
flooded; at other times during the year, its habitat suffers from 
severe drought. During periods of drought, nestlings are sometimes 
neglected and starve.
    High rainfall occurs during the summer months; the wet season is 
between September and May. Annual precipitation is between 110 and 250 
cm (43 and 98 in) (Haase and Beck 1989 in Kingsbury 2010, p. 9). Very 
heavy rainfall in this region can continue for long periods of time 
(Kyle 2006, pp. 5-6; Hanagarth and Sarmiento 1990 in Beck and Moraes, 
undated). Every 6 to 12 years, 80 to 90 percent of the region is 
inundated (Beck and Moraes, undated). Although these areas are 
seasonally flooded, they are also prone to periods of drought (Kyle 
2007a, p. 3; Mayle et al. 2007, p. 294; Yamashita and M. de Barros 
1997, p. 144).
    Severe storms, such as one that occurred in 2005, are described as 
``nest killers.'' These severe storms cause the dead palm trees in 
which the nests have been constructed to collapse or flood (Kyle 2007b, 
p. 15), which causes nest failure for the season and subsequently no 
recruitment.
    Dead palm trees often collapse in these storms. During the 2006-
2007 season, this phenomenon was observed when the nest of one blue-
throated macaw pair in a dead motac[uacute] palm tree collapsed due to 
strong winds (Kyle 2007a, p. 4). Although the reason is unclear, these 
dead palm trees are currently the preferred sites for nest construction 
by the blue-throated macaw, and the species has strong nest site 
fidelity (Berkunsky 2012, pers. comm.). The extent to which this 
behavior is learned and modified is also unclear. However, researchers 
are working with the blue-throated macaw to introduce nest sites that 
are safer and less prone to predation and nest failure due to extreme 
weather events such as flooding (Berkunsky 2010, pp. 4-5).
    Flooding, a significant cause of nest failure in the recent past, 
has not been documented since 2008 at monitored and human-manipulated 
nests. This is due to one of the conservation measures in place: 
drilling drain holes in the nests and at the bottom of the dead palm 
trees to prevent nest flooding. However, flooding can still occur if 
nests are not monitored and manipulated.

Competition for Nest Sites

    In addition to nest failure, there is a shortage of nests in some 
areas. As described above, there is little remaining of the preferred 
habitat of motac[uacute] palms. The species appears to ``learn'' 
nesting sites, and will re-use nesting locations that they had used in 
the past (Berkunsky 2010; Kyle 2007a, p. 4). Blue-throated macaws 
choose to nest in the top of dead motac[uacute] palms which provide 
easy access to their preferred food source. These nesting sites also 
expose the birds to predation, competition from other species for 
nests, drought, excessive rainfall, and nest flooding. Many species, in 
addition to the blue-throated macaw, use the motac[uacute] palm for 
feeding and nesting. In the Llanos de Mojos, there are 21 species of 
parrots that may compete for nest sites (Kingsbury et al. 2010, p. 83; 
Yamashita and M. de Barros 1997, p. 144). Some species known to compete 
for nest sites with the blue-throated macaw include the blue and yellow 
macaw, woodpeckers, and bees (Kyle 2007a, p. 6; LPF 2003, p. 33).
    In order to provide more choices for nesting habitat, conservation 
organizations are installing nest boxes. In 2009, in the Barba Azul 
Nature Reserve, 46 artificial nests were monitored, in part by video 
cameras; however, the majority of them (24 nests) were occupied by blue 
and yellow macaws (LPF 2010, p. 15). Likely due to the larger size of 
the blue and yellow macaw or perhaps their more aggressive nature, blue 
and yellow macaws usually win most confrontations for nests (Kyle 
2007a, p. 6). During the 2010 field study at the Barba Azul Nature 
Reserve, researchers also observed that there were a greater number of 
blue and yellow macaws using the Barba Azul Nature Reserve than blue-
throated macaws (Kingsbury 2010, p. 83). At an area where both species 
were drinking water, researchers noted that the blue-throated macaws 
exhibited agitated behavior when blue-and-yellow macaws were nearby 
(Kingsbury 2010, p. 83). Although the Barba Azul Nature Reserve

[[Page 61214]]

was established specifically for the blue-throated macaws, other 
species use the reserve and compete for nesting sites.
    As stated earlier, to mitigate this problem, at least two 
conservation organizations are installing nest boxes to create more 
available sites for nesting, but despite the past 10 years of 
conservation efforts and experimentation with nest boxes, nest failure 
still occurs. In addition to predation, other reasons for nest failure 
are numerous, which has instigated the experimentation and installation 
of these nest boxes. Bees and other species continue to compete with 
blue-throated macaws for these nest boxes. After many years of 
experimentation, the nest boxes are slowly becoming more effective at 
providing suitable nesting sites. Blue-throated macaws seem to 
habituate to certain nesting sites and locations, likely based on food 
availability and learned behavior.
    Although blue-throated macaws have begun to use some of the nest 
boxes, it has been a slow and tedious process to encourage blue-
throated macaws to use these boxes, and the population continues to 
suffer losses, particularly due to nest failure, which the installation 
of suitable nest boxes is attempting to alleviate. When nests fail (no 
nestlings survive that season), a significant amount of effort has been 
expended by that breeding pair. Because this species has such a small 
population (likely there are fewer than 500 individuals remaining in 
the wild), each nestling survival has great significance to the overall 
species' status. The effect of the death of each new nestling on the 
population of blue-throated macaws is devastating to the viability of 
the population. If the nestlings survive the first season to the point 
that they fledge, their chances of survival are much greater than when 
they are new nestlings and are entirely dependent on their parents for 
survival.
    Bees can also make both natural nesting cavities and manmade nest 
boxes inhospitable for blue-throated macaws (Berkunsky 2008, p. 5). At 
the beginning of one breeding season, 67 percent of nest boxes 
monitored were occupied by bees (Berkunsky 2008, p. 5). After being 
removed, bees had returned within 2 weeks. Most naturally occurring 
nest sites, because there are so few of them and they are in demand by 
numerous species, require intense monitoring and manipulation in order 
to maintain an attractive, suitable environment for blue-throated 
macaws.

Disease

    Macaws are susceptible to many bacterial, parasitic, and viral 
diseases (Kistler et al. 2009, p. 2,176; Portaels et al. 1996, p. 319; 
Bennett et al. 1991). Macaws are prone to many viral infections such as 
retrovirus, pox virus, and paramyxo virus, which can cause weakened 
immune systems and subsequent death (Gaskin 1989, pp. 249, 251, 252). 
Recently, an examination of tissue revealed the likely presence of the 
pox virus in dead blue-throated macaw nestlings, indicating that close 
contact between blue-throated macaws and domestic poultry may be 
facilitating pathogen transmission to this species (Wildlife 
Conservation Society (WCS) in litt. 2011). In one location within the 
limited range of the species, blue-throated macaws share water sources 
with chickens, ducks, and other birds (WCS in litt. 2011; Kingsbury 
2010, p. 83). Blue-throated macaws in this area are being closely 
monitored to decrease the possibility of transmission of the pox virus; 
however, it remains a concern.
    Proventricular dilatation disease (PDD) is one of the most serious 
diseases known to affect parrots (Kistler et al. 2008, p. 2). PDD, also 
known as avian born virus (ABV) or macaw wasting disease, is a fatal 
disease that poses a serious threat to all captive-held and wild 
parrots worldwide, particularly those with very small populations 
(Kistler et al. 2008, p. 1; Abramson et al. 1995, p. 288). This 
contagious disease causes damage to the nerves of the upper digestive 
tract, so that food digestion and absorption are negatively affected. 
The disease has a 100-percent mortality rate in affected birds, 
although the exact manner of transmission between birds is unclear 
(Kistler et al. 2008, p. 1). PDD has been documented in several 
continents in more than 50 different parrot species and in free-ranging 
species in at least five other orders of birds (Kistler et al. 2008, p. 
2). This disease is concerning because blue-throated macaws share water 
sources with other species of birds, and this disease could be 
transmitted between individuals that are within close range.
    This species is closely monitored in the wild; conservationists 
working with this species are taking precautions so that diseases are 
not introduced into the wild population. Despite close monitoring and 
precautions, disease is likely to affect this extremely small 
population; therefore, we are concerned that diseases will become 
problematic to this species in the wild. At this time, we do not find 
that disease is contributing to the risk of extinction of blue-throated 
macaws, but it may affect this species in the future.

Small Population Size

    An additional factor that affects the continued existence of this 
species is its small, declining population of likely fewer than 500 
individuals in the wild. Recently, two observations have been made: (1) 
Malformations in chicks, and (2) reduced fertility in many reproductive 
pairs (WCS in litt. 2011). Small, rapidly declining populations of 
species, combined with other threats such as reduced reproductive 
success, lead to an increased risk of extinction (Strem and Bouzat 
2012, p. 22; Harris and Pimm 2008, p. 169).
    Species tend to have a higher risk of extinction if they occupy a 
small geographic range and occur at low density (Purvis et al. 2000, p. 
1949). A small, declining population size renders a species vulnerable 
to any of several risks including inbreeding depression, loss of 
genetic variation, and accumulation of new mutations. A species' small 
population size, combined with its restricted range may increase the 
species' vulnerability to adverse natural events and manmade activities 
that destroy individuals and their habitat (Holsinger 2000, pp. 64-65; 
Young and Clarke 2000, pp. 361-366; Primack 1998, pp. 279-308). 
Extinction risk is heightened in small, declining populations by an 
increased vulnerability to the loss of genetic variation due to 
inbreeding depression and genetic drift (changes in relative frequency 
of gene sequences). This, in turn, compromises a species' ability to 
adapt genetically to changing environments (Frankham 1996, p. 1507) and 
reduces fitness, thus increasing extinction risk (Reed and Frankham 
2003, pp. 233-234). Inbreeding can have individual or population-level 
consequences either by increasing the phenotypic expression (the 
outward appearance or observable structure, function, or behavior of a 
living organism) of recessive, deleterious alleles (harmful gene 
sequences) or by reducing the overall fitness of individuals in the 
population (Charlesworth and Charlesworth 1987, p. 231; Shaffer 1981, 
p. 131).
    Strem and Bouzat indicated in their population viability analysis 
(PVA) that continuing threats, such as declines in abundance, small 
population size, and low population growth rates, make this species 
highly vulnerable to any change (2012, p. 12). Their study indicated 
that even small increases in habitat loss (2 percent) and population 
harvesting (3 percent) had severe effects on the population (2012, p. 
12). We note that Strem and Bouzat conducted the PVA simulations using 
only published data

[[Page 61215]]

on the blue-throated macaw population size (2012, p. 13). However, even 
considering the recent discovery of a new population, the researchers 
indicated that ``multiple anthropogenic factors threaten the species' 
survival over the long term'' (Strem and Bouzat 2012, p. 22). They 
noted that the results showed that the blue-throated macaw has a 
relatively low probability of extinction over the next 50 years. 
However, they also noted that after the 50- to 100-year period 
considered for the simulations, population decreased considerably to 
approximately half of the initial abundance (Strem and Bouzat 2012, p. 
22).
    This species faces many challenges: it has many predators, limited 
suitable habitat, and competition from other species for nest sites, in 
addition to its small population size. Any loss of potentially 
reproducing individuals could have a devastating effect on the ability 
of its population to increase. Small populations have a higher risk of 
extinction due to random environmental events (Shaffer 1987, pp. 69-75; 
Gilpin and Soule 1986, pp. 24-28; Shaffer 1981, p. 131). Because of its 
small population and restricted range, the blue-throated macaw is 
vulnerable to random environmental events; in particular, it is 
threatened by extreme precipitation events and nest flooding.

Removal From the Wild

    Removal of macaws from the wild over the past few hundred years 
contributed to this species' small population size (LPF 2012; Herrera 
and Hennessey 2009, p. 233; Kyle 2007a). Macaws, both live and dead, 
have been a significant part of Bolivian culture for thousands of 
years. Evidence of this exists in pre-Colombian Andean feather art 
(American Museum of Natural History 2012). Feathers have been used 
historically in headdresses, and parrots have been used in ceremonial 
sacrifices (American Museum of Natural History 2012; Berdan 2004, p. 4; 
Creel and McKusick 1994, pp. 510-511). Feathers of blue-throated macaws 
would still be used for headdresses today if it were not for 
intervention and education programs implemented by nongovernmental 
conservation organizations (NGCOs) (BLI 2012; LPF 2010; LPF 2003, p. 
29). In addition to being used in ceremonies and costumes, there is 
evidence that parrots have been household pets since at least A.D. 1000 
(Creel and McKusick 1994, pp. 513-515) as evidenced in burial remains; 
live macaws likely had commercial value even during that time period. 
Parrots were traded over long distances; archeological remains indicate 
that parrots were found well outside their native range (Creel and 
McKusick 1994, pp. 515-516).
    Historically, the most significant impact to the decline of this 
species' population was likely due to collection of birds from the wild 
during the late 1800s and early 1900s (Yamashita and M. de Barros 1997, 
p. 144). During this time period, bird-skin traders of European descent 
sold thousands of bird skins, particularly in the United States, for at 
least three generations (Yamashita and M. de Barros 1997, p. 144; 
Trimble 1936, pp. 41-43).

The Inadequacy of Existing Regulatory Mechanisms

    Under the Act, we are required to evaluate whether the existing 
regulatory mechanisms are adequate. There are limited regulatory 
mechanisms in place to protect this species (de la Torre et al. 2011, 
p. 334; Herrera and Hennessey 2007, p. 295; LPF 2003, pp. 6-7). This 
species is considered critically endangered by the International Union 
for Conservation of Nature (IUCN) (BLI 2012; LPF 2012). However, IUCN 
rankings do not confer any actual protection or management. This 
species is listed in Appendix I of the Convention on International 
Trade in Endangered Species of Wild Fauna and Flora (CITES) (CITES 
2012). CITES regulates international trade in animal and plant species 
listed under the Convention. For additional information on CITES, visit 
https://www.cites.org. An Appendix-I listing includes species threatened 
with extinction whose trade is permitted only under exceptional 
circumstances, which generally precludes commercial trade. These 
protections under CITES were put in place for the blue-throated macaw 
because the species had suffered substantial population declines 
throughout its range due to habitat destruction and overexploitation.
    The government of Bolivia has enacted various laws and regulatory 
mechanisms to protect and manage wildlife and their habitats in 
Bolivia. For example, the Bolivian Government prohibits and imposes 
sanctions against the possession and the trafficking of any protected 
species, such as the blue-throated macaw (LPF Recovery Plan 2003, p. 
7). Additionally, the CITES listing and the ban by the Bolivian 
Government in 1984 to export this species effectively limit legal 
international trade (LPF 2012; Herrera and Hennessey 2009, pp. 233-234; 
LPF Recovery Plan 2003, p. 7). However, even after the export of this 
species was prohibited in the 1980s, and despite the laws in place and 
the intense conservation efforts ongoing for this species, localized 
illegal trade is still occurring.
    International trade in this species is now negligible (https://www.unep-wcmc.org, accessed June 4, 2012). International trade of the 
blue-throated macaw was initially restricted by the listing of the 
species in Appendix II of CITES in 1981, and in 1983, the species was 
transferred from Appendix II to Appendix I. The World Conservation 
Monitoring Centre (WCMC) at the United Nations Environment Programme 
(UNEP) manages a CITES Trade Database on behalf of the CITES Parties. 
Each Party to CITES is responsible for compiling and submitting annual 
reports to the CITES Secretariat regarding their country's 
international trade in species protected under CITES. Data obtained 
from UNEP-WCMC (https://www.unep-wcmc.org/citestrade) show that during 
the 2-year period (1981-1982) that the blue-throated macaw was listed 
in Appendix II, a total of 29 specimens (all live birds) were legally 
exported from Bolivia. The trade database indicates that a total of 84 
specimens (all live birds) have been exported from Bolivia since the 
species was listed in Appendix I in 1983, with no specimens traded 
between 1993 and 2010). The CITES database does not indicate any trends 
in the trade data to cause concern.
    In addition to Bolivia's restrictions and the trade restrictions 
implemented through CITES, the Wild Bird Conservation Act (WBCA) that 
was enacted in 1992 in the United States may have assisted in dampening 
the demand for this species. The purpose of the WBCA is to promote the 
conservation of exotic birds and to ensure that importation of exotic 
birds into the United States does not negatively affect wild 
populations. The WBCA generally restricts the importation of most 
CITES-listed live or dead exotic birds except for certain limited 
purposes such as zoological display or cooperative breeding programs. 
Import of dead specimens is allowed for scientific specimens and museum 
specimens. The Service may approve cooperative breeding programs and 
subsequently issue import permits under such programs. Wild-caught 
birds may be imported into the United States if certain standards are 
met and they are subject to a management plans that provides for 
sustainable use. Parrot imports to the United States were already 
declining before the enactment of the WBCA, but the WBCA contributed to 
curtailing the import of wild parrots.

[[Page 61216]]

    Although international trade is not a concern, poaching for local 
sale continues to occur (LPF 2012; Herrera and Hennessey 2009, p. 233; 
Kyle 2007a). Although Bolivia banned the export of live parrots in 1984 
(Brace et al. 1995, pp. 27-28), localized illegal trade within South 
America continued to occur, although it became less frequent (Herrera 
and Hennessey 2009, p. 233). For example, in 1993, investigators 
reported that an Argentinian bird dealer was offering Bolivian dealers 
a ``high price'' for blue-throated macaws (Jordan and Munn 1993, p. 
695).
    More recently, a study of markets in Santa Cruz, Bolivia estimated 
that over 22,000 individuals of 31 parrot species were illegally traded 
during 2004-2005, despite Bolivian laws (Herrera and Hennessey 2007, p. 
298). Bolivian Law 1333 (Ministerio de Desarrollo Sostenible y 
Planificacion 1999), Article 111 states that all persons involved in 
trade, capture, and transportation without authorization of wild 
animals will suffer a 2-year prison sentence together with a fine 
equivalent to 100 percent of the value of the animal. This law is 
supported by an addendum that states that all threatened species are of 
national importance and must be protected (Herrera and Hennessey 2007, 
p. 295). Asociaci[oacute]n Armon[iacute]a (a nonprofit organization in 
Bolivia) monitored the trade of wild birds that passed through a pet 
market in Santa Cruz, Bolivia between July 2004 to December 2007 
(Herrera and Hennessey 2009, p. 233; Herrera and Hennessey 2007, p. 
295). During the 2004-2005 study period, none of the parrots found were 
blue-throated macaws. In 2006, two blue-throated macaws were found for 
sale (Herrera and Hennessey 2009, p. 233). However, the blue-throated 
macaw was absent in the market during the monitoring period prior to 
2006, and no blue-throated macaws were found for sale in this market in 
2007 (Herrera and Hennessey 2009, p. 233; Herrera and Hennessey 2007, 
p. 295). This absence of the species in the market may be due either to 
the effectiveness of the ongoing conservation programs and laws in 
Bolivia, or it may be indicative of the scarcity of blue-throated 
macaws in the wild. Ninety-four percent of the birds documented were 
believed to be wild-caught. This illegal activity occurs despite the 
national laws that ban unauthorized trade (Herrera and Hennessey 2007, 
p. 298).
    The high value of this species could lead to continued illegal 
trade. An internet search indicated that captive-bred specimens of this 
species sell for between $1,500 and $3,000 in the United States (https://www.hoobly.com, accessed September 13, 2010). One search advertised 
that this is a ``very rare species and there are only 300 left in the 
wild.'' However, alternatively, because these birds are not difficult 
to breed in captivity, the supply of captive-bred birds has increased, 
which some experts believe may be alleviating illegal collection of 
wild birds (Waugh 2007a).
    Removal of blue-throated macaws from the wild can have a 
particularly devastating effect given their low reproductive rate and 
slow recovery from various environmental pressures (Lee 2010, p. 3; 
Wright et al. 2001, p. 711). Some blue-throated macaws have even been 
used for fish bait (Kyle 2007a, p. 7). The remains of a blue-throated 
macaw were found near a lake stuffed into a tree cavity with a bag of 
salt (Kyle 2007a, p. 7). Because this species has so few individuals 
remaining, any removal from the wild is extremely detrimental to the 
survival of the species when considered with all of the other factors 
acting upon the species.

Other Factors

    An additional factor that affects the nesting success of blue-
throated macaws is the availability of food sources--not only the 
abundance of food, but the timing of its availability. Phenology (how 
the timing of plant life cycle events interacts with animal biological 
processes) is influenced by variations in climate. The timing of 
motac[uacute] palm fruit production is critical for various life stages 
of the blue-throated macaw, particularly during the period following 
hatching. The motac[uacute] palms, on which blue-throated macaws depend 
for nesting as well as feeding, are affected by drought, burning, and 
excessive rainfall. In years when there is significant drought or 
excessive rainfall, the fruiting abundance and timing of fruit 
production can significantly affect the success of nestlings, or it can 
prohibit blue-throated macaws from even attempting to nest (Kyle 2007). 
In some seasons when food is not as plentiful, breeding pairs may 
choose not to brood, and the weakest of the nestlings are neglected by 
its parents and die of starvation (Kyle 2007a, pp. 4-5). During these 
times, in some cases, the diet is supplemented by these conservation 
organizations; however, it is a very intensive process.
    In summary, there are many factors that are causing stress to this 
species' population in the wild. It is affected by several factors such 
as habitat loss and degradation (factor A), poaching to a limited 
extent (factor B), predation (factor C), and nest flooding and lack of 
nest sites in part due to competition from other species but also due 
to habitat loss and degradation (factor E). Despite numerous laws and 
regulatory mechanisms to administer and manage wildlife and their 
habitats, existing laws are inadequate (factor D) to protect the 
species and its habitat from these other factors. Combined with its 
reduced population size, the species lacks sufficient redundancy and 
resiliency to recover from present and future threats without 
intervention and intense conservation actions. This was corroborated by 
the recent PVA conducted in 2012, regarding the viability of the 
population of the blue-throated macaw (Strem and Bouzat 2012, p. 22). 
Overall, the researchers indicate that population growth rates are 
likely not at replacement levels because the species has undergone a 
rapid population reduction over the past 50 years, in part due to 
habitat loss and poaching (Strem and Bouzat 2012, p. 20). The PVA found 
that growth rate estimates do not reach the rate of replacement 
necessary to maintain the viability of population over the long term 
(Strem and Bouzat 2012, p. 20), making the species particularly 
vulnerable to any change or threat. These factors acting on the species 
are expected to continue into the future.

In-situ Conservation

    This species is considered by many organizations to be the most 
endangered macaw remaining in the wild (BLI 2012; World Parrot Trust 
(WPT) 2012; LPF 2010; LPF 2003, p. 4). Several NGCOs are working 
intensely on various conservation projects to protect this species and 
its habitat. Various NGCOs have been involved in the conservation of 
this species since 1995, with authorization from the Bolivian 
Government (Waugh 2013, pers. comm.; Gilardi 2012, pers. comm.; LPF 
2002, p. 10). NGCOs involved include Asociaci[oacute]n Armon[iacute]a 
(Bolivia's BirdLife International partner), the Loro Parque 
Fundaci[oacute]n (LPF), and WPT. A species recovery plan that provides 
the basis for the blue-throated macaw conservation program was approved 
by Bolivia's Ministry for Sustainable Development in 2004, and has been 
in place since then (LPF 2003, pp. 6-7).
    Within its breeding range, a multitude of efforts are in progress 
to conserve the species (Waugh 2013, pers. comm.; Gilardi 2012, pers. 
comm.; Berkunsky 2010, p. 5, Kyle 2007, pp. 1-11). Conservation 
measures include constant monitoring, protection, and manipulation of 
nests; supplementing nestlings' diet when food sources are scarce; 
agreements with private landowners to protect this species'

[[Page 61217]]

habitat; patrolling existing macaw habitat by foot and motorbike; and 
monitoring the Beni lowlands for additional populations (LPF 2012; Kyle 
2007a; Snyder et al. 2000). NGCOs have implemented cooperation 
agreements with the Federation of Cattle Farmers of the Beni (FEGABENI) 
and the local authorities in Trinidad, Bolivia (LPF et al. 2003, p. 6).
    Land acquisition to expand protected habitat for this species has 
been funded by the World Land Trust and the Loro Parque 
Fundaci[oacute]n (Waugh 2013, pers. comm.). In 2008, Asociaci[oacute]n 
Armon[iacute]a and LPF purchased a 3,555-ha (8,785-ac) reserve for the 
purpose of establishing a protected area for the blue-throated macaw 
(World Land Trust 2010, https://www.worldlandtrust-us.org, accessed July 
16, 2010; BLI 2008). In 2010, the Barba Azul Nature Reserve 
(``Reserve'') was expanded by 1,123 ha (2,775 ac), creating a total 
protected area for the blue-throated macaws of 4,664 ha (11,525 ac) 
(Asociaci[oacute]n Armon[iacute]a 2012). Currently, this Reserve is the 
only protected area designated for the blue-throated macaw. The legal 
protections that apply fall under Bolivian Law 1333 (Ministerio de 
Desarrollo Sostenible y Planificacion 1999), Article 111. This Reserve 
protects savanna habitat, and habitat restoration is occurring in the 
Reserve, although it is unclear the extent the Reserve is used by blue-
throated macaws. The actual protections in place include monitoring of 
habitat, local education and awareness programs about the species, and 
establishment of suitable nesting sites. Approximately 70 blue-throated 
macaws have been observed in or around this Reserve (Herrera 2012, 
pers. comm.); however, these macaws may be some of the same macaws that 
are observed in other parts of the species' range during the breeding 
season (Berkunsky 2012, pers. comm.).
    Despite the existence of the Reserve, there are no nests in the 
Reserve that are known to be occupied by blue-throated macaws (Herrera 
2012, pers. comm.). Although the species is present in the Barba Azul 
Nature Reserve, it has not yet been shown to be breeding there (Waugh 
2013, pers. comm). There is evidence that they use the Reserve for 
feeding (Herrera 2012, pers. comm.; Kingsbury 2010, pp. 69-82). New 
information provided indicates that the blue-throated macaws that 
inhabit this Reserve and adjacent ranches are different than the birds 
in the southern portion of its range (see Appendix A for a map of the 
species' range; Strem and Bouzat 2012, p. 23; Milpacher 2012, pers. 
comm.; Herrera 2012, pers. comm.). Other than the Barba Azul Nature 
Reserve, there are no protected areas in the Llanos de Mojos except the 
Beni Biosphere Reserve, which has been in existence since 1986. 
However, to our knowledge, the blue-throated macaw does not use the 
Beni Biosphere Reserve (Hesse and Duffield 2000, p. 258).
    In addition to conservation efforts, the NGCOs working in Bolivia 
are conducting field research to better understand the current state of 
this species. However, the conservation work is difficult due to 
various factors that affect the species. Because some of this species' 
habitat is flooded for 6 months of the year, monitoring its habitat is 
difficult during certain seasons (Berkunsky 2010, p. 5). There have 
also been discussions of reintroducing captive-raised birds into the 
wild; however, this practice could inadvertently introduce disease into 
the wild population if precautions are not taken to minimize the 
transmission of disease to other blue-throated macaws (Sainsbury et al. 
2012, p. 442).
    Another conservation measure in place is research on the 
motac[uacute] palm (Milpacher 2012, pers. comm.) because the number of 
motac[uacute] palms is decreasing. This palm species plays a 
significant role in the life cycle of the blue-throated macaw. One 
study found that the old and senescent motac[uacute] palms are 
significantly more abundant than the younger palms (LPF 2003, p. 21). 
Based on their findings, researchers concluded that the islands 
containing motac[uacute] are not regenerating motac[uacute] palms 
sufficiently. It is likely that the lack of regeneration is due to 
overgrazing by cattle and excessive use of fire over centuries (Kyle 
2006, p. 5). The World Parrot Trust has recently attempted several 
small-scale palm germination experiments to assess reestablishing palm 
habitat (Milpacher 2012, pers. comm.). The motac[uacute] palm has 
commercial value in addition to its ecological role. Palm trees are 
used for a multitude of purposes, such as thatch for housing, fruit, 
and palm oil (de la Torre et al. 2011, pp. 327-369; Zambrana et al. 
2007, pp. 2771-2778). Motac[uacute] palm-dominated islands may have 
persisted in part due to their various ecological and commercial 
values, but they certainly persist in part because the islands are 
raised areas within the lowlands that are prone to flooding. With 
respect to the short term, local researchers believe that there will be 
adequate motac[uacute] fruits in the region for a few more decades (LPF 
2003, p. 21); however, research on the motac[uacute] is vital to the 
conservation of the blue-throated macaw.
    Educational awareness programs are in place in addition to research 
and monitoring. As an example, the Asociaci[oacute]n Armon[iacute]a is 
involved in an awareness campaign to encourage that the protection and 
conservation of these birds occurs at a local level (e.g., protection 
of macaws from trappers and the sustainable management of key habitats, 
such as palm groves and forest islands, on private property) (Llampa 
2007; BLI 2008a; Snyder et al. 2000). Two educational awareness centers 
have been established in the towns of Santa Ana del Yacuma and Santa 
Rosa del Yacuma (LPF 2010, p. 16). In response to the limited but 
continued poaching that occurs in the wild, LPF initiated a travelling 
exhibition, ``Extinction is Forever,'' which visited 17 urban 
localities in Bolivia in 2010 (LPF 2010, p. 15). The exhibition 
includes 21 photographs that explain the ancestral and present-day 
relationship between people and birds, and highlights the effects of 
illegal trade of wild birds in Bolivia currently. An estimated 1,000 
visitors attended each showing in the main cities (LPF 2010, p. 15).
    Reproductive success is vital to the blue-throated macaw's 
recovery, and this species faces many challenges to successfully 
reproducing. This species' nests often have an open crown (i.e., no 
roof) and are prone to flooding (Berkunsky 2010, p. 4; Kyle 2007a, p. 
3). During many seasons, nests, eggs, and nestlings are destroyed due 
to flooding. Both WBT and Asociaci[oacute]n Armon[iacute]a have been 
conducting conservation activities, such as installation of artificial 
nest boxes that provide safe habitat, manipulating nests so that they 
do not flood, and discouraging predators and nest competitors. The 
installation of a multitude and variety of nest boxes is a way to boost 
breeding success. Because many other species compete for these nest 
boxes, and blue-throated macaws tend to re-use previously used nesting 
sites, the process of introducing nest boxes and encouraging blue-
throated macaws to use them, while discouraging other species from 
using them, is a very time-intensive process. Despite all of these 
conservation efforts, fewer than 500 individuals of this species are 
believed to remain in the wild. In summary, the conservation efforts 
underway are abundant, but will need to continue in order to have 
lasting impacts on the species.
    It is our policy that we do not consider captive-held specimens in 
our analysis of the five factors under Section 4(a) of the Act; we do 
not believe that it was within the Congressional intent when the Act 
was written, unless there is some obvious reason for doing so. For 
additional background on our interpretation of the provisions of the

[[Page 61218]]

Act, see 78 FR 35204, June 12, 2013. We do not believe that captive-
held members of blue-throated macaws either create or contribute to 
threats to the species or remove or reduce threats to the species. 
There are likely more than 1,000 individual blue-throated macaws held 
in captivity worldwide according to the 2011 North American Regional 
Studbook, however, many of these birds are of uncertain origin 
(Anderson 2011, p. 4). We also note that it is not possible to separate 
captive-held specimens as a different legal status under the Act.

Finding (Listing Determination)

    In assessing whether the blue-throated macaw meets the definition 
of an endangered or threatened species, we considered the five factors 
in section 4(a)(1) of the Act. A species is ``endangered'' for purposes 
of the Act if it is in danger of extinction throughout all or a 
significant portion of its range and is ``threatened'' if it is likely 
to become endangered within the foreseeable future throughout all or a 
significant portion of its range. In considering what factors might 
constitute threats to a species, we must look beyond the mere exposure 
of the species to the factor to evaluate whether the species may 
respond to the factor in a way that causes actual impacts to the 
species. If there is exposure to a factor and the species responds 
negatively, the factor may be a threat and we attempt to determine how 
significant a threat it is. The threat is significant if it drives, or 
contributes to, the risk of extinction of the species such that the 
species may warrant listing as endangered or threatened as those terms 
are defined in the Act. We conducted a review of the status of this 
species and assessed whether the blue-throated macaw is endangered or 
threatened throughout all or a significant portion of its range.
    We have assessed the best scientific and commercial information 
available regarding the past, present, and future threats affecting 
this species. Historically, the blue-throated macaw existed in much 
higher numbers in more continuous, connected habitat; its suitable 
habitat is now extremely small. Its small population size, combined 
with its restricted range, increases the species' vulnerability to 
adverse natural events that destroy individuals and their habitat. It 
is subject to inbreeding depression, loss of genetic variation, and 
accumulation of new mutations. In addition to its small population 
size, many factors currently affect blue-throated macaws. These 
include: Inadequate nest sites (both in abundance and effectiveness); 
nest (clutch) failure (when one or all of the nestlings fail to survive 
to fledgling stage due to a variety of reasons such as starvation, 
inadequate nutrition, sibling competition); nest flooding; botflies; 
competition for nests with more competitive species, such as bees, and 
other avian species, such as large woodpeckers and other macaw species; 
and predation by numerous species, particularly other bird species 
(such as toucans, owls, vultures, other raptors, and even other macaw 
species). Regulatory mechanisms are ineffective at reducing the factors 
affecting the blue-throated macaw (Factor D).
    We have determined that captive-held specimens cannot be given 
separate consideration under the ESA based on their captive state (see 
78 FR 35204, June 12, 2013), but captive-held specimens can, in some 
cases, create, contribute to, reduce, or remove threats to the species. 
We have no information in this case indicating that captive-held blue-
throated macaws either create or contribute to threats to this species 
or remove or reduce threats to the species. Due to the effectiveness of 
CITES and, in the United States, the WBCA, international trade for pets 
is not a concern. Removal of some birds from the wild for the pet trade 
may still be occurring, but there is no information indicating to what 
extent animals currently held in captivity are motivating poachers to 
capture and remove additional birds from the wild. Regarding whether 
captive-held birds reduce any threats to the species, there are likely 
more than 1,000 individual blue-throated macaws held in captivity 
worldwide according to the 2011 North American Regional Studbook. 
However, many of these birds are of uncertain origin (Anderson 2011, p. 
4) and may harbor diseases that do not exist in the wild population and 
therefore may not be suitable for reintroduction efforts.
    Our review of the information pertaining to the five threat factors 
supports a conclusion that these factors place the blue-throated macaw 
in danger of extinction throughout all of its range, such that a 
listing of endangered is warranted. The species is currently in danger 
of extinction because the species exists at such low levels that it is 
vulnerable to a multitude of threats. Given the species' low 
reproductive capacity, it is very difficult to increase to the levels 
of abundance that allow the species to withstand such events. All of 
these factors are now and will continue to result in threats to the 
continued existence of the species. We also examined the blue-throated 
macaw to analyze if any other listable entity under the definition of 
``species,'' such as subspecies or distinct population segments, may 
qualify for a different status. However, because of the magnitude and 
uniformity of the threats throughout its range, we find that there are 
no other listable entities that may warrant a different determination 
of status. Since threats extend throughout its entire range, it is 
unnecessary to determine if the blue-throated macaw is in danger of 
extinction throughout a significant portion of its range.
    Based on our evaluation of the best available scientific and 
commercial information and given its current population size, and 
severely limited distribution throughout its historical range, we have 
determined the species is in danger of extinction throughout all of its 
range and thus meets the definition of an endangered species. Because 
the species is in danger of extinction now, as opposed to in the 
foreseeable future, the blue-throated macaw meets the definition of an 
endangered species rather than a threatened species. Therefore, we are 
listing the blue-throated macaw as endangered under the Act.

Available Conservation Measures

    Conservation measures provided to species listed as endangered 
under the Act include recognition, requirements for Federal protection, 
and prohibitions against certain practices. Recognition through listing 
results in public awareness, and encourages and results in conservation 
actions by Federal and State governments, private agencies and interest 
groups, and individuals.
    The Act and its implementing regulations set forth a series of 
general prohibitions and exceptions that apply to all endangered 
wildlife. These prohibitions, at 50 CFR 17.21, in part, make it illegal 
for any person subject to the jurisdiction of the United States to 
``take'' (includes harass, harm, pursue, hunt, shoot, wound, kill, 
trap, capture, or to attempt any of these) within the United States or 
upon the high seas; import or export; deliver, receive, carry, 
transport, or ship in interstate or foreign commerce in the course of 
commercial activity; or sell or offer for sale in interstate or foreign 
commerce any endangered wildlife species. It also is illegal to 
possess, sell, deliver, carry, transport, or ship any such wildlife 
that has been taken in violation of the Act. Certain exceptions apply 
to agents of the Service, other Federal land management agencies, the 
National Marine Fisheries Service, and State conservation agencies.
    Permits may be issued to carry out otherwise prohibited activities 
involving endangered wildlife species under certain circumstances.

[[Page 61219]]

Regulations governing permits for endangered species are codified at 50 
CFR 17.22. With regard to endangered wildlife, a permit may be issued 
for the following purposes: For scientific purposes, to enhance the 
propagation or survival of the species, and for incidental take in 
connection with otherwise lawful activities.

Clarity of Rule

    We are required by Executive Orders 12866 and 12988 and by the 
Presidential Memorandum of June 1, 1998, to write all rules in plain 
language. This means that each rule we publish must:
    (a) Be logically organized;
    (b) Use the active voice to address readers directly;
    (c) Use clear language rather than jargon;
    (d) Be divided into short sections and sentences; and
    (e) Use lists and tables wherever possible.
    If you feel that we have not met these requirements, send us 
comments by one of the methods listed in the ADDRESSES section. To 
better help us revise the rule, your comments should be as specific as 
possible. For example, you should tell us the names of the sections or 
paragraphs that are unclearly written, which sections or sentences are 
too long, the sections where you feel lists or tables would be useful, 
etc.

National Environmental Policy Act (NEPA)

    We have determined that environmental assessments and environmental 
impact statements, as defined under the authority of the National 
Environmental Policy Act of 1969 (42 U.S.C. 4321 et seq.), need not be 
prepared in connection with regulations adopted under section 4(a) of 
the Act. We published a notice outlining our reasons for this 
determination in the Federal Register on October 25, 1983 (48 FR 
49244).

References Cited

    A list of all references cited in this rule is available on the 
Internet at https://www.regulations.gov under Docket No. FWS-R9-ES-2012-
0034 or upon request from the Branch of Foreign Species, Endangered 
Species Program, U.S. Fish and Wildlife Service.

Author

    The primary author of this rule is Amy Brisendine, Branch of 
Foreign Species, Endangered Species Program, U.S. Fish and Wildlife 
Service.

List of Subjects in 50 CFR Part 17

    Endangered and threatened species, Exports, Imports, Reporting and 
recordkeeping requirements, Transportation.

Regulation Promulgation

    Accordingly, we amend part 17, subchapter B of chapter I, title 50 
of the Code of Federal Regulations, as set forth below:

PART 17--[AMENDED]

0
1. The authority citation for part 17 continues to read as follows:

    Authority: 16 U.S.C. 1361-1407; 1531-1544; and 4201-4245, unless 
otherwise noted.


0
2. Amend Sec.  17.11(h) by adding a new entry for ``Macaw, blue-
throated'' in alphabetical order under BIRDS to the List of Endangered 
and Threatened Wildlife to read as follows:


Sec.  17.11  Endangered and threatened wildlife.

* * * * *
    (h) * * *

--------------------------------------------------------------------------------------------------------------------------------------------------------
                        Species                                                    Vertebrate
--------------------------------------------------------                        population where                                  Critical     Special
                                                            Historic range       endangered or         Status      When listed    habitat       rules
           Common name                Scientific name                              threatened
--------------------------------------------------------------------------------------------------------------------------------------------------------
 
                                                                      * * * * * * *
              Birds
 
                                                                      * * * * * * *
Macaw, blue-throated.............  Ara glaucogularis...  Bolivia............  Entire.............  E                       814           NA           NA
 
                                                                      * * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------

* * * * *

    Dated: September 20, 2013.
Rowan W. Gould,
Acting Director, U.S. Fish and Wildlife Service.
[FR Doc. 2013-24215 Filed 10-2-13; 8:45 am]
BILLING CODE 4310-55-P