Endangered and Threatened Wildlife and Plants; Listing Foreign Bird Species in Peru and Bolivia as Endangered Throughout Their Range

DEPARTMENT OF THE INTERIOR

Fish and Wildlife Service

50 CFR Part 17

[Docket No. FWS-R9-IA-2009-0059; 4500030115]

RIN 1018-AV77

Endangered and Threatened Wildlife and Plants; Listing Foreign Bird Species in Peru and Bolivia as Endangered Throughout Their Range

AGENCY:

Fish and Wildlife Service, Interior.

ACTION:

Final rule.

SUMMARY:

We, the U.S. Fish and Wildlife Service (We or Service), determine endangered status for the following six South American bird species (collectively referred to as species for purposes of this final rule) under the Endangered Species Act of 1973, as amended (Act): Ash-breasted tit-tyrant

(Anairetes alpinus),

Junín grebe

(Podiceps taczanowskii),

Junín rail

(Laterallus tuerosi),

Peruvian plantcutter

(Phytotoma raimondii),

royal cinclodes

(Cinclodes aricomae),

and white-browed tit-spinetail

(Leptasthenura xenothorax).

These species are in danger of extinction throughout all of their ranges. All six species are native to Peru. The ash-breasted tit-tyrant and royal cinclodes are also native to Bolivia.

DATES:

This rule becomes effective August 23, 2012.

ADDRESSES:

This final rule is available on the Internet at

http://www.regulations.gov

. Comments and materials received, as well as supporting documentation used in the preparation of this rule, are available for public inspection at

http://www.regulations.gov

or by appointment, during normal business hours at: U.S. Fish and Wildlife Service, Endangered Species Program, 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. If you use a telecommunications device for the deaf (TDD), call the Federal Information Relay Service (FIRS) at 800-877-8339.

SUPPLEMENTARY INFORMATION:

Executive Summary

On January 5, 2010, we published a proposed rule (75 FR 606) to list these six foreign bird species as endangered: Ash-breasted tit-tyrant, Junín grebe, Junín rail, Peruvian plantcutter, royal cinclodes, and white-browed tit-spinetail. These species are all native to Peru. The ash-breasted tit-tyrant and royal cinclodes are also native to Bolivia. Each of these six species is affected by the loss and degradation of habitat. In addition to severely contracted ranges and distributions of these species, their small, declining populations are an additional threat to their survival.

This action is authorized by the Endangered Species Act of 1973 (Act) (16 U.S.C. 1531

et seq.

), as amended. It affects part 17, subchapter B of chapter I, title 50 of the Code of Federal Regulations.

These six foreign bird species will be listed as endangered under the Act.

Background

On January 5, 2010, we published a proposed rule (75 FR 606) to list these six species as endangered: Ash-breasted tit-tyrant

(Anairetes alpinus),

Junín grebe

(Podiceps taczanowskii),

Junín rail

(Laterallus tuerosi),

Peruvian plantcutter

(Phytotoma raimondii),

royal cinclodes

(Cinclodes aricomae),

and white-browed tit-spinetail

(Leptasthenura xenothorax).

These species are all native to Peru. The ash-breasted tit-tyrant and royal cinclodes are also native to Bolivia.

We opened the public comment period on the proposed rule for 60 days, which ended March 8, 2010, to allow all interested parties an opportunity to comment on the proposed rule.

We are addressing these six species under a single rule for efficiency. Each of these species is affected by similar threats. The major threat to these species is the loss and degradation of habitat. In addition to severely contracted ranges and distributions of these species, their small, declining populations are an additional threat. In this rule, we combined the evaluation of species that face similar threats within the same general habitat type and geographic area into one section to maximize our limited staff resources.

Previous Federal Actions

On May 6, 1991, we received a petition (the 1991 petition) from the International Council for Bird Preservation (ICBP) to add 53 foreign bird species to the List of Endangered and Threatened Wildlife, including the six Peruvian bird species that are the subject of this proposed rule. In response to the 1991 petition, we published a substantial 90-day finding on December 16, 1991 (56 FR 65207), for all 53 species and initiated a status review. On March 28, 1994 (59 FR 14496), we published a 12-month finding on the 1991 petition, along with a proposed rule to list 30 African birds under the Act (which included 15 species from the 1991 petition). In that document, we announced our finding that listing the remaining 38 species from the 1991 petition, including the six Peruvian bird species that are the subject of this proposed rule, was warranted but precluded by higher priority listing actions. We made a subsequent warranted-but-precluded finding for all outstanding foreign species from the 1991 petition, including the six Peruvian bird species that are the subject of this proposed rule, as published in our annual notice of review (ANOR) of foreign species on May 21, 2004 (69 FR 29354).

Per the Service's listing priority guidelines (September 21, 1983; 48 FR 43098), our 2007 ANOR (77 FR 20184, April 23, 2007) identified the listing priority numbers (LPNs) (ranging from 1 to 12) for all outstanding foreign species. The six Peruvian bird species that are the subject of this proposed rule were designated with an LPN of 2, and we determined that their listing continued to be warranted but precluded because of other listing actions. A listing priority of 2 indicates that the species faces imminent threats of high magnitude. With the exception of the listing priority ranking of 1, which addresses monotypic genera that face imminent threats of high magnitude, LPN categories 2 and 3 are among the Service's highest priorities for listing.

On July 29, 2008 (73 FR 44062), we published in the

Federal Register

a notice announcing our annual petition findings for foreign species. In that notice, we announced listing to be warranted for 30 foreign bird species, including the six Peruvian bird species that are the subject of this proposed rule, and stated that we would promptly publish proposals to list these 30 taxa. In selecting these six species from the list of warranted-but-precluded species, we took into consideration the magnitude and immediacy of the threats to the species, consistent with the Service's listing priority guidelines.

On September 8, 2008, the Service received a 60-day notice of intent to sue from the Center for Biological Diversity (CBD) and Peter Galvin over violations of section 4 of the Act for the Service's failure to promptly publish listing proposals for the 30 warranted species identified in our 2008 ANOR. Under a settlement agreement approved by the U.S. District Court for the Northern District of California on June 15, 2009, (

CBD et al.

v.

Salazar,

09-CV-02578-

CRB), we were required to submit to the

Federal Register

proposed listing rules for the ash-breasted tit-tyrant, Junín grebe, Junín rail, Peruvian plantcutter, royal cinclodes, and white-browed tit-spinetail by December 29, 2009. That proposed rule published on January 5, 2010 (75 FR 606).

Summary of Changes From the Proposed Rule

This final rule incorporates changes to our proposed listing based on new information located on these species since the proposed rule was published, including comments and information received from peer reviewers. In order to be concise and efficient, we are incorporating by reference background information that was published on these six species in the proposed rule, 75 FR 606, published January 5, 2010. Species descriptions, taxonomy, and habitat and life history may be found in the proposed rule, unless we are making technical corrections or incorporating new information. In this final rule, we included new information on recent location data for the royal cinclodes. We also updated the population estimates, range, and conservation status on the other species.

We also changed the format of this final rule to make it more readable, particularly in light of the Plain Writing Act of 2010 (Executive Order 13563). We organized it first by species descriptions for all six species, and then by the evaluation of factors affecting the species. We organized the threats evaluation for these six species (also known as the five-factor analysis, see Section 4(a)(1) of the Act), primarily by three habitat types and locations for efficiency. Three species occur in

Polylepis

forest, two species occur at Lake Junín, and the Peruvian plantcutter is evaluated on its own due to its unique habitat requirements and distribution. Because each habitat experiences similar threats, for each threat factor, we identified and evaluated those factors that affect these species within the particular habitat and that are common to all of the species within that habitat. For example, the degradation of habitat and habitat loss are threats to all six species. We also identified and evaluated threats that may be unique to certain species, but that may not apply to all of the species addressed in this final rule. For example, the Peruvian plantcutter is the only species addressed in this rule that is found in the northwestern coast of Peru, and we have addressed threats that are unique to that species specifically. Lastly, we included range maps for each species to better identify their ranges to the public.

Summary of Comments and Recommendations

In the proposed rule that published on January 5, 2010 (75 FR 606), we requested that all interested parties submit information that might contribute to the development of a final rule. We also contacted appropriate scientific experts and organizations and invited them to comment on the proposed listings.

We received three comments on the proposed rule from the public. One comment from the public expressed support for the proposed listings but provided no substantive information. One commenter requested that we take climate change into account when evaluating threats to these species. Although the science of climate change is still uncertain with respect to how it will affect the long-term viability of species and the ecosystems upon which they depend, the Service did consider effects of climate change to these species in this final rule.

The other comment received from the public was also non-substantive—the commenter asked why these species should be listed under the Act if they are not native to the United States. The Act provides for the listing of any species that qualifies as an endangered or threatened species, regardless of its native range. Protections under the Act apply to species not native to the United States and include restrictions on importation into the United States; sale or offer for sale in foreign commerce; and delivery, receipt, carrying, transport, or shipment in foreign commerce and in the course of a commercial activity. Listing also serves to heighten awareness of the importance of conserving these species among foreign governments, conservation organizations, and the public.

Peer Review

In accordance with our policy published on July 1, 1994 (59 FR 34270), we solicited expert opinions from six knowledgeable individuals with scientific expertise that included familiarity with one or more of these six species, the geographic region in which the species occur, and conservation biology principles. We received responses from four peer reviewers. The peer reviewers generally agreed that the description of the biology and habitat for each species was accurate and was based on the best available information. New location data were provided for the royal cinclodes, and we incorporated the information into the rule. Supporting data and information such as the species' biology, ecology, life history, population estimates, threat factors, and current conservation efforts were provided and also incorporated into this rule. In response to a comment from a peer reviewer who thought that the proposed rule was difficult to read, we have tried to reorganize our evaluation and finding in a clearer manner in this final rule.

Species Information

Below is a description of each species. The species are described in alphabetical order, beginning with the ash-breasted tit-tyrant, followed by the Junín grebe, Junín rail, Peruvian plantcutter, royal cinclodes, and the white-browed tit-spinetail.

I. Ash-breasted tit-tyrant

(Anairetes alpinus)

Species Description

The ash-breasted tit-tyrant, locally known as “torito pechicenizo,” is a small New World tyrant flycatcher in the Tyrannidae family that is native to high-altitude woodlands of the Bolivian and Peruvian Andes (BirdLife International (BLI) 2000, p. 392; Collar

et al.

1992, p. 753; del Hoyo

et al.

2004, pp. 170, 281; Fjeldså and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1; Supreme Decree No. 034-2004-AG 2004, p. 276854). The sexes are similar, with adults approximately 13 centimeters (cm) (5 inches (in)) in length, with dark gray, inconspicuously black-streaked upperparts (BLI 2009o, p. 1; del Hoyo

et al.

2004, p. 281). The two subspecies (see Taxonomy) are distinguished by their underbelly color, which is yellowish-white in the nominate subspecies and white in the other (BLI 2009o, p. 1). Juvenile plumage is duller in appearance, but is otherwise similar to the adult coloration (del Hoyo

et al.

2004, p. 281).

Taxonomy

When the species was first taxonomically described by Carriker (1933, pp. 27-29), it was placed in its own genus,

Yanacea

. It was not until the 1960s that

Yanacea

was merged into

Anairetes

(a genus long-known as

Spizitornis)

by Meyer de Schauensee (1966, p. 376). Some contemporary researchers have suggested retaining the species within

Yanacea

(Fjeldså and Krabbe 1990, p. 468). Smith (1971, pp. 269, 275) and Roy

et al.

(1999, p. 74) confirmed that the ash-breasted tit tyrant is a valid species based on its phylogenetic placement and degree of genetic divergence from other species of

Anairetes,

and recent texts continue to place it in

Anairetes

(e.g., del Hoyo

et al.

2004, p. 281). Therefore, we accept

the species as

Anairetes alpinus,

which follows the Integrated Taxonomic Information System (ITIS 2009, p. 1). Two subspecies are recognized, including,

A. alpinus alpinus

(the nominate subspecies) and

A. alpinus bolivianus

. These subspecies occur in two widely separated areas (see Current Range) (ITIS 2009, p. 1; del Hoyo

et al.

2004, p. 281) and are distinguished by the color of their underbellies (see Taxonomy) (BLI 2009o, p. 1).

Habitat and Life History

Density of foliage rather than size of tree seems to be an important factor for this species (Fjeldså 2010 pers. comm.). This species forages in the terminal branches and outer foliage, usually in the treetops but also at ground level at the edges of dense forest patches. In areas where all trees have been cut, it forages in the dense regrowth near ground level. In general, these patches are found in a zone of persistent cloudiness, in places with difficult accessibility and few people (Fjeldså 2010 pers. comm.).

In west-central Peru, the species occurs in the Cordilleras (mountains in Spanish) Central and Occidental (in the Peruvian Administrative Regions of Ancash, Huánuco, La Libertad, and Lima) (BLI 2009, p. 1; del Hoyo

et al.

2004, p. 281). Until 1992, the taxon in this locality was highly localized and known only in Ancash Region (Collar

et al.

1992, p. 753). The species was subsequently reported in other regions between 2003 and 2007, such as Lima, Huánuco, and Libertad (BLI 2009i, p. 1; BLI 2007, pp. 1, 5; del Hoyo

et al.

2004, p. 281). There is little remaining

Polylepis

habitat in its elevational zone in the humid east Andean slope of Puno, so there may be a large distribution gap there today (Purcell and Brelsford 2004, p. 155).

The ash-breasted tit-tyrant is restricted to remnant patches of semihumid

Polylepis

or Polylepis-Gynoxys woodlands of Peru and Bolivia (See

http://www.birdlife.org/datazone/speciesfactsheet.php?id=4173

for a range map of the species), where the species is found at elevations between 3,700 and 4,600 meters (m) (12,139 and 15,092 feet (ft)) above sea level. It is found in severely fragmented and local populations in remote valleys in the Andes (Benham

et al.

2011, p. 145; Association Armonia 2011, p. 1; InfoNatura 2007, p. 1; del Hoyo

et al.

2004, pp. 170, 281; Collar

et al.

1992, p. 753; Fjeldså and Krabbe 1990, pp. 468-469). The genus

Polylepis

(locally referred to as “queuña”) (Aucca and Ramsay 2005, p. 1), in the Rosaceae family, comprises approximately 20 species of evergreen bushes and trees (Kessler and Schmidt-Lebuhn 2006, pp. 1-2; De la Via 2004, p. 10; Kessler 1998, p. 1), 19 of which occur in Peru (Chutas

et al.

2008, p. 3). In Bolivia, the ash-breasted tit-tyrant is associated only with

P. pepei

forests, but the bird is found among a greater variety of

Polylepis

species in Peru (Chutas

et al.

2008, p. 16; I. Gómez, in litt. 2007, p. 1). The average

Polylepis

species are 3-10 m (10-33 ft) tall, but may grow to a height of 36 m (118 ft) (Purcell

et al.

2004, p. 455).

P. pepei

is considered vulnerable by IUCN and is described as rare. The genus

Gynoxys

includes several species of flowering shrubs. The ash-breasted tit-tyrant is known to exist in disjunct areas: West-central Peru and in suitable habitat stretching from southern Peru into northern Bolivia (Benham

et al.

2011, pp. 145-157; del Hoyo

et al.

2004, p. 281).

Polylepis

woodlands occur as dense forests, as open-canopied stands with more arid understories, or as shrubland with scattered trees (De la Via 2004, pp. 10-11; Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113; Lloyd and Marsden in press, as cited in Lloyd 2008, p. 532). Ash-breasted tit-tyrants prefer dense

Polylepis

forests (Fjeldså 2002a, p. 114; Smith 1971, p. 269), which often include a mixture of

Gynoxys

trees (no common name), in the Asteraceae family (International Plant Names Index (IPNI) 2009, p. 1; De la Via 2004, pp. 10). Dense

Polylepis

woodlands are characterized by moss- or vine-laden vegetation, with a shaded understory and a rich diversity of insects, making good feeding grounds for insectivorous birds (De la Via 2004, p. 10), such as the ash-breasted tit-tyrant (BLI 2009o, p. 1; Lloyd 2008, p. 535).

There is little information about the ecology and breeding behavior of the ash-breasted tit-tyrant. The species' territory ranges from 1-2 hectares (ha) (2.5-5 acres (ac)) (BLI 2009o, p. 1). The breeding season appears to occur during late dry season (Collar

et al.

1992, p. 754)—November and December (BLI 2009o, p. 1). Juveniles have been observed in March and July (del Hoyo

et al.

2004, p. 281; Collar

et al.

1992, p. 754). Although species-specific information is not available, tit-tyrant nests are generally finely woven, open cups, built in a bush (Fjeldså and Krabbe 1990, p. 468).

The ash-breasted tit-tyrant forages alone, in family groups, and sometimes in mixed-species flocks. The bird takes short flights, either hovering or perching to consume invertebrates near the tops and outer edges of

Polylepis

shrubs and trees (BLI 2009o, p. 1; Lloyd 2008, p. 535; del Hoyo

et al.

2004, p. 281; Engblom

et al.

2002, p. 58; Fjeldså and Krabbe 1990, p. 468). In winter, when invertebrate populations diminish, tit-tyrants may also forage on seeds (Fjeldså and Krabbe 1990, p. 468).

Historical Range and Distribution

The ash-breasted tit-tyrant may once have been well-distributed throughout previously dense and contiguous

Polylepis

high-Andes woodlands of Peru and Bolivia. Researchers believe that these woodlands were historically contiguous with lower-elevation cloud forests and widespread above 3,000 m (9,843 ft) (Fjeldså 2002a, pp. 111-112, 115; Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; Collar

et al.

1992, p. 753). Researchers consider the reduction in

Polylepis

forest habitat to be the result of historical human activities, including burning and grazing, which have prevented regeneration of the woodlands and resulted in the fragmented habitat distribution seen today (Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; Fjeldså and Kessler 1996, Kessler 1995a, Kessler 1995b, and Lægaard 1992, as cited in Fjeldså 2002a, p. 112; Kessler and Herzog 1998, pp. 50-51). Modeling studies by Fjeldså (2002a, p. 116) indicate that this habitat reduction was accompanied by a loss in species richness. It is estimated that only 2-3 and 10 percent of the original forest cover still remain in Peru and Bolivia, respectively (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113). Of this amount, only 1 percent of the remaining

Polylepis

woodlands are found in humid areas, where denser stands occur (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113) and which are preferred by the ash-breasted tit-tyrant (BLI 2009o, p. 1; Lloyd 2008, p. 535; Fjeldså 2002a, p. 114; Smith 1971, p. 269) (see Factor A).

Current Range and Distribution

The current range of the ash-breasted tit-tyrant is estimated to be 11,900 square kilometers (km

2

)) (4,595 square miles (mi

2

) (BirdLife International [BLI] 2011a, p. 1; see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=4173

for a range map). However, BLI (2000, pp. 22, 27) defines a species' range as the extent of occurrence or the area contained within the shortest continuous imaginary boundary that can be drawn to encompass all the known, inferred, or projected sites of present occurrence of a species, excluding cases of vagrancy. Given that the species is known to occur in disjunct locations, this range estimate includes a large area of habitat in which the species is not known to occur, and its actual occupied

habitat is much smaller than its range (Jetz

et al.

2008, p. 2).

Population Estimates

The species has experienced a population decline of between 10 and 19 percent in the past 10 years, and this rate of decline is predicted to continue (BLI 2009o, pp. 1, 4). The population is considered to be declining in close association with continued habitat loss and degradation (see Factor A) (BLI 2009o, p. 5; BLI 2007, pp. 1, 4). Population information is presented first on a global population estimate, and then at the range country level. The range country estimates will begin with Peru, where the majority of the population resides.

Global population estimate. BLI, a global organization that consults with and assimilates information from bird species experts, categorizes the ash-breasted tit-tyrant as having a population size between 250 and 999 individuals, with an estimated actual population size to be in the mid- to upper-hundreds (BLI 2009o, p. 1; BLI 2007, p. 1). Combining the estimated number of ash-breasted tit-tyrants in Peru and Bolivia, the total population consists of possibly 780 individuals (Benham

et al.

2011, p. 155; Aucca-Chutas 2007, pp. 4, 8; Gómez

in litt.

2007, p. 1), consistent with the BLI category of between 250-999 individuals.

Peru. Peruvian population estimates are incomplete, with no estimates for the ash-breasted tit-tyrants in Arequipa, Huánuco, La Libertad, or Lima (BLI 2009g, p. 1; del Hoyo

et al.

2004, p. 281). Aucca-Chutas (2007, p. 8) surveyed five disjunct

Polylepis

forest patches in Peru and estimated that a total of 461 ash-breasted tit-tyrants were located in these areas. This included 30 birds in Corredor Conchucos (Ancash Region); 181 and 33 birds in Cordilleras Vilcanota and Vilcabamba, respectively (Cusco Region); 22 birds in Cordillera de Carabaya (Puno Region); and 195 birds in a study site called Cordillera del Apurímac (Apurímac Region) (Aucca-Chutas 2007, pp. 4, 8), referring to an area within the Runtacocha highlands. Other research in the Runtacocha highlands has indicated that the ash-breasted tit-tyrant is relatively common there (BLI 2009o, p. 1), with an estimated 100 pairs of birds found in approximately 40 forest patches (Fjeldså

in litt.

1990, as cited in Collar

et al.

1992, p. 753). Small numbers of birds are reported in La Libertad Region (del Hoyo

et al.

2004, p. 281).

Bolivia. Although BLI reports an estimated population size of 150-300 ash-breasted tit-tyrants in Bolivia (Gómez

in litt.,

2003 and 2007, as cited in BLI 2009o, p. 1), recent surveys indicate that the population is smaller. Over a 6-year period, Gómez (

in litt.

2007, p. 1) conducted intensive searches throughout 80 percent of the suitable habitat in Bolivia in the Cordillera Real and the Cordillera Apolobamba (La Paz Department), to detect the presence of the ash-breasted tit-tyrant. From this work, researchers inferred or observed the presence of 2-10 individuals in each of four forest patches, and estimated that approximately 180 ash-breasted tit-tyrants occur in Bolivia.

Within La Paz, there may be two separate populations separated by the Mapiri canyon (see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=4173

). The population in the Runtacocha highland in Apurímac, Peru, is morphologically distinct from that in Cusco, although a formal subspecies description has not been published (Fjeldså 2010 pers. comm.). Research on Bolivian localities indicates that gene flow has occurred between some subpopulations, but not all (Gómez 2005, p. 86). In Bolivia, the birds are distributed in 2 metapopulations, with at least 5 subpopulations in one location and 14 subpopulations in the other (Gómez 2005, p. 86). Research in 2011 documented this species traveling distances greater than 30 m (98 ft) between patches (Benham

et al.

2011, p. 153). A “patch” is considered to be any contiguous area of forest separated from other fragments by 30 m (98 ft) or more (Lloyd 2008, p. 166); and patch sizes are categorized generally as follows: small is less than 4 hectares (ha) (9.9 acres [ac]), medium is between 4 and 12 ha (29.6 ac), and large is greater than 12 ha (Benham

et al.

2011, p. 148; Lloyd 2008, p. 166). Ash-breasted tit-tyrants occupy territories of 1-2 ha (2.5-5 ac) (BLI 2009o, p. 1).

Because the ash-breasted tit-tyrant may exist as two subspecies (BLI 2009o, p. 5; ITIS 2009, p. 1), it is reasonable to conclude that there may be little or no gene flow between the population that is in Bolivia and the population that is in Peru. However, there is insufficient information at this time to determine the extent of gene flow. All populations of this species essentially face the same threats, are all generally in the same region and habitat type, and all have quite small populations. Absent peer-reviewed information to the contrary and based on the best available information, we recognize all populations of ash-breasted tit-tyrants as a single species. For the purpose of this rule, the ash-breasted tit-tyrant includes all subspecies, if they are later identified as such.

Conservation Status

The ash-breasted tit-tyrant is considered endangered by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276,855). This Decree prohibits hunting, take, transport, and trade of protected species, except as permitted by regulation. Peru follows the IUCN RedList classification for its species. The IUCN considers the ash-breasted tit-tyrant to be endangered because it has a very small population that is undergoing continued decline in the number of mature individuals, is confined to a habitat that is severely fragmented, and is also undergoing a continuing decline in extent, area, and quality of habitat (BLI 2009o, p. 4; IUCN 2001, pp. 8-12). The ash-breasted tit-tyrant occurs within the following Peruvian protected areas: Parque Nacional Huascarán, in Ancash, and Santuario Histórico Machu Picchu, in Cusco, and Zona Reservada de la Cordillera Huayhuash, spanning Ancash, Huánuco, and Lima (BLI 2009i, p. 1; BLI 2009l, p. 1; BLI 2009n, p. 1; Aucca-Chutas

et al.

2008, p. 16). In La Paz Department, Bolivia, the species is found in Parque Nacional y Área Natural de Manejo Integrado Madidi, Parque Nacional y Área Natural de Manejo Integrado Cotapata, and the colocated protected areas of Reserva Nacional de Fauna de Apolobamba, Área Natural de Manejo Integrado de Apolobamba, and Reserva de la Biosfera de Apolobamba (BLI 2009i, p. 1; Aucca-Chutas

et al.

2008, p. 16; Auza and Hennessey 2005, p. 81).

II. Junín Grebe

(Podiceps taczanowskii)

Species Description

The Junín grebe is a highly social, flight-impaired water bird in the

Podicipedidae

family that is endemic to a single location (Lake Junín) in Peru. It was observed being in the air 5-10 meters (16-33 ft) during the crossing of a mud bank (Fjeldså 2010, pers. comm.). Its underparts are white with a strong silky gloss rather than mottled (Fjeldså 2010, pers. comm.). Common names for the species in English are: Junín flightless grebe, puna grebe, and Taczanowski's grebe. This species is also known by two Spanish names: “zampullín del Junín” or “zambullidor de Junín” (del Hoyo

et al.

1992, p. 195; Fjeldså 2004, p. 199; Instituto Nacional de Recursos Naturales (INRENA) 1996, p. 3; Ramsen

et al.

2007, p. 18; Supreme Decree 034-2004-AG 2004, p. 276854).

A slim, long-necked bird, the Junín grebe is about 35 cm (13.78 in) in length, and its weight ranges from 0.30 to 0.47 kilograms (0.66 to 1.04 pounds) (BLI 2009b, p. 1; UNEP-WCMC 2009, p. 1). The Junín grebe has a pointed head, with dark feathers on its back, a white throat, and mottled, dusky-colored underparts. This grebe is distinguished by its slender gray bill, red iris, and dull yellow-orange colored feet. Immature birds are darker gray on the flanks than mature birds (BLI 2009b, p. 1).

Taxonomy

The Junín grebe was taxonomically described by Berlepsch and Stolzmann in 1894 (ITIS 2009, p. 1). It is one of nine species of grebes in the genus

Podiceps

worldwide (Dickinson 2003, p. 80). The species' taxonomic status as

Podiceps taczanowskii

is valid (ITIS 2009, p. 1).

Habitat and Life History

The typical feeding habitat of this species consists of shallow water in Lake Junín with calcareous sediments and extensive carpets of chalk-encrusted algae known as

Chara

(brittlewort or stonewort), which is its principal feeding substrate (O'Donnel and Fjeldså 1997, p. 30). Lake Junín

Chara,

is an aquatic plant genus (Denike and Geiger undated, p. 18). Over the last 20 years, the extent of

Chara

vegetation has decreased in Lake Junín (Tueros

in litt;

in Fjeldså pers. comm. 2010, pp. 2-3.) As a result, the feeding habitat for the grebe has also changed dramatically. The disappearance of

Chara

(specifically

Chara fragilis;

ParksWatch 2006, p. 8) may be linked with zinc pollution. Higher zinc concentration levels are detrimental to green algae (Fjeldså pers. comm. 2010, pp. 2-3). The concentrations of heavy metals are reported to be within legal limits for humans; however, copper and zinc concentrations may be limiting factors for the Chara vegetation. Local reports indicate that vegetation, particularly sedges within the

Schoenoplectus

genus family (this species' nesting habitat), has disappeared completely in recent years, likely due to low water levels and grazing cattle in the marshes and wetlands (Fjeldså pers. comm. 2010).

The Junín grebe is endemic to the open waters and marshlands of Lake Junín, located at 4,080 m (13,390 ft) above sea level in the Peruvian Administrative Region of Junín (BLI 2009b, p. 1). The 147-km

2

(57-mi

2

) lake, also known as “Chinchaycocha” or “Lago de Junín,” is large but fairly shallow (ParksWatch 2009, p. 1; Tello 2007, p. 1). Situated within “puna” habitat, the climate is seasonal and can be “bitterly cold” in the dry season (Fjeldså 1981, p. 240). Local vegetation is characterized by tall dense grasslands and scrubland with open, rocky areas, all interspersed with wetlands and woodlands (BLI 2003, p. 1; ParksWatch 2009, pp. 1, 4). The dominant terrestrial plant species surrounding the lake includes 43 species of grass

(Poaceae

family), 15 species of asters

(Asteraceae

family), and 10 species of legumes

(Fabaceae

family) (ParksWatch 2009, p. 1). Aquatic vegetation includes Andean water milfoil

(Myriophyllum quitense),

several species of pondweed (including

Elodea potamogeton, Potamogeton ferrugineus,

and

P. filliformis),

and bladderwort

(Utricularia

spp.). Floating plants, such as duckweed

(Lemna

species (spp.)), large duckweed

(Spiodela

spp.), and water fern

(Azolla filiculoides),

also occur on the lake (ParksWatch 2009, p. 2). The Lake is surrounded by extensive marshland along the lake shore (BLI 2009a, p. 1; BLI 2009b, p. 1) that extends into the lake up to 1-3 mi (2-5 km) from shore (O'Donnel and Fjeldså 1997, p. 29). The marshes are dominated by two robust species of cattails, giant bulrush

(Schoenoplectus californicus

var.

Totara)

and totorilla

(Juncus articus

var.

Andicola)

(Fjeldså 1981, pp. 244, 246). Both cattail species can reach nearly 2 m (6.6 ft) in height. These plant communities, or “tortoras,” grow so densely that stands are often impenetrable (ParksWatch 2009, p. 1). In shallow water, during low lake levels, tortora communities can become partially or completely dry (ParksWatch 2009, p. 2).

Lake Junín supports one of the richest and most diverse arrays of bird species of all Peruvian high Andean wetlands (ParksWatch 2009, p. 3). These bird species include migratory birds, birds that nest at high altitudes, aquatic birds, and local endemic species such as the Junín grebe, the Junín rail

(Laterallus tuerosi;

also the subject of this final rule), the giant coot (

Fulica ardesiaca

), and the Chilean flamingo

(Phoenicopterus chilensis)

(BLI 2009a, pp. 2-3; ParksWatch 2009, p. 3; Tello 2007, p. 2). Mammals are relatively scarce in the area, although there are some predators (ParksWatch 2009, p. 4) (see Factor C).

Breeding season for this species occurs annually from November to March (O'Donnell and Fjeldså 1997, p. 29; Fjeldså 1981, pp. 44, 246). The Junín grebe nests in the protective cover of the marshlands during the breeding season (Tello 2007, p. 3; Fjeldså 1981, p. 247), particularly in stands of giant bulrush (ParksWatch 2009, p. 4). Under natural conditions, winter rains increase the lake water level during the breeding season, allowing the grebes to venture into local bays and canals, although they are never found nesting on the lake's shore (Tello 2007, p. 3). The species nests in the giant bulrush marshlands (ParksWatch 2009, p. 4). Well-hidden floating nests can contain up to three eggs, with an average of two eggs, laid during November and December (Fjeldså 1981, p. 245). The species is believed to have a deferred sexual maturation (Fjeldså 2004, p. 201) and exhibits low breeding potential, perhaps as a reflection to adaptation to a “highly predictable, stable environment” (del Hoyo

et al.

1992, p. 195), laying one clutch during the breeding season (ParksWatch 2009, p. 4). Junín grebes occasionally produce a replacement clutch if their original nest is disturbed (Fjeldså 2004, pp. 199, 201). After the eggs hatch, the male grebe cares for the chicks, and does not leave the nest to feed. The female grebe is responsible for feeding the male and chicks until the chicks can leave the nest (Tello 2007, p. 3). The Junín grebe is likely a long-lived species (Fjeldså 2004, p. 201), and its breeding success and population size are highly influenced by the climate (BLI 2009b, p. 2; BLI 2008, pp. 1, 3-4; Fjeldså 2004, p. 200; Hirshfeld 2007, p. 107; Elton 2000, p. 3) (see Factor A).

The Junín grebe feeds in the open waters of the lake and around the marsh edges, moving into the open waters of the lake to feed where it is easier to dive for food during the winter (Tello 2007, p. 3; Fjeldså 1981, pp. 247-248). Fish (primarily pupfish

(Orestias

spp.)) account for over 90 percent of the grebe's diet (Fjeldså 1981, pp. 251-252). Pupfish become scarce when the marshlands dry during periods of reduced water levels, and the Junín grebe is then known to vary its diet with midges (Order

Diptera),

corixid bugs

(Trichocorixa reticulata),

amphipods

(Hyalella simplex),

and shore fly maggots and pupa

(Ephydriid

spp.).

Historical Range and Distribution

The Junín grebe was historically known to be endemic to Lake Junín, in the Peruvian Administrative Region of Junín (Fjeldså 2004, p. 200; Fjeldså and Krabbe 1990, p. 70; INRENA 1996, p. 1; Fjeldså 1981, p. 238). Experts believe that the species was previously distributed throughout the entire 57-mi

2

(147-km

2

) lake (BLI 2009a, p. 1; BLI 2003, p. 1; Fjeldså 1981, p. 254; Gill and Storer in Fjeldså 2004, p. 200). In 1938, the Junín grebe was encountered throughout the entire lake (Morrison 1939, p. 645). The Junín grebe is now

absent from the northwestern portion of Lake Junín due to mine waste contamination (Gill and Storer, pers. comm. As cited in Fjeldså 2004, p. 200; Fjeldså 1981, p. 254).

Current Range and Distribution

The Junín grebe is endemic to Lake Junín, located at 4,080 m (13,390 ft) above sea level in the Peruvian high Andes (see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=3644

for a range map of the species; BLI 2009a, p. 1; BLI 2009b, p. 1). Although BLI (2009b, p. 1) reports the current estimated range of the species as 143 km

2

(55 mi

2

), BLI's definition of a species' range is the total area within its extent of occurrence, noting that Lake Junín is only a 147-km

2

(57-mi

2

) lake (BLI 2009a, p. 1) and that the Junín grebe is restricted to the southern portion of the lake (Gill and Storer, pers. comm. As cited in Fjeldså 2004, p. 200; Fjeldså 1981a, p. 254), its current range is actually smaller than the figure reported by BLI. The entire population of this species is located only within a protected area, the Junín National Reserve (BLI 2009a, p. 1; BLI 2009b, p. 1; ParksWatch 2009, p. 4).

Population Estimate

The current population of the Junín grebe is estimated to be 100-300 individuals (BLI 2009b, p. 3), having undergone a severe population decline in the latter half of the 20th century, with extreme population fluctuations during this time (Fjeldså 1981, p. 254). Field studies in 1938 indicated that the Junín grebe was extremely abundant throughout Lake Junín (Morrison 1939, p. 645). Between 1961 and 1979, the population fell from more than 1,000 individuals to an estimated 250-300 birds (BLI 2009b, p. 2; Collar

et al.

1992, p. 43; Harris 1981, as cited in O'Donnell and Fjeldså 1997, p. 30; Fjeldså 1981, p. 254). Surveys during the mid-1980s estimated a total of 250 individuals inhabiting the southern portion of Lake Junín (BLI 2009b, p. 2; Collar

et al.

1992, p. 43). In 1992, only 100 birds were observed, and by 1993, the population had declined to 50 birds, of which fewer than half were breeding adults (BLI 2008, p. 3; BLI 2009b, p. 2). In 1995, an estimated 205 Junín grebes were present on Lake Junín (O'Donnell and Fjeldså 1997, p. 30). Breeding and fledging were apparently unsuccessful from 1995 to 1997. However, there were two successful broods fledged during the 1997 and 1998 breeding seasons (BLI 2008, p. 3; Valqui

in litt.,

as cited in BLI 2009b, p. 2). In 1998, more than 250 Junín grebes were counted in a 4-km

2

(1.5-mi

2

) area in the southern portion of Lake Junín, suggesting a total population of 350 to 400 birds (Valqui

in litt.,

as cited in BLI 2009b, p. 2). In 2001, field surveys indicated that there may have been a total population of 300 birds, but that estimate has been considered optimistic (Fjeldså

in litt.

2003, as cited in BLI 2009b, p. 2). Fjeldså (

in litt.

2003, as cited in BLI 2009b, p. 2) postulated that perhaps only half that number would have been mature individuals.

The species has experienced a population decline of 14 percent in the past 10 years, and the population is expected to continue to decline (BLI 2009b, pp. 1, 6-7). The species' decline is associated with continued habitat loss and degradation (Gill and Storer, pers

.

comm. as cited in Fjeldså 2004, p. 200; Fjeldså 1981, p. 254). These population fluctuations are strongly linked to precipitation (see Factor A).

Conservation Status

The Junín grebe is considered critically endangered by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, pp. 276, 853). The IUCN categorizes the Junín grebe as critically endangered because it is endemic to one location and has undergone significant population declines, such that an extremely small number of adults remain (BLI 2009b, pp. 1, 3). The single known population of the Junín grebe occurs wholly within one protected area in Peru, the Junín National Reserve (BLI 2009b, pp. 1-2).

III. Junín rail

(Laterallus tuerosi)

Species Description

The Junín rail is a secretive bird of the

Rallidae

family that is endemic to a single lake (Lake Junín) in Peru. The species is also referred to as the Junín black rail (Fjeldså 1983, p. 281) and is locally known as “gallinetita de Junín” (Supreme Decree 034-2004-AG 2004, p. 27684). This rail measures 12-13 cm (4.7-5.1 in) in length, and has a dark slate-colored head, throat, and underparts. Its belly and vent (anal aperture) are black. The characteristic feature of this rail is the heavily barred (black and white) entire upperparts of the body, including its wings and flanks (Fjeldså 2010 pers comm.). The under-tail coverts (feathers on the underside of the base of the tail) are buff in color, with a dull rufous-brown back. The remaining underparts are dark brown and boldly barred in white, and the legs are greenish-yellow (BLI 2009b, p. 1).

Taxonomy

This species was discovered by Fjeldså in 1977 and described in 1983 (BLI 2011; Fjeldså 2010 pers. comm.). BirdLife International considers this rail a full species based on morphological features (BLI 2009b; p. 1). The closely related black rail,

Laterallus jamaicensis

occurs at much lower elevations (i.e., 0 to 1,350 m (0 to 4,429 ft) above sea level) (BLI 2007, p. 1; BLI 2000, p. 170; Collar

et al.

1992, p. 190). Based on the morphological differences and the species' distinct and disjunct ranges, we consider the Junín rail to be a discrete species and recognize it as

L. tuerosi.

It should be noted that it appears that only 2 specimens of the Junín rail have ever been collected (near Ondores) (Fjeldså 1983, pp. 278-279) and that all expert accounts of this species rely solely on that collection and a subsequent observation of the species in Pari (Fjeldså in litt., 1992, as cited in Collar

et al.

1992, p. 190).

Habitat and Life History

The Junín rail occurs in the dense, interior marshlands of Lake Junín where rushes

(Juncus

spp.) predominate or in more open mosaics of rushes, mosses (division Bryophyta), and low herbs (Fjeldså 1983, p. 281). Lake Junín is located in the seasonally climatic “puna” habitat, with a variety of species of grasses, asters, and trees of the bean family forming tall, dense grasslands and open scrubland, interspersed with wetlands and woodlands (ParksWatch 2009, pp. 1, 4; ParksWatch 2006, p. 2). Giant bulrushes and totorilla dominate the extensive marshlands surrounding the lake (BLI 2009b, p. 1; ParksWatch 2009, p. 1; Fjeldså 1983, p. 281). In shallow water, during low lake levels, “tortora” communities can become partially or completely dry (ParksWatch 2009, p. 2). The lake supports a wide variety of bird species and aquatic vegetation (BLI 2009a, pp. 2-3; ParksWatch 2009, p. 3; Tello 2007, p. 2; BLI 2003, p. 1).

There is little information regarding the ecology of the Junín rail. The species appears to be completely dependent on the wide marshlands located around the southeastern shoreline of the lake for nesting, foraging, and year-round residence (BLI 2009b, p. 2; Collar

et al.

1992, p. 190; Fjeldså 1983, p. 281) (see also Current Range and Distribution). Information received during the comment period on the proposed rule indicates that the species inhabits mosaic vegetation with dense

Juncus

(rush) beds (often areas where the vegetation is broken down) and open waterlogged areas with short but

densely matted vegetation of mosses and

Lilaeopsis

(grassworts) rather than the drier bunchgrass hills (puna habitat). The habitat provides a complex mosaic of niches that leads to the patchy distribution of many bird species throughout the region, indicating that this species has specialized habitat requirements that are only satisfied locally (Fjeldså and Krabbe 1990, p. 32). The species' distribution is highly localized around the lake. The Junín rail apparently prefers the dense, interior marshlands comprised primarily of rushes and mosaics of rushes, mosses (division Bryophyta), and low herbs in more open marsh areas (Fjeldså 1983, p. 281). High habitat specificity is consistent with related rail species. The water depth, emergent vegetation used for cover, and access to upland vegetation are all important factors in the rail's habitat use (Flores and Eddleman 1995, p. 362). Similar to all rails, the Junín rail is furtive and remains well-hidden in the marshes surrounding the lake (BLI 2009b, p. 2). The Junín rail reportedly nests at the end of the dry season, in September and October. Nests are built on the ground within dense vegetative cover, and the species' clutch size is two eggs (BLI 2009b, p. 2; Collar

et al.

1992, p. 190). The diet of the Junín rail has not been studied specifically, but other black rail species feed primarily on small aquatic and terrestrial invertebrates and seeds (Eddleman

et al.

1994, p. 1).

Historical Range and Distribution

The Junín rail is endemic to Lake Junín (BLI 2009b, p. 2; Fjeldså 1983, p. 278). The species may have been historically common in the rush-dominated marshlands surrounding the entire lake (Fjeldså 1983, p. 281). In addition to the species' specific habitat preferences (see Current Range and Distribution), it is believed that the Junín rail is now restricted to the marshes at the southwestern corner of the lake due to the high level of water contamination that flows into the northwestern margins of the lake via the San Juan River (Martin and McNee 1999, p. 662).

Current Range and Distribution

The Junín rail is restricted to the southwestern shore of Lake Junín (Lago de Junín), in the Andean highlands of central Peru (see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=2842

for a range map of the species). It is currently known from only two localities (near the towns of Ondores and Pari) (Fjeldså 2010 pers. comm.; BLI 2009b, p. 2; Collar

et al.

1992, p. 190; Fjeldså 1983, p. 281). However, based on habitat needs, it may occur in other portions of the approximately 150 km

2

(57.9 mi

2

) of marshland surrounding the lake, discussed in more detail below.

The range of the species is estimated to be 160 km

2

(62 mi

2

) (BLI 2011b, p. 1). However, this is likely an overestimate of the species' actual range for several reasons. First, BLI's definition of a species' range results in an overestimate of the actual range. Second, the species' range was calculated based on the availability of presumed suitable habitat for the Junín rail. It has long been assumed that the rail potentially occupies the entire marshland area surrounding Lake Junín (Fjeldså 1983, p. 281). The two localities mentioned, Ondores and Pari, are villages at the lake shore. Information received during the comment period on the proposed rule indicates that there is continuous rail habitat in the outer part of the marshes outside these villages, 1-2 km (0.6-1.2 mi) outside the firm ground (Fjeldså 2010 pers. comm.). The rail has been documented along this 6-7 km (3.7-4.3 mi) section; the area of suitable habitat here is about 10 km

2

(3.9 mi

2

). East and north of the lake, there is similar habitat, approximately 25 km

2

(9.6 mi

2

) combined (Fjeldså 2010 pers. comm.). However, the Junín rail's actual range is very likely smaller than the approximated range reported by BLI since 2000 (BLI 2009b, p. 1; BLI 2008, p. 3; BLI 2007, p. 1; BLI 2000, p. 170).

Population Estimates

The species has experienced a population decline of between 10 and 19 percent in the past 10 years (BLI 2009b, p. 2). However, rigorous population estimates have not been conducted (Fjeldså 1983, p. 281), and the species' elusiveness makes it difficult to locate (BLI 2009b, p. 2). The population is considered to be declining in close association with continued habitat loss and degradation (see Factor A) (BLI 2008, p. 1). Local fishermen have reported serious declines in some years, and several individual birds have been found dead (Fjeldså 2010 pers. comm.). In 1983, the Junín rail was characterized as possibly common, based on local fishermens' sightings of groups of up to a dozen birds at a time (Fjeldså 1983, p. 281). The species continues to be reported as fairly common (BLI 2009b, p. 1; BLI 2007, p. 1). BLI estimates that this species' population size falls within the population range category of 1,000-2,499 (BLI 2009b, p. 1; BLI 2007, p. 1; BLI 2000, p. 170). This estimate is an extrapolation that continues to be based on the assumption that the species may be fairly common in the entire circa 150 km

2

(58 mi

2

) of available marshland around Lake Junín (BLI 2009b, p. 1; BLI 2007, p. 1). The species has never been confirmed outside its two known localities and, therefore, it is possible that the species is locally common, but not widely distributed. If the Junín rail is not common throughout Lake Junín's marshland, the actual population size may be much lower.

Conservation Status

The Junín rail is considered endangered by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276855). The IUCN categorizes the Junín rail as endangered because it is known only from a small area of marshland around a single lake, where the habitat quality is declining (BLI 2008, p. 3). The single known population of the Junín rail occurs wholly within one protected area in Peru, the Junín National Reserve (BLI 2009b, pp. 1-2; BLI 2008, p. 1).

IV. Peruvian Plantcutter

(Phytotoma raimondii)

Species Description

The Peruvian plantcutter, locally known as “cortarrama Peruana,” is a small finch-like bird endemic to the dry forests of coastal northwest Peru (Schulenberg

et al.

2007, p. 488; Walther 2004, p. 73; Ridgely and Tudor 1994, p. 733; Collar

et al.

1992, p. 805; Goodall 1965, p. 636; Sibley and Monroe 1990, p. 371). The Peruvian plantcutter is an herbivore with a predominantly leaf-eating diet (Schulenberg

et al.

2007, p. 488; Walther 2004, p. 73; Bucher

et al.

2003, p. 211).

Plantcutters have bright yellow eyes, short wings and rather long tails, and their crown feathers form a slight crest (Ridgely and Tudor 1994, p. 732; Goodall 1965, p. 635). Adult birds are 18.5 to 9 cm (7.28 to 7.48 in) in length and weigh approximately 36 to 44 grams (g) (1.26 to 1.55 ounces (oz)) (Schulenberg

et al.

2007, p. 488; Walther 2004, p. 73). Males are pale ashy gray, except a broad cinnamon-rufous color band on the belly and above the bill, and white colored bands on their wings (BLI 2009a, p. 1; Goodall 1965, p. 636; Ridgely and Tudor 1994, p. 733). Females are buff-brown with broad, dark brown stripes above, and white with heavy black-striped underparts (BLI 2009a, p. 1; Collar

et al.

1992, p. 805). Juvenile birds have not been described (Walther 2004, p. 73). The Peruvian plantcutter's bill is stout, short, conical, and finely serrated with

sharp tooth-like projections that run the length of the beak on both sides, and which are well suited for plucking buds, leaves, shoots, and fruits (Schulenberg

et al.

2007, p. 488; Ridgely and Tudor 1994, p. 732; Goodall 1965, p. 635) (see Habitat and Life History).

Taxonomy

The Peruvian plantcutter was first taxonomically described as

Phytotoma raimondii

by Taczanowski in 1883 (ITIS 2009, p. 1; Sibley and Monroe 1990, p. 371). The type-specimen of the Peruvian plantcutter (the specimen that was described by Taczanowski) was collected by the ornithologist Konstanty Jelski, who recorded the specimen as being collected in the Tumbes Department of Peru (Flanagan

et al.

in litt. 2009, p. 2). However, the reported collection location may have been inaccurate (see Historical range and Distribution, below).

The genus

Phytotoma

contains three species of plantcutters, all endemic to South America (Walther 2004, p. 73; Dickinson 2003, p. 346; Sibley and Monroe 1990, p. 371; Goodall 1965, p. 635). Ornithologists have long debated to which family this genus belongs. Some ornithologists have recommended that the genus be placed in its own family, Phytotomidae (Lanyon and Lanyon 1989, p. 422), while others placed the genus within the Tyrannidae family (Sibley and Monroe 1990, p. 371). Molecular research using DNA sequencing supports the inclusion of

Phytotoma

in the Cotingidae family (Ohlson

et al.

2006, p. 10;

et al.

2002, p. 993; Irestedt

et al.

2001, p. 23; Johansson). Therefore, based on the information currently available to us, we accept that the Peruvian plantcutter belongs to the Cotingidae family, which follows the Integrated Taxonomic Information System (ITIS 2009, p. 1).

Habitat and Life History

The Peruvian plantcutter is reportedly selective in its habitat preference and requires a variety of arid tree and shrub species with dense low-hanging branches close to the ground (Flanagan

et al.

in litt. 2009, p. 7; Williams 2005, p. 2; Flanagan and More 2003, p. 5; Collar

et al.

1992, p. 805). The primary habitat for the Peruvian plantcutter is seasonally dry tropical forest, which is also referred to as equatorial dry tropical forest, and occurs in the semiarid lowlands of northwestern Peru (Schulenberg

et al.

2007, p. 21; Linares-Palomino 2006, pp. 260, 263-266; Walther 2004, p. 73). The Peruvian plantcutter also uses arid lowland scrub (dense and open) and dense riparian shrub communities (BLI 2009a. p. 2; Schulenberg

et al.

2007, pp. 21, 488; Walther 2004, p. 73; Stotz

et al.

1996, p. 19; Collar

et al.

1992, p. 805). The Peruvian plantcutter is a key indicator species for Equatorial Pacific Coast arid lowland scrub (Stotz

et al.

(1996, pp. 19, 428). The lowland dry tropical forest and scrub are characterized as small and heavily fragmented patches of plant species adapted to the arid conditions of the prolonged dry season of northwestern Peru (Bridgewater

et al.

2003, pp. 132, 140; Best and Kessler 1995, p. 40; Ridgely and Tudor 1994, p. 734).

The lowland dry forest in northwestern Peru is open-canopied, with trees occurring in scattered clumps or individually (Flanagan and More 2003, p. 4). The dominant tree species of the lowland dry forest is

Prosopis pallida

(common name “kiawe;” also locally referred to as “algarrobo”) in the Fabaceae family (legume family) (Lopez

et al.

2005, p. 542; More 2002, p. 39).

Prosopis pallida

is a wide-spreading tree or large shrub, 8-20 m (26-65 ft) tall, with dense branches; spines can be present or absent (Pasiecznik

et al.

2001, p. 36). This deep-rooted drought-tolerant species, related to mesquite species of the southwestern United States and Mexico, provides an important ecological function by improving and stabilizing soil conditions (Pasiecznik

et al.

2001, pp. 101-102; Brewbaker 1987, p. 1). Typical of legumes,

P. pallida

is able to “fix” atmospheric nitrogen for plant utilization and growth (Pasiecznik

et al.

2001, p. 3; Brewbaker 1987, p. 1).

Three of the most common tree species associated with

P. pallida

dry forest habitat used by the Peruvian plantcutter are

Capparis scabrida

(locally known as “sapote”), in the Capparaceae (caper) family, and

Acacia macracantha

(long-spine acacia, locally known as “faique”) and

Parkinsonia aculeata

(Jerusalem thorn, locally known as “palo verde”), both in the Fabaceae family (More 2002, pp. 17-23). Associated flowering shrubs in dry forest habitat include

Capparis avicennifolia

(locally known as “bichayo”) and

C. crotonoides

(locally known as “guayabito de gentil”), both in the Capparaceae (caper) family;

Cordia lutea

(locally known as “overall”) in the Boraginaceae (borage) family; and

Maytenus octogona

(locally known as “realengo”) in the Celastraceae (bittersweet) family. Other commonly occurring dry forest vegetation includes vines (e.g., Convolvulaceae (morning-glory) and Cucurbitaceae (gourd) families),

Psittacanthus chanduyensis

(tropical mistletoe; locally known as “suelda con suelda”) in the Loranthaceae (mistletoe) family, scattered herbaceous species (e.g., Asteraceae (sunflower), Scrophulariaceae (figwort), and Solanaceae (nightshade) families), and grasses (e.g., Poaceae (grass) family) (Elton 2004, p. 2; Walther 2004, p. 73; More 2002, pp. 14-17; Ferreyera 1983, pp. 248-250). Riparian vegetation includes dense shrub and small trees of

P. pallida, A. macracantha, Capparis

spp., and

Salix

spp. (willow spp.) (Lanyon 1975, p. 443).

The arid climate of northwestern Peru is due to the influence of the cold Humboldt Current that flows north, parallel to the Peruvian Coast (UNEP 2006, p. 16; Linares-Palomino 2006, p. 260; Rodriguez

et al.

2005, p. 2). The Humboldt Current has a cooling influence on the climate of coastal Peru, as the marine air is cooled by the cold current and, thus, is not conducive to generating rain. To the east, the Andean Mountains prevent humid air from the Amazon from reaching the western lowlands (Linares-Palomino 2006, p. 260; Lanyon 1975, p. 443).

Coastal northwestern Peru experiences a short rainy season during the summer months (January-April) (Linares-Palomino 2006, p. 260), which can also include precipitation in the form of mist or fine drizzle along the coast (Lanyon 1975, p. 443). The mean annual precipitation across the range of the Peruvian plantcutter is 5.0 to 99 mm (0.196 to 3.80 in) (hyper-arid to arid) (Galan de Mera

et al.

1997, p. 351). The climate is warm and dry with the annual temperature range of 23 to 25 °C (74 to 77 °F) at elevations below 600 m (1,968 ft) (Linares-Palomino 2006, p. 260). Northwestern Peru is strongly influenced by the El Niño Southern Oscillation (ENSO) cycle (Rodriguez

et al.

2005, p. 1), which can have particularly profound and long-lasting effects on arid terrestrial ecosystems (Mooers

et al.

2007, p. 2; Holmgren

et al.

2006a, p. 87) (see Factor A).

Knowledge of the breeding of most species within the Cotingidae family, including the Peruvian plantcutter, is not well known (Walther 2004, p. 73). The Peruvian plantcutter is considered a resident species in Peru, which indicates that it breeds there (Snow 2004, p. 61; Walther 2004, p. 73). Nesting activity of plantcutters appears to occur from March to April (Walther 2004, p. 73; Collar

et al.

1992, p. 805). Plantcutters build shallow, cup-shaped nests that are made of thin dry twigs and lined with root fibers and other softer material (Snow 2004, p. 55). Nests can be built 1 to 3 m (3.3 to 9.8 ft) above the ground inside a thick thorny shrub

or higher in the fork of a tree (Elton 2004, p. 2; Snow 2004, p. 55; Flanagan and More 2003, p. 3). Females lay two to four eggs, and the incubation period lasts about 2 weeks (Snow 2004, p. 56; Walther 2004, p. 73; Goodall 1965, p. 636). Males assist in rearing the chicks, which fledge after 17 days or so (Snow 2004, p. 56).

Plantcutters are herbivores with a predominantly leaf-eating diet (Snow 2004, p. 46; Bucher

et al.

2003, p. 211). As an herbivore, the Peruvian plantcutter is dependent on year-round availability of high-quality food, particularly during the dry season when plant growth is very limited (Bucher

et al.

2003, p. 216). Peruvian plantcutters eat buds, leaves, and shoots of

P. pallida

and various other trees and shrubs, as well as some fruits (e.g., mistletoe) (Schulenberg

et al.

2007, p. 488; Walther 2004, p. 73; Goodall 1965, p. 635). The seeds, green seed pods, leaves, and flowers of

P. pallida

provide a protein-rich food source for animals (Lewis

et al.

2006, p. 282). The Peruvian plantcutter appears to prefer to feed while perched in shrubs and trees, although individuals also have been observed foraging on the ground (Snow 2004, p. 50). Birds have been observed in pairs and small groups (Schulenberg

et al.

2007, p. 488; Walther 2004, p. 73; Flanagan and More 2003, p. 3; Collar

et al.

1992, p. 804).

Historical Range and Distribution

The Peruvian plantcutter is a restricted-range species that is confined to the mostly flat, narrow desert zone, which is less than 50 km (31 mi) in width (Lanyon 1975, p. 443) and runs along the coast of northwestern Peru (Ridgely and Tudor 1994, p. 734; Stattersfield

et al.

1998, p. 213; Walther 2004, p. 73). The historical range of the Peruvian plantcutter reportedly extended from the town of Tumbes, located in the extreme northwestern corner of Peru and approximately south to north of Lima within the Regions of Tumbes, Piura, Lambayeque, La Libertad, Ancash, and Lima (Collar

et al.

1992, pp. 804-805).

The historical distribution of the Peruvian plantcutter was most likely throughout the contiguous lowland

P. pallida

dry forest and riparian vegetation, below 550 m (1,804 ft) (Williams 2005, p. 1; Collar

et al.

1992). According to Collar

et al.

(1992, pp. 804-805), the Peruvian plantcutter is known from 14 historical sites.

The type-specimen of the Peruvian plantcutter was most likely collected south of the town of Tumbes (Flanagan

et al.

in litt. 2009, pp. 2, 15). It is unknown whether the type specimen was lost or destroyed, or if it was ever returned to Peru (Flanagan

et al.

in litt. 2009, p. 2). Today, there is good indication that the type-specimen was mislabeled as being collected in Tumbes (Flanagan

et al.

in litt. 2009, p. 2). Although the Tumbes Region has been extensively surveyed for the Peruvian plantcutter, including the North-West Biosphere Reserve, there have never been other collections in or near the vicinity of Tumbes or other evidence to suggest that the Peruvian plantcutter ever occurred in the area (Flanagan

et al.

in litt. 2009, p. 2). Thus, it appears that the Peruvian plantcutter never occurred in the Tumbes Region.

Researchers consider the reduction in dry forest habitat to be the result of historical human activities, including extensive land clearing for agriculture, timber and firewood extraction, charcoal production, and overgrazing. These activities have led to the reduction and severe fragmentation of dry forest habitat today (Flanagan

et al.

in litt. 2009, pp. 1-9; Schulenberg

et al.

2007, p. 488; Lopez

et al.

2006, p. 898; Bridgewater

et al.

2003, p. 132; Pasiecznik

et al.

2001, pp. 10, 75, 78, 95; Stotz

et al.

1998, p. 52; Lanyon 1975, p. 443; Ridgely and Tudor 1994, p. 734) (see Factor A).

Current Range and Distribution

The current range of the Peruvian plantcutter is approximately 4,900 km

2

(1,892 mi

2

) (BLI 2009a, p. 1), at an elevation of between 10 and 550 m (33 and 1,804 ft) above sea level. It occurs within the Peruvian regions of Piura, Lambayeque, Cajamarca, La Libertad, and Ancash (from north to south) (Flanagan

et al. in litt.

2009, pp. 14-15). This species occurs within two protected areas in Peru (see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=4474

for a range map of the species). It has been documented in the

Prosopis pallida

(a legume known as huarango, bayahonda, or carob) dry forest within the protected archeological sites of the Pómac Forest Historical Sanctuary (BLI 2009e, p. 1) and Murales Forest (Walther 2004, p. 73). The species' reported range is likely an overestimate (Jetz

et al.

2008, p. 2). BLI defines a species' range as the total area within its extent of occurrence; however, the Peruvian plantcutter's current distribution is severely fragmented and distributed among

small, widely separated remnant patches of

P. pallida

dominated dry forest (Flanagan

et al.

2009, pp. 1-9; BLI 2009a, pp. 2-3; Ridgely and Tudor 1994, p. 18), which are usually heavily disturbed fragments of forest (Bridgewater

et al.

2003, p. 132). Therefore, the species' actual range is likely smaller than this figure.

The Peruvian plantcutter is extirpated from 11 of its 14 historical sites due to loss of habitat or degradation of habitat (Elton 2004, p. 1; Hinze 2004, p. 1; Flanagan and More 2003, p. 5). Depending on habitat quality, it is estimated that the Peruvian plantcutter requires approximately 1 ha (2.5 ac) of habitat for suitable food and nesting sites (Flanagan

et al. in litt.

2009, p. 7; Flanagan and More 2003, p. 3). Although the Peruvian plantcutter has been found in patches of

P. pallida

dry forest habitat that are near agricultural lands, tracks or roads, and human settlement (Flanagan

et al. in litt.

2009, pp. 2-7), much of the available

P. pallida

dry forest habitat is not occupied by the Peruvian plantcutter (Schulenberg

et al.

2007, p. 488; Snow 2004, p. 69; Walther 2004, p. 73; BLI 2000, p. 401).

Flanagan

et al.

(

in litt.

2009, pp. 1-15) recently completed a comprehensive review of 53 locations where there have been documented sightings of the Peruvian plantcutter. Of these, the species was determined to be extant (still living) in 29 sites. In the Piura Region, 17 of the 22 documented sites of the Peruvian plantcutter were extant as of a 2009 report (Flanagan

et al. in litt.

2009, pp. 2-4, 14). In this particular region, the Talara Province contained the largest concentration of intact

P. pallida

dry forest habitat in northwestern Peru and the largest subpopulation of the Peruvian plantcutter (Flanagan

et al. in litt.

2009, p. 3; BLI 2009a, p. 2; Walther 2004, p. 73; Flanagan and More 2003, p. 5). Additionally, there are several other documented sites of the Peruvian plantcutter in the Piura Region (e.g., Manglares de San Pedro, Illescas Peninsula, and Cerro Illescas) (Flanagan

et al. in litt.

2009, pp. 4, 14; BLI 2009c, p. 1).

In the Lambayeque Region, Flanagan

et al.

(

in litt.

2009, pp. 4-5, 14) reported a total of 13 locations of the Peruvian plantcutter, of which 5 are considered extant. Within the Region, there are four important areas for the Peruvian plantcutter:

(1) The Pómac Forest Historical Sanctuary (Santuario Histórico de Bosque de Pómac), designated as a protected archeological site in 2001, comprises 5,887 ha (14,547 ac) of

P. pallida

dry forest (Flanagan

et al. in litt.

2009, p. 4; BLI 2009e, p. 1). The Sanctuary includes the archeological site Batan Grande, an area comprised of 500 ha (1,235 ac) of

P. pallida

dry forest (Flanagan

et al. in litt.

2009, p. 4; BLI 2009e, p. 1).

(2) Near the small town of Rafan are remnant patches of

P. pallida

dry forest,

encompassing approximately 1,500 ha (3,706 ac) (BLI 2009f, p. 1). The Rafan area has become a popular birding site for the Peruvian plantcutter (BLI 2009f, p. 1; Engblom 1998, p. 1).

(3) Murales Forest (Bosque de Murales), comprised of

P. pallida

dry forest, is a designated archeological reserved zone (BLI 2009a, p. 3; Stattersfield

et al.

2000, p. 402).

(4) Chaparri Ecological Reserve, comprised of 34,412 ha (85,033 ac) with

P. pallida

dry forest, is a community-owned and managed protected area (Walther 2004, p. 73).

The remaining sites in the Lambayeque Region are small remnant patches of

P. pallida

dry forest and comprise a few acres (Flanagan

et al. in litt.

2009, pp. 4-5; Walther 2004, p. 73). The protected areas are further discussed under Factors A and D.

In the Cajamarca Region, Flanagan

et al.

(

in litt.

2009, pp. 5, 14) reported one occupied site of the Peruvian plantcutter, consisting of approximately 6 ha (14.8 ac) of remnant

P. pallida

dry forest in the Río Chicama Valley. Six of the 12 known sites of the Peruvian plantcutter in the La Libertad Region are considered extant (Flanagan

et al. in litt.

2009, pp. 5-6, 14). Each of these sites consists of small patches of remnant

P. pallida

dry forest habitat (Flanagan

et al. in litt.

2009, pp. 5-6; Walther 2004, p. 73). Of the three known sites of the Peruvian plantcutter in the Ancash Region, only one was reported to be extant as of 2009 (Flanagan

et al. in litt.

2009, pp. 6, 14). Additionally, in the Lima Region, the authors reported that the two historical sites were also unoccupied in the most recent survey (Flanagan

et al. in litt.

2009, pp. 7, 15).

This species was found recently in central coastal Peru, in the area of Huarmey, Áncash (Rosina y Mónica 2010, p. 257). Additional surveys are needed to determine if other available

P. pallida

dry forest habitat is occupied by the Peruvian plantcutter (Flanagan

et al. in litt.

2009, p. 7).

Population Estimates

There have been no rigorous quantitative assessments of the Peruvian plantcutter's population size (Williams 2005, p. 1). The estimated extant population size is between 500 and 1,000 individuals and comprises 2 disjunct subpopulations (BLI 2009g, pp. 1-2; Walther 2004, p. 73) and several smaller sites (Flanagan

et al. in litt.

2009, pp. 2-7; Williams 2005, p. 1; Walther 2004, p. 73; Flanagan and More 2003, pp. 5-9).

The northern subpopulation, located in the Talara Province in Piura Region, reportedly has between 400 and 600 individuals, or approximately 60 to 80 percent of the total population of the Peruvian plantcutter (BLI 2009a, p. 2; Williams 2005, p. 1; Snow 2004, p. 69; Walther 2004, p. 73). The second subpopulation, located at Pómac Forest Historical Sanctuary (Lambayeque Region), reportedly has 20 to 60 individuals (BLI 2009a, p. 2; BLI 2009e, p. 1; Walther 2004, p. 73). The smaller sites are estimated to consist of a few individuals up to 40 individuals (Flanagan

et al. in litt.

2009, pp. 2-7; Walther 2004, p. 73; Williams 2005, p. 1; Flanagan and More 2003, pp. 5-9).

The population estimate for the Peruvian plantcutter—that is, the total number of mature individuals—is not the same as the effective population size (i.e., the number of individuals that actually contribute to the next generation). The subpopulation structure and the extent of interbreeding among the occurrences of the Peruvian plantcutter are unknown. Although the two large subpopulations and many of the smaller occurrences of the Peruvian plantcutter are widely separated (BLI 2009a, pp. 2-3; Flanagan

et al. in litt.

2009, pp. 1-9; Ridgely and Tudor 1994. p. 18), there is insufficient information to determine whether these occurrences function as genetically isolated subpopulations.

The Peruvian plantcutter has experienced a population decline of between 1 and 9 percent in the past 10 years, and this rate of decline is predicted to continue (BLI 2009g, p. 1). The population is considered to be declining in close association with continued habitat loss and degradation of habitat (see Factor A) (BLI 2009a, pp. 1-3; BLI 2009g, pp. 1-3; Snow 2004, p. 69; Ridgely and Tudor 1994, p. 18).

Conservation Status

The Peruvian plantcutter is considered endangered by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276855). The IUCN considers the Peruvian plantcutter to be endangered because of ongoing habitat destruction and degradation of its small and severely fragmented range (BLI 2009a, pp. 2-3; BLI 2009g, pp. 1-2). From 1996 to 2000, the IUCN considered the Peruvian plantcutter to be critically endangered (BLI 2009g, p. 1), following changes to the IUCN listing criteria in 2001. Experts have suggested returning the species to its previous classification of critically endangered, due to the numerous and immediate threats to the species (Flanagan,

in litt.

2009 p. 1; Snow 2004, p. 69; Walther 2004, p. 74).

V. Royal cinclodes

(Cinclodes aricomae)

Species Description

The royal cinclodes, also known as “churrete real” and “remolinera real,” is a large-billed ovenbird in the Furnaridae family that is native to high-altitude woodlands of the Bolivian and Peruvian Andes (BLI 2009i, pp. 1-2; InfoNatura 2007, p. 1; del Hoyo

et al.

2003, p. 253; Supreme Decree No. 034-2004-AG 2004, p. 27685; Valqui 2000, p. 104). The adult is nearly 20 cm (8 in) in length, with a darker crown and a buff-colored area above the eyes. Its underparts are mostly gray-brown; it has only limited whitish mottling (this and the more distinctive rufous-brown wingbar are the main differences from the closely related species, the stout-billed

Cinclodes (C. excelsior);

Fjeldså 2010 pers. comm.). The throat is buff-colored, and the remaining underparts are gray-brown to buff-white. The wings are dark with prominent edging that forms a distinctive wing-bar in flight. The large, dark bill is slightly curved at the tip (BLI 2009i, p. 1).

Taxonomy

When the species was first taxonomically described, the royal cinclodes was placed in the genus

Upucerthia

(Carriker 1932, pp. 1-2) and was then transferred to

Geositta

as a subspecies

(Geositta excelsior aricomae)

(Vaurie 1980, p. 14). Later, it was transferred to the genus

Cinclodes,

where it was considered a race or subspecies of the stout-billed

Cinclodes (Cinclodes excelsior)

until recently (BLI 2009i, p. 1; Fjeldså and Krabbe 1990, pp. 337-338; Vaurie 1980, p. 15). The royal cinclodes is now considered a distinct species

(C. aricomae)

based on differences in its habitat, morphology, and genetic distance (Chesser 2004, p. 763; del Hoyo

et al.

2003, p. 253). Therefore, we accept the species as

Cinclodes aricomae,

which also follows ITIS (2009, p. 1).

Habitat and Life History

In the Cordillera Vilcanota, southern Peru, the royal cinclodes shows distinctive preferences for areas with primary (lesser disturbed) woodland habitat quality in larger remnant woodland patches: Specifically tall, dense

Polylepis

vegetation cover, high density of large

Polylepis

trees, and areas with dense and extensive moss ground cover (Lloyd 2008b. pp. 735-745).

Near Lampa, Junín Department, the royal cinclodes has recently been observed in

Gynoxys

dominated woodlands where no

Polylepis

species occur (Lloyd 2010, pers. comm.). These findings suggest that in some areas, the

royal cinclodes may not be dependent on

Polylepis

species, but can occur in other high-elevational woodland habitats with similar habitat structure and habitat quality to

Polylepis

(Lloyd 2010, pers. comm.; Witt and Lane 2009, pp. 90-94).

In the Cordillera Vilcanota, the royal cinclodes has a very narrow estimated niche breadth, and it is largely intolerant of the surrounding disturbed non-woodland puna matrix habitat (Lloyd and Marsden 2008, pp. 2645-2660). Individuals here have been observed foraging on the ground or on boulders, concentrating foraging efforts on moss or bark litter substrates (Lloyd 2008). The royal cinclodes is restricted to elevations between 3,500 and 4,600 m (11,483 and 12,092 ft) (BLI 2009i, p. 2; del Hoyo

et al.

2003, p. 253; BLI 2000, p. 345; Collar

et al.

1992, p. 588). The characteristics of

Polylepis

habitat were described above as part of the Habitat and Life History of the ash-breasted tit-tyrant. The royal cinclodes prefers dense woodlands (BLI 2009i, p. 2; del Hoyo

et al.

2003, p. 253; BLI 2000, p. 345; Collar

et al.

1992, p. 588), with more closed canopies that provide habitat for more lush moss growth (Engblom

et al.

2002, p. 57). The moss-laden vegetation and shaded understory harbor a rich diversity of insects, making good feeding grounds for insectivorous birds (De la Via 2004, p. 10) such as the royal cinclodes (del Hoyo

et al.

2003, p. 253; Engblom

et al.

2002, p. 57). In Bolivia, the royal cinclodes has been observed only in

P. pepei

forests, but it is found amongst a greater variety of

Polylepis

species in Peru (Chutas

et al.

2008, p. 16; I. Gómez, in litt. 2007, p. 1).

Information on the ecology and breeding behavior of royal cinclodes is limited. The species' feeding territory ranges from 3 to 4 ha (7 to 10 ac) (del Hoyo

et al.

2003, p. 253; Engblom

et al.

2002, p. 57). Breeding pairs may occupy smaller, 2-ha (2.5-ac) territories (Chutas 2007, p. 7). The royal cinclodes is described as “nervous” and is easily disturbed by humans (Engblom

et al.

2002, p. 57). The breeding season probably begins in December, but territorialism among pairs can be seen in austral winter (June-August) (del Hoyo

et al.

2003, p. 253; BLI 2000, p. 345).

Cinclodes

species construct burrows or use natural cavities, crevices, or rodent burrows for nesting (Fjeldså and Krabbe 1990, p. 337; Vaurie 1980, pp. 30, 34). The royal cinclodes' clutch size may be similar to that of the closely related stout-billed

Cinclodes (C. excelsior),

which is two eggs per clutch (Graves and Arango (1988, p. 252).

The royal cinclodes appears to mainly feed on beetle larvae, grubs, and earthworms, which they find by turning and tossing away moss and debris on the forest floor with their powerful bills (Fjeldså 2010 pers. comm.). It has also been observed to consume invertebrates, seeds, and occasionally small vertebrates (frogs) (del Hoyo

et al.

2003, p. 253). The royal cinclodes forages, solitary or in pairs, by probing through moss and debris on the forest floor (del Hoyo

et al.

2003, p. 253; Fjeldså 2002b, p. 9; BLI 2000, p. 345; Collar

et al.

1992, p. 589). Their feeding is done so violently that the forest floor looks as if pigs have been feeding there. Due to its feeding behavior, the moss cover rapidly dries up and dies unless the humidity is very high. This characteristic limits the species to areas where the landscape is persistently covered by clouds and mists, or where the canopy is dense enough to provide permanent shade (Fjeldså 2010 pers. comm.). Because this species can heavily disturb its habitat, it requires large feeding territories (thus, only large forest patches can sustain more than one pair). This ground-feeding strategy may facilitate interbreeding amongst groups located on adjoining mountain peaks when the species likely descends the mountains during periods of snow cover (Engblom

et al.

2002, p. 57).

Historical Range and Distribution

The royal cinclodes may once have been locally common and distributed across most of central to southern Peru and into the Bolivian highlands, in once-contiguous expanses of

Polylepis

forests above 3,000 m (9,843 ft) (BLI 2009i, p. 1; Fjeldså 2002a, pp. 111-112, 115; Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; BLI 2000, p. 345).

Polylepis

woodlands are now restricted to elevations of 3,500 to 5,000 m (11,483 to 16,404 ft) (Fjeldså 1992, p. 10). As discussed above for the Historical Range and Distribution of the ash-breasted tit-tyrant, researchers consider human activity to be the primary cause for historical habitat decline and resultant decrease in species richness (Fjeldså 2002a, p. 116; Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; Fjeldså and Kessler 1996, Kessler 1995a, b, and Lægaard 1992, as cited in Fjeldså 2002a, p. 112; Kessler and Herzog 1998, pp. 50-51). The royal cinclodes may have been extirpated from its type locality (Aricoma Pass, Puno), and possibly throughout the entire Puno Region, where

Polylepis

forest no longer exists (Collar

et al.

1992, p. 589; Engblom

et al.

2002, p. 57) (see Population Estimates). It is estimated that between 2-3 and 10 percent of the original forest cover still remains in Peru and Bolivia, respectively (BLI 2009i, p. 1; Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113) (see Factor A). Of this amount, less than 1 percent of the remaining woodlands occur in humid areas, where

Polylepis

denser stands occur (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113) and which are preferred by the royal cinclodes (del Hoyo

et al.

2003, p. 253; Engblom

et al.

2002, p. 57). The royal cinclodes was initially discovered in Bolivia in 1876, but was not observed there again until recently (BLI 2009i, p. 2; Hirshfeld 2007, p. 198) (see Current Range and Distribution).

Current Range and Distribution

The royal cinclodes is generally restricted to moist and mossy habitat on steep rocky slopes of semihumid

Polylepis

or

Polylepis-Gynoxys

woodlands, where the species is found at elevations between 3,500 and 4,600 m (11,483 and 12,092 ft) (Benham

et al.

2011, p. 151; BLI 2009i, p. 2; del Hoyo

et al.

2003, p. 253; Collar

et al.

1992, p. 588). The current potential range of the species is approximately 2,700 km

2

(1,042 mi

2

) (BLI 2009i, p. 1), which is an overestimate of the actual range, given the fragmented nature of the species' remaining habitat (BLI 20091, p. 1; Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113). The royal cinclodes was rediscovered in Bolivia within the last decade, after more than 100 years of not being observed there (Mobley 2010

in litt.;

Hirshfeld 2007, p. 198). It occurs in the Andes of southeastern Peru (Cusco, Apurímac, Puno and Junín) and adjacent Bolivia (La Paz) (Gomez 2010, p. 1; see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=9773

for a range map of the species).

Within the last 15 years, royal cinclodes has been observed in Peru's Runtacocha highlands and in the Laguna Anantay Valley (both in Apurímac), Pariahuanca Valley (Junín), and Cordillera Vilcanota (Cusco), and in Bolivia, Department of La Paz: Cordillera Apolobamba and the Cordillera Real (including Ilampu Valley, Sanja Pampa, and Cordillera de La Paz) (Benham

et al.

2011, p. 151; Hirshfeld 2007, p. 198; del Hoyo

et al.

2003, p. 253; Engblom

et al.

2002, p. 57; Valqui 2000, p. 104). It was also recently discovered in central Peru, approximately 5 km (3.1 mi) from Lampa, Junín Department, at 3700 m (12,139 ft). This represents a 300 km (186 mi) northward range extension for the species (Witt and Lane 2009, pp. 90-94).

Population Estimate

Population information is presented first by range country and then in terms of a global population estimate. The range country estimates begin with Peru, where the majority of the population resides. The royal cinclodes is believed to be a naturally low-density species (Lloyd 2008, pp. 164-180).

Peru. In the Puno Region of Peru, it is unclear whether a viable population of royal cinclodes remains. The royal cinclodes was first observed in Puno in 1930 (Fjeldså and Krabbe 1990, p. 338) and has continued to be reported there (BLI 2009i, pp. 1-2; BLI 2007, pp. 1-2; del Hoyo 2003, p. 253; Collar

et al.

1992, p. 588). However, based on habitat availability, InfoNatura (2007, p. 1) predicted that the royal cinclodes does not occur in Puno because suitable habitat no longer exists there. Only two royal cinclodes individuals have been reported in the Puno Region (Cordillera de Carabaya) in recent decades (Aucca-Chutas 2007, pp. 4, 8).

Bolivia. The species' current range is more widespread in Bolivia than previously understood. The royal cinclodes had not been observed in Bolivia for more than a century, when it was rediscovered there in 1997 (BLI 2009i, p. 2; Hirshfeld 2007, p. 198). Recent surveys in La Paz Department found it in at least 13 localities (8 in Cordillera Apolobamba and 5 in Cordillera La Paz) (BLI 2009i, p. 1).

BLI reports an estimated population size of 50-70 royal cinclodes in Bolivia (Gómez

in litt.

2003, 2008, as cited in BLI 2009i, p. 2). Studies in Bolivia reported in 2007 found a density of 1-8 royal cinclodes in each of 30 forest patches (Gómez

in litt.

2007, p. 1). Thus, they estimated that the royal cinclodes population in Bolivia is approximately 30 birds. Researchers added that, because the royal cinclodes does not always respond to tape-playbacks, these numbers may underestimate the actual population size (Gómez

in litt.

2007, p. 1).

Global Population Estimate

In 1990, the global population of the royal cinclodes was estimated to be 100-150 individuals (Fjeldså and Krabbe 1990, p. 338). This number represented only the estimated Peruvian population because the royal cinclodes was thought to exist only in Peru at the time of this estimate (BLI 2009i, p. 2; Hirshfeld 2007, p. 198). In 2007, Aucca-Chutas (2007, p. 8) reported an estimated 189 birds located within four separate

Polylepis

forest patches in Peru, with a combined area of 629 ha (1,554 ac). This estimate included 116 birds and 30 birds in Cordilleras Vilcanota and Vilcabamba, respectively (Cusco); 2 birds in Cordillera de Carabaya (Puno); and 41 birds in Cordillera del Apurímac (Runtacocha highlands in Apurímac) (Aucca-Chutas 2007, pp. 4, 8). Subpopulations at the four locations in the Cordillera Vilcanota may contain as few as 1-4 individuals (BLI 2008, p. 2).

In 2002, Engblom

et al.

(p. 57) estimated a total population size of up to 250 pairs of birds. In 2003, the global population was once again reported to include only a few hundred individuals (del Hoyo

et al.

2003, p. 253). Based on recent observations in both countries, there are likely approximately 270 birds in Peru and 50-70 in Bolivia, totaling 239-340 individuals (this includes the 2011 observations in Laguna Anantay, Apurímac Department (Benham

et al.

2011). While the BLI estimate of the population is between 50 and 249 individuals (BLI 2011d), recent research has found new habitat and birds in newly identified locations (Benham

et al.

2011, pp. 145-157).

Population estimates are incomplete, and the population structure and the extent of interbreeding among the various localities are unknown. The species' territory ranges from 3 to 4 ha (7 to 10 ac), and its habitat is fragmented, dispersed, and sparse (del Hoyo

et al.

2003, p. 253; Engblom

et al.

2002, p. 57). Fjeldså (2010, pers. comm.) indicated that because of the range disjunction, the species may not be breeding as a single population. In the proposed rule, we indicated that there was no information to indicate the distance that this species is capable of or likely to travel between localities. However, research in 2011 found that this species was making flights greater than 100 m (328 ft) between

Polylepis

patches in Apurímac, and was also observed at forest edges (Benham

et al.

2011, pp. 152).

Engblom

et al.

(2002, p. 57) noted that gene flow between localities likely occurs when the species descends the mountains to forage in the valleys during periods of snow cover at the higher altitudes such that interbreeding may occur at least among localities with shared valleys. Although the information available suggests that the species does not breed as a single population, we have insufficient information to determine if they are genetically isolated. The species has experienced a population decline of approximately 30 and 49 percent in the past 10 years, and this rate of decline is predicted to continue (BLI 2009i, pp. 1, 5). The population is considered to be declining in close association with continued habitat loss and degradation (BLI 2009i, p. 6).

Conservation Status

The royal cinclodes is considered critically endangered by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276854). The IUCN considers the royal cinclodes to be critically endangered due to its extremely small population, which consists of small subpopulations that are severely fragmented and dependent upon a rapidly deteriorating habitat (BLI 2009i, p. 1; BLI 2007, p. 1). The royal cinclodes occurs within the Peruvian protected area of Santuario Histórico Machu Picchu, in Cusco (BLI 2009h, p. 1; BLI 2009i, p. 6; Aucca-Chutas

et al.

2008, p. 16). In La Paz Department, Bolivia, the species is found in Parque Nacional y Área Natural de Manejo Integrado Madidi, Parque Nacional y Área Natural de Manejo Integrado Cotapata, and the colocated protected areas of Reserva Nacional de Fauna de Apolobamba, Área Natural de Manejo Integrado de Apolobamba, and Reserva de la Biosfera de Apolobamba (BLI 2009a, p. 1; BLI 2009b, p. 1; Aucca-Chutas et al. 2008, p. 16). At Abra Málaga Thastayoc, Cordillera Vilcanota, Peru, a new visitor's center was completed in the Royal Cinclodes Private Conservation Area in February 2011 (ECOAN 2012).

VI. White-browed tit-spinetail

(Leptasthenura xenothorax)

Species Description

The white-browed tit-spinetail, or “tijeral cejiblanco,” is a small dark ovenbird in the Furnaridaii family that is native to high-altitude woodlands of the Peruvian Andes (del Hoyo

et al.

2003, pp. 266-267; BLI 2000, p. 347; Fjeldså and Krabbe 1990, p. 348; Parker and O'Neill 1980, p. 169; Chapman 1921, pp. 8-9). The sexes are similar in size (approximately 18 cm (7 in) in length). The most distinct feature of this species is its checkered (black-and-white) throat and dark grey body underparts, which distinguishes it from the rusty-crowned tit-spinetail

(Leptasthenura pileata)

(Fjeldså 2010 pers. comm., p. 4). The species is characterized by its bright rufous crown and prominent white supercilium (eyebrow) (Lloyd 2009, p. 2; del Hoyo

et al.

2003, p. 267), which gives the species its name. The species is highly vocal, “often singing while acrobatically foraging from the outermost branches of

Polylepis

trees” (Lloyd 2009, p. 2).

Taxonomy

The white-browed tit-spinetail was first described by Chapman in 1921 (del Hoyo

et al.

2003, p. 267). The species was synonymized with the nominate subspecies of the rusty-crowned tit-spinetail

(Leptasthenura pileata pileata)

by Vaurie (1980, p. 66), but examination of additional specimens in combination with field observations strongly suggests that

L. xenothorax

is a valid species (Collar

et al.

1992, p. 596; Fjeldså and Krabbe 1990, p. 348; Parker and O'Neill 1980, p. 169). Therefore, we accept the species as

Leptasthenura xenothorax,

which follows the Integrated Taxonomic Information System (ITIS 2009, p. 1).

Habitat and Life History

The white-browed tit-spinetail is restricted to high-elevation, semihumid

Polylepis

and

Polylepis-Gynoxys

woodlands, where the species is found between 3,700 and 4,550 m (12,139 and 14,928 ft) above sea level (Lloyd 2009, pp. 5-6; del Hoyo

et al.

2003, p. 267; BLI 2000, p. 347; Collar

et al.

1992, p. 595; Fjeldså and Krabbe 1990, p. 348). Dense stands of

Polylepis

woodlands are characterized by moss-laden vegetation and a shaded understory, and provide for a rich diversity of insects, making these areas good feeding grounds for insectivorous birds (De la Via 2004, p. 10), such as the white-browed tit-spinetail (BLI 2009d, p. 2). The characteristics of

Polylepis

habitat are described above in more detail as part of the Habitat and Life History of the ash-breasted tit-tyrant.

This species appears to prefer primary (lesser disturbed) woodland habitat in larger remnant patches at the lower to mid-elevation range of its known elevational range distribution (Lloyd 2008b, pp. 735-745). It prefers areas of high density of tall, large

Polylepis

trees. These usually correspond with areas containing dense and extensive moss ground cover (Lloyd 2008b, pp. 735-745). This species generally forages on vertical trunks and on thicker, epiphyte-clad branches of

Polylepis

trees covered with moss and lichens, unlike other

Leptasthenura

species, which generally forage on the thin terminal branches of the outer canopy (Fjeldså 2010 pers. comm., p. 4). The species is different from other

Polylepis

-dependent insectivorous bird species, in particular

L. yanacensis,

in that it uses different foraging perch types, substrates, and a different niche position (Lloyd 2010 pers. comm.). The white-browed tit-spinetail has been observed to regularly use woodland patches smaller than 0.1 ha (0.25 ac) for foraging in Cordillera Vilcabamba (Lloyd 2008, p. 531; Engblom

et al.

(2002, pp. 57-58).

It is classified as an “infrequent flyer” across gaps between woodland patches. At one site in the Cordillera Vilcanota, the species was observed avoiding flying across gaps to the most distant small woodland patches if these patches were separated by more than 73 m (239 ft) from larger woodland patches (Benham

et al.

2011, p. 153; Lloyd and Marsden 2010,

in press).

Based on these observations, Engblom

et al.

(2002, p. 58) suggest that the species is able to persist in very small forest fragments, especially if a number of these patches are in close proximity. The lower elevation of this species' range changes to a mixed

Polylepis-Escallonia

(no common name) woodland, and the white-browed tit-spinetail has been observed there on occasion, such as during a snowstorm (del Hoyo

et al.

2003, p. 267; Collar

et al.

1992, p. 595; Fjeldså and Krabbe 1990, p. 348). It may not be entirely as dependent on

Polylepis

forests; rather this species may be more dependent on the density of the forest which creates the moss-lichen-insect environment (Fjeldså 2010 pers. comm.)

There is limited information on the ecology and breeding behavior of the white-browed tit-spinetail. Lloyd (2006, as cited in Lloyd 2009, p. 8) reports that the species breeds in October in Cordillera Vilcanota in southern Peru. In the same area, one adult was seen attending a nesting hole in a

Polylepis

tree in November 1997 (del Hoyo

et al.

2003, p. 267; Bushell in litt. (1999), as cited in BLI 2009d, p. 2). Only one nest of the white-browed tit-spinetail has ever been described. According to Lloyd (2006, as cited in Lloyd 2009, p. 8), the nest was located within a natural cavity of a

Polylepis racemosa

tree's main trunk, approximately 2 m (7 ft) above the ground. To construct their nest, the white-browed tit-spinetail pair uses moss, lichen, and bark fibers they stripped from

Polylepis

tree trunks, large branches, and large boulders while foraging. The nest was cup-shaped and contained two pale-colored eggs (Lloyd 2006, as cited in Lloyd 2009, p. 8).

The white-browed tit-spinetail is insectivorous, with a diet consisting primarily of arthropods (Lloyd 2009, p. 7; del Hoyo

et al.

2003, p. 267). The species forages in pairs or small family groups of three to five, and often in mixed-species flocks, gleaning insects from bark crevices, moss, and lichens on twigs, branches, and trunks (BLI 2009d, pp. 2-3; Engblom

et al.

2002, pp. 57-58; Parker and O'Neill 1980, p. 169). The white-browed tit-spinetail is highly arboreal, typically foraging acrobatically from the outer branches of

Polylepis

trees while hanging upside-down (Lloyd 2008b, as cited in Lloyd 2009, p. 7; del Hoyo

et al.

2003, p. 267).

Historical Range and Distribution

In our 2008 Annual Notice of Findings on Resubmitted Petitions for Foreign Species (73 FR 44062; July 29, 2008), we stated that, historically, the white-browed tit-spinetail may have occupied the

Polylepis

forests of the high-Andes of Peru and Bolivia. We included both countries in the historical range of the species because the species' primary habitat, the

Polylepis

forest, was historically large and contiguous throughout the high-Andes of both Peru and Bolivia (Fjeldså 2002a, p. 115). However, based on further research, we have determined that historically, the species was known from only two Regions in south-central Peru, Cusco and Apurímac (del Hoyo

et al.

2003, p. 267; Collar

et al.

1992, p. 594), and not in Bolivia.

The white-browed tit-spinetail may once have been distributed throughout south-central Peru, in previously contiguous

Polylepis

forests above 3,000 m (9,843 ft) (BLI 2009d, pp. 1-2; Fjeldså 2002a, pp. 111-112, 115; Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; BLI 2000, p. 347). However,

Polylepis

woodlands are now restricted to elevations of 3,500 to 5,000 m (11,483 to 16,404 ft) (Fjeldså 1992, p. 10). As discussed above for the Historical Range and Distribution of the ash-breasted tit-tyrant, researchers consider human activity to be the primary cause for historical habitat decline and resultant decrease in species richness (Fjeldså 2002a, p. 116; Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; Fjeldså and Kessler 1996, Kessler 1995a, b, and Lægaard 1992, as cited in Fjeldså 2002a, p. 112; Kessler and Herzog 1998, pp. 50-51). It is estimated that only 2-3 percent of the original forest cover still remains in Peru (Fjeldså 2002a, pp. 111, 113). Less than 1 percent of the remaining woodlands occur in humid areas, where denser stands are found (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113), and which are preferred by the white-browed tit-spinetail (BLI 2009d, p. 2; Lloyd 2008a, as cited in Lloyd 2009, p. 6).

Current Range and Distribution

The white-browed tit-spinetail occurs in high-elevation, semihumid patches of

Polylepis

and

Polylepis-Gynoxys

woodlands in the Andes Mountains of south-central Peru (see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=4824

for a range map of the species). The species

has a highly restricted and severely fragmented range, and is currently known from only a small number of sites in the Apurímac Department in these areas: The Runtacocha highlands; Nevado Sacsarayoc massif (mountain range); Cordillera Vilcanota and in the Laguna Anantay Valley in Apurímac. It is also known to occur in Vilcabamba in Cusco Department (within the Peruvian protected area of Santuario Histórico Machu Picchu) (Benham

et al.

2011, p. 153; Fjeldså 2010 pers. comm., p. 4; Lloyd 2010; BLI 2009c, pp. 1, 3; BLI 2009d, p. 6; del Hoyo

et al.

2003, p. 267). The species occurs at an altitude of 3,700-4,550 m (12,139-14,928 ft) (Lloyd 2009, pp. 1, 5-6; del Hoyo

et al.

2003, p. 267; Fjeldså and Krabbe 1990, p. 348). It is more commonly encountered in the lower elevations within this range. Subpopulations of white-browed tit-spinetail in the Cordillera Vilcanota have a very narrow estimated niche (Benham

et al.

2011, p. 153; Fjeldså 2010 pers. comm.; Lloyd 2009, p. 5; Lloyd and Marsden 2008, pp. 2645-2660). The estimated potential range of the species is approximately 2,500 km

2

(965 mi

2

) (BLI 2011f, p. 1).

Population Estimates

Peru. An estimated 305 birds were located within 3 disjunct

Polylepis

forest patches in Peru (Aucca-Chutas 2007, p. 8). This included 205 birds and 36 birds in Cordilleras Vilcanota and Vilcabamba, respectively (Cusco), and 64 birds in Cordillera del Apurímac (Runtacocha highlands of Apurímac) (Aucca-Chutas 2007, p. 8). The species may occur at higher densities in other areas of

Polylepis

forests (Lloyd 2008c, as cited in Lloyd 2009, p. 9). Despite the low population estimates of this species, the quantitative data from Cordillera Vilcanota indicates that the white-browed tit-spinetail is one of the most abundant

Polylepis

specialists in southern Peru (Lloyd 2009, p. 9). This species was documented in Laguna Anantay, Apurímac in 2010, and its estimated population size in this location was 229 individuals (Benham

et al.

2011, p. 153).

Global population estimate: BLI categorizes the white-browed tit-spinetail as having a population size between 500 and 1,500 mature individuals (BLI 2011f, p. 1). However, the estimate is based on Engblom

et al.

2002 (p. 58). In 2002, Fjeldså (2002b, p. 9) also estimated a total population size of between 250 and 1,000 pairs of birds. More recently it was described as having one of the highest densities of all the threatened

Polylepis

bird species in this area (Benham

et al.

2011, p. 153; Lloyd 2010, pers. comm.). It is described as being common in a rare and patchy (fragmented) habitat (Lloyd 2008). Some species have always been rare (Donald

et al.

2010, p. 10); particularly those associated with habitat such as

Polylepis-

dominated forest

.

However, as of 2009, the species was described as experiencing a population decline between 10 and 19 percent in the past 10 years, and this rate of decline was predicted to continue (BLI 2009d, p. 5). The species' population decline is correlated with the rate of habitat loss and degradation (see Factor A) (BLI 2009d, p. 6). Based on the best available information, we consider the population estimate to be between 500 and 1,500 mature individuals.

Conservation Status

The white-browed tit-spinetail is considered endangered by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276854). The IUCN considers the white-browed tit-spinetail to be endangered due to its very small and severely fragmented range and population, which continue to decline with ongoing habitat loss and a lack of habitat regeneration (BLI 2009d, p. 1). Additional protections that are likely to benefit this species include three new recently approved community-owned, private conservation areas (3,415 ha or 8,438 ac) to protect

Polylepis

forest in the Vilcanota Mountains of southeastern Peru, near Cusco, which will subsequently provide protection for bird species such as the white-browed tit-spinetail (American Bird Conservancy 2011, unpaginated; Salem News 2010, p. 1).

Summary of Factors Affecting the Species

Section 4 of the Act (16 U.S.C. 1533), and its implementing regulations at 50 CFR part 424, set forth the procedures for adding species to the Federal Lists of Endangered and Threatened Wildlife and Plants. A species may be determined to be an endangered or threatened species due to one or more of the five factors described in section 4(a)(1) of the Act. The five factors are: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; and (E) other natural or manmade factors affecting its continued existence. Listing actions may be warranted based on any of the above threat factors, singly or in combination. In considering what factors might constitute threats, we look beyond the exposure of the species to determine whether the species responds to the factor in a way that causes actual impacts to the species, and we look at the magnitude of the effect. If there is exposure to a factor, but no response, or only a beneficial response, that factor is not a threat. If there is exposure and the species responds negatively, the factor may be a threat and we then attempt to determine how significant the factor is. If the factor is significant and, therefore, a threat, it may drive or contribute to the risk of extinction of the species such that the species warrants listing as threatened or endangered as those terms are defined by the Act. In making this final listing determination, we evaluated threats to each of these six species. Our evaluation of this information is discussed below.

There are three habitat types in which these six species exist. All six species occur in Peru; two of them occur in Bolivia. The Peruvian plantcutter occurs in coastal northern Peru, the Junín grebe and Junín rail occur in and around Lake Junín, and three (the white-browed tit-spinetail, royal cinclodes, and ash breasted tit-tyrant) occur in forest habitat dominated by

Polylepis

species. Within each of these three habitats, these three species depend on similar physical and biological features and on the successful functioning of their ecosystems to survive. They also face the same or very similar threats within each habitat type. One peer reviewer thought that the proposed rule was difficult to follow, so we hope that the way we have organized our evaluation and finding in this final rule is more clear.

Although the listing determination for each species is analyzed separately, to avoid redundancy we have organized the specific analysis for each species within the context of the broader scale and threat factor in which it occurs. Since within each habitat, these species face a suite of common or mostly overlapping threats, similar management actions would reduce or eliminate those threats. Effective management of these threat factors often requires implementation of conservation actions at a broader scale to enhance or restore critical ecological processes and provide for long-term viability of those species in their native environment. Thus, by taking this broader approach, we hope this final rule is effectively organized.

Summary of Factors

A. The Present or Threatened Destruction, Modification, or Curtailment of the Species' Habitat or Range

Ash-breasted tit-tyrant, royal cinclodes, and white-browed tit-spinetail (Polylepis habitat)

1.

Ash-breasted tit-tyrant.

The ash-breasted tit-tyrant is dependent upon high-elevation semihumid

Polylepis

or

Polylepis-Gynoxys

woodlands (del Hoyo

et al.

2004, pp. 281; Collar

et al.

1992, p. 753; Fjeldså and Krabbe 1990, pp. 468-469). Researchers believe that this habitat was historically contiguous with lower-elevation cloud forests and widespread above 3,000 m (9,843 ft) (Fjeldså 2002a, pp. 111, 115; Collar

et al.

1992, p. 753), but

Polylepis

woodlands occur today only between 3,500 and 5,000 m (11,483-16,404 ft) (Fjeldså 1992, p. 10). The species prefers dense woodlands (Fjeldså 2002a, p. 114; Smith 1971, p. 269), where the best foraging habitat exists (De la Via 2004, p. 10).

Within La Paz, there may be two separate populations that are separated by the Mapiri canyon (see

www.birdlife.org/datazone/speciesfactsheet.php?id=4173

for a range map of the species). The population in the Runtacocha highland in Apurímac, Peru, is morphologically distinct from that in Cusco, although a formal subspecies description has not been published (Fjeldså 2010 pers. comm.). Several other areas with similar dense

Polylepis

stands exist further south in Apurímac, east of the Chalhuanca valley (a zone with fairly high precipitation) and could hold other populations. These could act as links or corridors to other suitable habitat such as a small

Polylepis

patch that exists near Nevado Solimana in western Arequipa. However, this patch is isolated and could only accommodate a few pairs of ash-breasted tit-tyrants (Fjeldså 2010 pers. comm.).

Although there is currently no evidence to suggest that populations in Cusco and in La Paz are connected, they may have been connected in the past. In 2007, the ash-breasted tit-tyrant was observed in the Ancash Region, Corredor Conchucos (Aucca-Chutas 2007, pp. 4, 8). Here, a

Polylepis

reforestation project is under way to connect two protected areas where ash-breasted tit-tyrants were known to occur: In Parque Nacional Huascarán and Zona Reservada de la Cordillera Huayhuash (MacLennan 2009, p. 1; Antamina Mine 2006, p. 5).

The second location spans the Peruvian-Bolivian border—in the Peruvian Administrative Regions of Apurímac, Cusco, Puno, and Arequipa (from north to south) and in the Bolivian Department of La Paz. Here it occurs in Cordillera Oriental (Apurímac and Cusco), Cordilleras Vilcanota and Vilcabamba (Cusco), and Cordillera de Carabaya (Puno)—in Peru—and ranges into Bolivia, where it is found in the Cordillera Real and the Cordillera Apolobamba (La Paz) (BLI 2009e, p. 1; Aucca-Chutas 2007, p. 8; del Hoyo

et al.

2004, p. 281; Collar

et al.

1992, p. 753; Fjeldså and Krabbe 1990, pp. 468-469). The ash-breasted tit-tyrant was only recently (in 2008) reported in Arequipa Region, Peru (BLI 2009j, p. 1).

The ash-breasted tit-tyrant is highly localized (Collar

et al.

1992, p. 753) and has been described as very rare, with usually only 1-2 pairs per occupied woodland (Fjeldså and Krabbe 1990, p. 469). It exists at such low densities in some places that it may go undetected (Collar

et al.

1992, p. 753). The species appears to be unable to persist in forest remnants smaller than 1 ha (2.5 ac) (BLI 2009o, p. 1).

2.

Royal cinclodes.

The royal cinclodes is restricted to high-elevation (3,500-4,600 m or 11,483-12,092 ft), moist, moss-laden areas of semihumid

Polylepis

or

Polylepis-Gynoxys

woodlands (BLI 2009i, p. 2; del Hoyo

et al.

2003, p. 253; BLI 2000, p. 345; Collar

et al.

1992, p. 588).

Polylepis

woodlands are dispersed and sparse, with an estimated remaining area of 1,000 km

2

(386 mi

2

) in Peru and 5,000 km

2

(1,931 mi

2

) in Bolivia (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113). Within the remaining

Polylepis

woodlands, the royal cinclodes' range is approximately 2,700 km

2

(1,042 mi

2

) (BLI 2011e, p. 1) (See

http://www.birdlife.org/datazone/speciesfactsheet.php?id=9773

for a range map of the species). Less than 1 percent of the remaining woodlands occur in humid areas, where denser stands occur (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113). The optimal habitat for the royal cinclodes is large areas of dense woodlands in the high Andes, with a closed canopy that supports its preferred foraging habitat of shady, moss-laden vegetation (Lloyd 2008, p. 735; De la Via 2004, p. 10; del Hoyo

et al.

2003, p. 253; Engblom

et al.

2002, p. 57).

3.

White-browed tit-spinetail.

The species is known from only a small number of sites at four locations: The Runtacocha highlands (in Apurímac Region), and the Nevado Sacsarayoc massif, Cordillera Vilcabamba, and Cordillera Vilcanota (in Cusco Region); however, new

Polylepis

habitat has been located (Benham

et al.

2011, p. 145). In the Cordillera de Vilcanota (Cusco, Peru), where a large portion of the known white-browed tit-spinetail population occurs (205 birds were recently observed there, of 305 total birds observed in 3 study sites in Peru) (Aucca-Chutas 2007, p. 8),

Polylepis

woodland habitat is highly fragmented and degraded. According to Engblom

et al.

(2002, pp. 57-58), the species has been recorded in patches of woodland as small as 0.25 ha (0.6 ac) in Cordillera Vilcabamba, but the species' persistence in small patches appears to be dependent on the patches being in close proximity to each other.

Polylepis habitat

High-Andean

Polylepis

woodlands are considered by experts to be the most threatened habitat in Peru and Bolivia (Purcell

et al.

2004, p. 457), throughout the Andean region (BLI 2009a, p. 2), and are one of the most threatened woodland ecosystem types in the world (Renison

et al.

2005, as cited in Lloyd 2009, p. 10). The IUCN has listed several

Polylepis

species as vulnerable, including two species,

Polylepis incana

and

P. pepei

that occur within the range of these three species (Ramsay and Aucca 2003, pp. 3-4; WCMC 1998a, p. 1; WCMC 1998b, p. 1). Peruvian and Bolivian

Polylepis

woodlands today are highly fragmented. In the late 1990s, Fjeldså and Kessler (1996, as cited in Fjeldså 2002a, p. 113) conducted comprehensive ground surveys and analyzed maps and satellite images of the area. They estimated that the current range of

Polylepis

woodlands had been reduced from historical levels by 97-98 percent in Peru and 90 percent in Bolivia. Contemporary

Polylepis

woodlands are dispersed and sparse, covering an estimated area of 1,000 km

2

(386 mi

2

) and 5,000 km

2

(1,931 mi

2

) in Peru and Bolivia, respectively (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113). Of the remaining

Polylepis

woodlands, only 1 percent is found in humid areas, where the denser

Polylepis

forests preferred by the ash-breasted tit-tyrant tend to occur (Fjeldså and Kessler 1996, as cited in Fjeldså 2002a, p. 113).

Habitat loss, conversion, and degradation throughout these three species' range have been and continue to occur as a result of ongoing human activity, including:

(1) Clear cutting and burning;

(2) Extractive activities;

(3) Human encroachment; and

(4) Climate fluctuations that may exacerbate the effects of habitat fragmentation.

Clearcutting and burning.

Clear cutting and burning are among the most destructive activities and are a leading cause for

Polylepis

habitat loss (WCMC 1998a, p. 1; WCMC 1998b, p. 1). Forested areas are cleared for agriculture and to create pasture for cattle, sheep,

and camels (BLI 2009a, p. 2; BLI 2009c, pp. 1-2; BLI 2009d, pp. 1-2; BLI 2009e, pp. 1, 5; BLI 2009h, p. 1; BLI 2009m, p. 1; BLI 2009n, p. 4). Grazing lands situated among remaining forest patches are regularly burned in order to maintain the grassland vegetation (locally known as

chaqueo

). Regular burning prevents regeneration of native forests and is considered the key factor limiting the distribution of

Polylepis

forests (BLI 2009f, p. 1; BLI 2009n, p. 4; Fjeldså 2002b, p. 8; WCMC 1998a, p. 1). In some areas, the burns escape control, causing further habitat destruction (BLI 2009a, p. 2; BLI 2009e, pp. 1, 5). Burning and clear cutting occur throughout the ash-breasted tit-tyrant's range, including Ancash, Apurímac, and Cusco in Peru; and in La Paz, Bolivia (BLI 2009a, p. 2). These activities are also ongoing within protected areas, including Parque Nacional Huascarán, Santuario Histórico Machu Picchu, and Zona Reservada de la Cordillera Huayhuash (BLI 2009l, p. 4; BLI 2009n, p. 2; Barrio 2005, p. 564).

With years of extremely high rainfall followed by years of extremely dry weather, the risk of fire is increased from the accumulated biomass during the wet period that dries and adds to the fuel load in the dry season (Block and Richter 2007, p. 1; Power

et al.

2007, p. 898). Evidence suggests that the fire cycle in Peru has shortened, particularly in coastal Peru and west of the Andes (Power

et al.

2007, pp. 897-898). Changes in the fire-regime can have broad ecological consequences (Block and Richter 2007, p. 1; Power

et al.

2007, p. 898). Research in Ecuadorian

Polylepis-Gynoxys

mixed woodlands indicated a strong reduction in

P. incana

adult and seedling survival following a single fire. This indicates that

Polylepis

species do not recover well from even a single fire event (Cierjacks

et al.

2007, p. 176). Because burning has been considered to be a key factor preventing

Polylepis

regeneration (Fjeldså 2002a, p. 112, 120; Fjeldså 2002b, p. 8), an accelerated fire cycle would exacerbate this situation.

As a result of the intensity of burning and grazing,

Polylepis

species are generally restricted to areas where fires cannot spread and where cattle and sheep do not normally roam—in stream ravines and on boulders, rock ledges, and sandy ridges (Fjeldså 2002a, p. 112; Fjeldså 2002b, p. 8). Grazing and trampling by domesticated animals further limit forest regeneration (Fjeldså 2002a, p. 120) and contribute to the degradation of remaining forest patches. Sheep and cattle have solid, sharp hooves that churn up the earth, damaging vegetation and triggering erosion (Purcell

et al.

2004, p. 458; Engblom

et al.

2002, p. 56). The loss of nutrient-rich soils leads to habitat degradation, which reduces the ability of the habitat to support dense stands of

Polylepis

woodlands (Jameson and Ramsay 2007, p. 42; Purcell

et al.

2004, p. 458; Fjeldså 2002b, p. 8).

Polylepis

habitat is also subject to conversion, degradation, or destruction caused by extractive activities such as firewood collection, timber harvest, and mining. Cutting wood for fuel has a consistent and ongoing impact throughout these three species' ranges (BLI 2009a, p. 2; BLI 2009b, pp. 1-2; BLI 2009c, pp. 1-2; BLI 2009d, pp. 1-2; BLI 2009f, p. 1; BLI 2009l, p. 1; WCMC 1998a, p. 1). The high-altitude zones where

Polylepis

occurs have long been inhabited by subsistence farmers who rely on

Polylepis

wood for firewood and charcoal production (Aucca-Chutas and Ramsay 2005, p. 287). Habitat degradation is occurring in the Santuario Histórico Machu Picchu in Peru (BLI 2009h, p. 4), and Parque Nacional y Área Natural de Manejo Integrado Madidi, Parque Nacional y Área Natural de Manejo Integrado Cotapata, and the colocated protected areas of Reserva Nacional de Fauna de Apolobamba, Área Natural de Manejo Integrado de Apolobamba, and Reserva de la Biosfera de Apolobamba in Bolivia (BLI 2009a, p. 2; BLI 2009b, p. 2; BLI 2009c, p. 2; BLI 2009d, p. 5).

Community-based

Polylepis

conservation programs fostered by the Peruvian nongovernmental organization Asociación Ecosistemas Andinos (ECOAN) have been under way in Peru and Bolivia since 2004, encompassing Cordilleras Vilcanota and Vilcabamba (Cusco Region), highlands of the Apurímac Region (Lloyd 2009, p. 10; Aucca-Chutas and Ramsey 2005, p. 287; ECOAN no date (n.d.), p. 1) and in the Ancash Region (MacLennan 2009, p. 2). These are known as the Vilcanota Project or ECOAN Projects (Aucca-Chutas and Ramsey 2005, p. 287; ECOAN n.d., p. 1). Local communities enter into and enforce management agreements aimed at mitigating the primary causes for

Polylepis

deforestation: burning, grazing, and wood-cutting. These projects foster local, sustainable use of resources (Aucca-Chutas and Ramsay 2005, p. 287; ECOAN n.d., p. 1; Engblom

et al.

2002, p. 56), such as the use of more fuel-efficient wood-burning stoves that require half the amount of wood fuel (MacLennan 2009, p. 2).

Polylepis

wood is also harvested for local commercial use, including within protected areas (BLI 2009a, p. 2; WCMC 1998a, p. 1). At one site, near Abra Málaga (Cusco Region), wood has been harvested for sale to local hotels in the towns of Urubamba and Ollantaytambo to support tourism activity (Engblom 2000, p. 1). Engblom (2000, p. 1) documented felling for firewood at this site in Cusco over a 2-day period that significantly reduced the size and quality of the forest patch. Purcell

et al.

(2004, p. 458) noted a positive correlation between habitat destruction and increased demand for (and the concomitant rise in the price of) fuel.

Polylepis

is also harvested for construction, fencing, and tool-making (Aucca-Chutas and Ramsey 2005, p. 287; BLI 2009a, p. 2). Commercial-scale activities such as clear cutting, logging, tourism, and infrastructure development are ongoing throughout these species' ranges, and alter otherwise sustainable resource use practices (MacLennan 2009, p. 2; Aucca-Chutas and Ramsay 2005, p. 287; Purcell and Brelsford 2004, pp. 156-157; Purcell

et al.

2004, pp. 458-459; Engblom

et al.

2002, p. 56; Engblom 2000, p. 2; WCMC 1998a, p. 1).

Human encroachment.

Human encroachment and concomitant increasing human population pressures exacerbate the destructive effects of ongoing human activities throughout

Polylepis

habitat. Habitat destruction is often caused by a combination of human activities that contribute to habitat degradation. In the Cordillera de Vilcanota (Cusco, Peru), where an estimated 181 ash-breasted tit-tyrants were reported in 2007 (Aucca-Chutas 2007, pp. 4, 8), the rate of habitat loss was studied by comparing forest cover between 1956 and 2005. This study revealed a rate of habitat loss averaging only 1 percent. However, remaining patches of

Polylepis

woodland were small, with a mean patch size of 3 ha (7.4 ac). Four forest patches had disappeared completely; and no new patches were located within the study area (Jameson and Ramsay 2007, p. 42). Lloyd (2008, p. 532) studied bird foraging habits at three

Polylepis

woodland sites in the Cordillera Vilcanota during 2003-2005. The sites were described as highly fragmented, consisting of many small remnant patches (less than 1 ha (2.5 ac)) and scattered trees separated from larger woodland tracts (greater than 10 ha (25 ac)) by distances of 30-1,500 m (98-4,921 ft) (Lloyd and Marsden in press, as cited in Lloyd 2008, p. 532). ECOAN is working with local communities in this area to address habitat degradation and is working on

Polylepis

reforestation projects, which are discussed below in this document (ABC undated, pp. 1-3).

Extractive activities.

Mining in

Polylepis

habitat occurs in the Peruvian regions of Ancash and Huánaco and in the Bolivian Department of La Paz (BLI 2009b, p. 1; BLI 2009d, p. 1; BLI 2009g, p. 1). As of 2006, Ancash was home to the largest zinc and copper mine in the world, with a monthly average production rate of 105,000 metric tons (231,485 pounds) of minerals per day and a 300-kilometer (km) (186-mile (mi)) underground pipeline that stretches from the mine to the port of Punta Lobitos along the coast (Antamina Mine 2006, pp. 4, 9;

www.antamina.com/02_operacion/En_puerto.html

). A mixture of water and minerals are transported by the pipeline (Biodiversity Neutral Initiative [BNI] 2006, p. 2). The actual mining footprint was estimated to be 2,221 hectares (5,488 acres) (BNI 2006, p. 2). As a result of mining activities, the habitat is affected by effluent containing metals such as copper, zinc, iron, and molybdenum) (BNI 2006, p. 7). Mining also occurs in ash-breasted tit-tyrant habitat in La Paz, Bolivia, where there are active gold, tin, silver, and tungsten mines, in addition to gravel excavation for cement production (USGS Minerals Yearbook 2005, pp. 4-7).

Recently, an accelerated rate of

Polylepis

forest destruction has been attributed to clear cutting for road building and industrialization projects, such as mining and construction of hydroelectric power stations (Purcell and Brelsford 2004, pp. 156-157). Between 1991 and 2003, approximately 200 ha (494 ac) of

Polylepis

habitat was destroyed. Thus, nearly two-thirds of the forest cover that existed in the 1990s no longer existed in 2003 (Purcell and Brelsford 2004, p. 155). Only 520 ha (1,285 ac) of

Polylepis

forest was estimated to remain in the Bolivian Department of La Paz, representing approximately a 40 percent rate of habitat loss in just over one decade. The researchers inferred that this rate of destruction could result in extirpation of the remaining

Polylepis

forest in La Paz within the next 30 years if no mitigation is implemented (Purcell and Brelsford 2004, pp. 157).

Since 2003, Antamina Mine has undertaken

Polylepis

habitat conservation programs within the areas affected by mineral extraction in partnership with ECOAN and other NGOs. Antamina Mine has committed to investing a million dollars in programs ranging from education and tourism, to organic agriculture and sustainable development, and reforestation of areas using

Polylepis

species. The Antamina Mining Company conservation program supports the planned reforestation within a 50,000-ha (123,552-ac) area. Planting of

Polylepis

species will assist in connecting habitat between two protected areas, Parque Nacional Huascarán and Zona Reservada de la Cordillera Huayhuash (Antamina Mine 2006, p. 5). As of 2009, the project had succeeded in restoring 150 ha (371 ac) of forest, with a 95 percent survival rate (MacLennan 2009, p. 1). Known as Corredor Conchucos, at least 30 ash-breasted tit-tyrants have recently been observed there (Aucca-Chutas 2007, p. 8).

Mining and hydroelectric projects open previously undisturbed areas to exploitation and attract people seeking employment (Purcell

et al.

2004, p. 458). Increased urbanization and mining have led to increased infrastructure development. Road building and mining projects further facilitate human access to remaining

Polylepis

forest fragments, throughout these three species' ranges (Purcell

et al.

2004, pp. 458-459; Purcell and Brelsford 2004, pp. 156-157), including protected areas. In the Bolivian Department of La Paz, one of the most transited highways in the country is located a short distance from the Parque Nacional y Área Natural de Manejo Integrado Cotapata (BLI 2009b, p. 2). Road building, mining, and other large-scale resource exploitations have major impacts on the habitat (Purcell and Brelsford 2004, p. 157).

Tourism.

Ecotourism is considered a growing problem within protected areas where these three species occur such as in the Zona Reservada de la Cordillera Huayhuash in Peru, and in the Apolobamba protected areas in Bolivia (BLI 2009e, p. 5; Barrio 2005, p. 564). For example, in Huascarán National Park, irresponsible tourism is affecting habitat (TNC 2011, p. 6). Visitors form base camps at the foot of mountains and make expeditions to the summits. Tourists camp and hike for several days (TNC 2011, p. 6). Tourism along the climbing routes and circuits is causing progressive loss of vegetative coverage and is disturbing wildlife in the surrounding areas (TNC 2011, pp. 6-8). Poorly managed tourism results in contamination by unmanaged garbage and waste, unauthorized trail and road openings, soil erosion, and vegetation loss (TNC 2011, p. 6). Burying garbage can damage soil because it causes erosion as well as contamination. Garbage and waste left behind contaminates water (originating from glaciers), lakes, rivers, and streams.

Lack of

Polylepis

forest regeneration during nearly 50 years underscores the ramifications of continued burning and clearing to maintain pastures and farmland, which are prevalent activities throughout the ranges of these three species (BLI 2009a, p. 2; BLI 2009b, p. 2; Engblom

et al.

2002, p. 56; Fjeldså 2002a, pp. 112, 120; Fjeldså 2002b, p. 8; Purcell

et al.

2004, p. 458; WCMC 1998a, p. 1). These habitat-altering activities are considered to be key factors preventing regeneration of

Polylepis

woodlands (Fjeldså 2002a, p. 112, 120) and are factors in the historical decline of

Polylepis

-dependent bird species, including these three species (BLI 2009i, p. 6; Fjeldså 2002a, p. 116; Herzog

et al.

2002, p. 94; Kessler 2002, pp. 97-101; Fjeldså and Kessler 1996).

The royal cinclodes' population size is considered to be declining in close association with continued habitat loss and degradation (BLI 2009i, p. 6). The royal cinclodes may once have been locally common and distributed across most of central to southern Peru and into the Bolivian highlands, in once-contiguous expanses of

Polylepis

forests (BLI 2009i, p. 1; Fjeldså 2002a, pp. 111-112, 115; BLI 2000, p. 345). In the Cordillera de Vilcanota (Cusco, Peru), where a large portion of the known royal cinclodes population occurs (116 birds were observed there, out of 189 total birds observed in 4 study sites in Peru) (Aucca-Chutas 2007, pp. 4, 8),

Polylepis

woodland habitat is highly fragmented and degraded. The species may have been extirpated from its type locality (Aricoma Pass, Puno), where

Polylepis

forest no longer occurs. A search for the species in 1987 resulted in no observations of the royal cinclodes (Engblom 2002, p. 57; Collar

et al.

1992, p. 589). The royal cinclodes is not predicted to occur in Puno because habitat no longer exists there (InfoNatura 2007, p. 1), and only two birds have been observed at that location in recent years (Aucca-Chutas 2007, pp. 4, 8). Therefore, further habitat loss will continue to impact the species' already small population size (see Factor E).

Polylepis

habitat throughout the range of the white-browed tit-spinetail has been and continues to be altered and destroyed as a result of human activities, including clear cutting and burning for agriculture and grazing lands and extractive activities including harvest for timber, firewood, and charcoal. It is estimated that only 2-3 percent of the dense

Polylepis

woodlands preferred by the species remain. Observations suggest that the white-browed tit-spinetail is able to persist in very small forest fragments (e.g., areas as small as 0.25 ha (0.6 ac) in Cordillera Vilcabamba); however, this depends on whether or not adequate

patches are near one another. Continued loss, degradation, and fragmentation of remaining

Polylepis

woodlands increase the degree of isolation (distance) between populations and subpopulations (and neighboring woodland fragments within the same site). Since individuals tend not to cross the larger gaps between neighboring woodland patches, increasing isolation (at whatever scale) is likely to affect the dispersal and other movement patterns between populations, and, therefore, impact the species' population persistence within the landscape.

The white-browed tit-spinetail prefers areas of high density of tall, large

Polylepis

trees, which usually correspond with areas containing dense and extensive moss ground cover. When habitat is degraded, there is often a lag time before the species losses are evident (Brooks

et al.

1999, p. 1140), so the white-browed tit-spinetail may still be present, despite the low quality of its habitat. This species is not likely able to persist in forest remnants smaller than 1 ha (2.5 ac) (Gomez

in litt.

2003, 2007 in BLI 2009o, p. 1), and the remaining

Polylepis

forest patch sizes have met or are approaching the lower threshold of this species' ecological requirements.

Larger concentrations of people put greater demand on the natural resources in the area (Donald

et al.

2010, p. 26). Increasing demand for firewood upsets informal and otherwise sustainable community-based forest management traditions (Purcell and Brelsford, 2004, p. 157). Increasing human populations in the high-Andes of Bolivia and Peru have also resulted in a scarcity of arable land. This has led many farmers to burn additional patches of

Polylepis

forests to plant crops, even on steep hillsides that are not suitable for cultivation (BLI 2009b, p. 2; BLI 2009h, p. 1; Hensen 2002, p. 199). These ongoing farming practices result in the rapid loss of

Polylepis

forests stretching from Bolivia to Peru.

Thus, habitat degradation has serious impacts in

Polylepis

woodlands (Jameson and Ramsay 2007, p. 42), especially given these species' preference for dense woodlands (Fjeldså 2002a, p. 114; Smith 1971, p. 269). The fact that no new

Polylepis

forest patches had become established between 1956 and 2005 underscores the long-term ramifications of ongoing burning, clearing, grazing, and other habitat-altering human activities that are pervasive throughout these three species' ranges (BLI 2009f, p. 1; BLI 2009n, p. 4; Fjeldså 2002b, p. 8; WCMC 1998a, p. 1; WCMC 1998b, p. 1). These activities are considered to be key factors both in preventing regeneration of

Polylepis

woodlands and in the historical decline of

Polylepis

-dependent bird species, including these three species (Fjeldså 2002a, p. 116). Therefore, further habitat loss will continue to impact these species' already small population sizes (see Factor E).

Climate Fluctuations

Peru is subject to climate fluctuations that may exacerbate the effects of habitat fragmentation, such as those that are related to the El Niño Southern Oscillation (ENSO). The term ENSO refers to a range of variability associated with the southern trade winds in the eastern and central equatorial Pacific Ocean. El Niño events are characterized by unusual warming of the ocean, while La Niña events bring cooler ocean temperatures (Tropical Atmosphere Ocean (TAO) Project no date (n.d.), p. 1). Generally speaking, extreme ENSO events alter weather patterns, so that precipitation increases in normally dry areas, and decreases in normally wet areas. During an El Niño event, rainfall dramatically increases, whereas a La Niña event brings near-drought conditions (Holmgren

et al.

2001, p. 89).

Climate change is characterized by variations in the earth's temperature and precipitation, causing changes in atmospheric, oceanic, and terrestrial conditions (Parmesan and Mathews 2005, p. 334). In addition to substrates (vegetation, soil, water), habitat is also defined by atmospheric conditions; changes in air temperature and moisture can effectively change a species' habitat. Periodic climatic patterns such as El Niño and La Niña can cause or exacerbate such negative impacts on a broad range of terrestrial ecosystems and Neotropical bird populations (Gosling

et al.

2009, pp. 1-9; Plumart 2007, pp. 1-2; Holmgren

et al.

2001, p. 89; England 2000, p. 86; Timmermann 1999, p. 694).

Over the past decade, there have been four El Niño events (1997-1998, 2002-2003, 2004-2005, and 2006-2007) and three La Niña events (1998-2000, 2000-2001, and 2007-2008) (National Weather Service (NWS) 2009, p. 2). Some research suggests the Andean highlands, and

Polylepis

species in particular, are strongly influenced by ENSO events (Christie

et al.

2008, p. 1; Richter 2005, pp. 24-25). Christie

et al.

(2008, p. 1) found that tree growth in

P. tarapacana

is highly influenced by ENSO events because ENSO cycles on the Peruvian Coast are strongest during the growing season (December-February). ENSO-related droughts can increase tree mortality and dramatically alter age structure within tree populations, especially in cases where woodlands have undergone disturbance such as fire and grazing (Villalba and Veblen 1998, pp. 2624, 2637; Villalba and Veblen 1997, pp. 121-123).

Some changes in the physical environment include changes in precipitation and temperature and the frequency and severity of events (Huber and Gulledge 2011, p. 3; Solman 2011, p. 20; Laurance and Useche 2009, p. 1432; Margeno 2008, p. 1; Nuñez

et al.

2008, p. 1). Climate change has also resulted in a variety of alterations in ecosystem processes, species distributions, and the timing of seasonal events such as bird migrations and the onset of flowering (GCCIUS 2009, pp. 79-88). Forecasts of the rate and consequences of future climate change are based on the results of extensive modeling efforts conducted by scientists around the world (Solman 2011, p. 20; Laurance and Useche 2009, p. 1432; Nuñez

et al.

2008, p. 1; Margeno 2008, p. 1; Meehl

et al.

2007, p. 753). While projections from global climate model simulations are informative and various methods exist to downscale global and national projections to the regional or local area in which the species lives, in many cases, downscaled projections are still being developed (Solman 2011, p. 20; Insel

et al.

2009; Nuñez

et al.

2008, p. 1; Marengo 2008, p. 1), and the local effect of climate change on

Polylepis

is unclear.

Jetz

et al.

(2007, p. 1,211) investigated the effects of climate change on 8,750 land bird species that are exposed to ongoing manmade land cover changes (i.e., habitat loss). They determined that narrow endemics such as these three species are likely to suffer greater impacts from climate change combined with habitat loss (Jetz

et al.

2007, p. 1213). This is due to the species' already small population size, specialized habitat requirements, and heightened risk of extinction from stochastic demographic processes (see also Factor E). According to this study, by 2050, up to 18 percent of the ash-breasted tit-tyrant's current remaining range is likely to be unsuitable for this species due to climate change. By 2100, one estimate predicted that about 18 to 42 percent of the species' range is likely to be lost as a result of climate change (Jetz

et al.

2007, Supplementary Table 2, p. 73). With respect to the royal cinclodes, researchers predicted that, by 2050, approximately 3 to 15 percent of its current remaining range is likely to be unsuitable for this species due to climate change and, by 2100, it is predicted that about 8 to 18 percent of the species' range is likely to be lost as a direct result of global climate change

(p. 89). With respect to the white-browed tit-spinetail, the researchers predicted that, by 2050, another one percent of its current remaining range is likely to be unsuitable for this species due to changes in the local climate. By 2100, it is predicted that about 43 percent of the species' range is likely to be lost as a direct result of global climate change (p. 89).

There is conflicting information about how changes in climate might affect these species' habitat, which is associated with cloud mist-zones. Fossil records indicate that these species' habitat,

Polylepis

forest in the central Andes, was at a maximum during warm, wet conditions approximately 1,000 years ago, but might be at a minimum during the warmer and drier-than-modern conditions predicted for later this century (Gosling

et al.

2009, pp. 2, 10). The maximum abundance of

Polylepis

is coincident with times of warmer, wetter conditions, while warmer, drier conditions minimize optimum habitat (Gosling 2009, p. 18). This suggests that

Polylepis

forests may become scarcer. If these three bird species are unable to adapt to other habitat, the lack of mature

Polylepis

forests may affect these species. However, this same paper and other research indicate that

Polylepis

habitat may experience more moisture (Gosling

et al.

2009, p. 11; Insel

et al.

2009, unpaginated; Marengo 2008, p. 4). The effects of climate change are still uncertain, in part due to the localized effects of the Andes (Insel

et al.

2009, pp. 1-2). Other recent regional models project both an increase in wet-season precipitation and a decrease in dry-season precipitation over most of South America (Kitoh

et al.

2011, p. 1; Nuñez

et al.

2008, p. 1081). In the future, for almost the entire South American continent, precipitation intensity is expected to increase (Kitoh

et al.

2011, p. 2; Avalos-Roldán 2007, p. 76).

Other new information suggests that climate change may not be a significant factor affecting species in

Polylepis

forests (Fjeldså 2010 pers. comm.). Although stronger ENSO impacts may cause drier conditions in Peru's western cordillera, the effect further east would likely be opposite. The areas where the ash-breasted tit-tyrant occurs, for example, correspond with peaks of endemism in the humid Peruvian Andes. These areas have been found to correlate with stable local environments, likely due to interactions between atmospheric flows and local topography (Fjeldså 2010 pers. comm.). The

Polylepis

forests generally occur at the transition between deep Andean valleys and cold highlands, where the mist-zone is determined more by topography rather than by regional or global climate (Fjeldså 2010 pers. Comm; Fjeldså

et al.

1999). This characteristic is demonstrated by the persistence of relict endemic species in these places. Therefore, preferred

Polylepis

habitat may be less susceptible to larger scales of climate change.

Unpredictable climate fluctuations may exacerbate the effects of habitat fragmentation (Jetz

et al.

2007, pp. 1,211, 1,213; Mora

et al.

2007, p. 1,027). In the face of an unpredictable climate, the risk of population decline due to habitat fragmentation is heightened. Researchers have found that the combined effects of habitat fragmentation and climate change (in this case, warming) had a synergistic effect, rather than additive (Laurance and Useche 2009, p. 1427; Mora

et al.

2007, p. 1,027). In other words, the interactive effects of both climate fluctuation and habitat fragmentation led to a greater population decline than if either climate change or habitat fragmentation were acting alone on populations. However, the effect of a changing climate on these species' habitat is still unclear.

Summary of Factor A—Ash-breasted tit-tyrant, royal cinclodes, and white-browed tit-spinetail (Polylepis habitat)

These three species are dependent on

Polylepis

habitat, with a preference for dense, shady woodlands. Although the white-browed tit-spinetail has been recorded in patches of woodland as small as 0.25 ha (0.6 ac), the ash-breasted tit-tyrant and the royal cinclodes both require larger ranges than the white-browed tit-spinetail: 1-2 ha (2.5-5 ac) and 3-4 ha (7-10 ac) respectively. In the Department of La Paz, Bolivia, which encompasses Bolivia's largest urban area, most of the

Polylepis

forest had been eliminated prior to the late 1990s (Purcell and Brelsford 2004, p. 157). In Cordillera Vilcanota (Cusco, Peru), where a large concentration of the royal cinclodes individuals was observed in 2007, the average size of forest fragments just meets the lower threshold of the species' ecological requirements.

Polylepis

habitat throughout their range has been and continues to be altered and destroyed as a result of human activities, including clear cutting and burning for agriculture and grazing lands; tourism; extractive activities including firewood, timber, and minerals; human encroachment, and concomitant increased pressure on natural resources. Forest fragments in some portions of these three species' ranges are approaching the lower threshold of the species' ecological requirements. The historical decline of habitat suitable for these species is attributed to the same human activities that are causing habitat loss today. Ongoing and accelerated habitat destruction of the remaining

Polylepis

forest fragments in both Peru and Bolivia continues to reduce the quantity, quality, distribution, and regeneration of remaining patches. Some NGOs and local communities are conducting reforestation efforts in areas such as the Cordillera Vilcanota, Peru (ECOAN 2012). However, the growth of

Polylepis

species will take some time, and the results of these efforts are not yet clear. Human activities that degrade, alter, and destroy habitat are ongoing throughout the species' range, including within protected areas.

Although some climate models predict that fluctuations in precipitation and temperature, particularly ENSO events, could affect this species' habitat, other research suggests that its very local climate will not be significantly affected (Fjeldså 2010 pers. comm.; Gosling

et al.

2009). Climate change models, like all scientific models, produce projections that have some uncertainty because of the assumptions used, the data available, and the specific model features (Fernanda and Solman 2010, p. 533). The science supporting climate model projections as well as models assessing their impacts on species and habitats will continue to be refined as more information becomes available, but there are still uncertainties. Nevertheless, the species' population declines are commensurate with the declining habitat. Therefore, we find that destruction and modification of habitat threaten the continued existence of these three species throughout their range (primarily

Polylepis-

dominant habitat).

Junín grebe and Junín rail (Lake Junín)

1.

Junín grebe.

The Junín grebe is endemic to Lake Junín, where it resides year-round. The species is completely dependent on the open waters and marshland margins of the lake for feeding and on the protective cover of the marshlands during the breeding season (BLI 2009a, p. 1; BLI 2008, p. 1; Tello 2007, p. 3; Fjeldså 1981, p. 247). The current estimated range of the species is 143 km

2

(55 mi

2

) (BLI 2009b, p. 1). However, its actual range is smaller (see

http://www.birdlife.org/datazone/speciesfactsheet.php?id=3644

for a range map of the species), because the species is restricted to the southern portion of the lake (BLI 2009b, p. 1; Gill and Storer in Fjeldså 2004, p. 200; Fjeldså 1981, p. 254). Breeding season

begins in November (O'Donnel and Fjeldså 1997, p. 29; Fjeldså 1981, pp. 44, 246). Junín grebes build their nests and obtain their primary prey, pupfish, in the expansive offshore flooded marshlands that may extend into the lake up to 2-5 km (1-3 mi) from shore (BLI 2008, p. 1; Tello 2007, p. 3; Fjeldså 2004, p. 200; O'Donnel and Fjeldså 1997, pp. 29-30; Fjeldså 1981, p. 247).

2.

Junín rail.

The Junín rail is also endemic to Lake Junín, where it also resides year-round and is restricted to two localities within the shallow marshlands encircling Lake Junín (BLI 2009b, p. 2; Fjeldså 1983, p. 278). The current estimated range of the species (160 km

2

, 62 mi

2

) (BLI 2009b, p. 1) is likely an overestimate of this species' range (see

www.birdlife.org/datazone/speciesfactsheet.php?id=2842

for a range map of the species). The species is known only from two discrete locations, which are near Ondores and Pari, on the southwest shore of the lake.

The quality of both Junín grebe and Junín rail habitat and their reproductive success is highly influenced by water levels and the water quality of the lake. Water levels in the lake are affected by hydropower generation which is exacerbated by unpredictable climate fluctuations (such as drought or excessive rain). Water quality in Lake Junín has been compromised by contamination, in part due to waste from mining activities that drain into the lake (ParksWatch 2012, pp. 2-3). Environmental Mitigation Programs (PAMA) have been implemented to combat pollution from mining wastes, and impacts have been reduced significantly because miners have begun to use drainage fields and residual water is being recycled (ParksWatch 2012). However, the PAMAs do not adequately address responsibilities for the mining wastes discharged into the San Juan River course and delta; sediments containing heavy metals in the San Juan River delta leach into Lake Junín (also see Factor D). Additionally, the Upamayo Dam, located at the northwestern end of the lake, has been in operation since 1936, and the lake water is used to power the 54-megawatt Malpaso hydroelectric plant (ParksWatch 2006, p. 5; Martin

et al.

2001, p. 178). Dam operations have caused seasonal water level fluctuations up to 2 m (6 ft) in Lake Junín (Martin and McNee 1999, p. 659). Under normal conditions, water levels are lower in the dry season (June to November), and the marshlands can become partially or completely dry (ParksWatch 2009, p. 2). The floodgates of the dam are often opened during the dry season (ParksWatch 2009, p. 2), and water offtake for hydropower generation further drains the lake, such that, by the end of the dry season, in November, the marshlands encircling the lake are more apt to become completely desiccated (Fjeldså 2004, p. 123).

Reduced water levels directly impact the Junín grebe's breeding success by reducing the amount of available nesting habitat (BLI 2008, p. 1; Fjeldså 2004, p. 200). The giant bulrush marshlands, upon which the Junín grebe relies for nesting and foraging habitat, have virtually disappeared from some sections of the lake (O'Donnel and Fjeldså 1997, p. 29). When the marshlands are completely desiccated, the Junín grebe is reported to not breed at all (Fjeldså 2004, p. 123).

Reduced water levels impact the species by reducing the Junín grebe's primary prey, pupfish

(Orestias

species) (Fjeldså 2004, p. 200). The perimeter of the flooded marshlands provides the primary recruitment habitat for fish in the lake particularly during extremely dry years (Fjeldså 2004, p. 200; O'Donnel and Fjeldså 1997, p. 29). Submerged aquatic vegetation, habitat for pupfish, has become very patchy, further triggering declines in the prey population. Few marshlands are permanently inundated now due to the power generation of the Upamayo Dam, and the giant bulrushes that previously provided extensive cover for this species for breeding and feeding have virtually disappeared, reducing both nesting and foraging habitat for the Junín grebe. The reduction in nesting and foraging habitat is believed to contribute to mass mortality of Junín grebes during extreme drought years such as those that occurred during 1983-1987, 1991, and 1994-1997 (O'Donnel and Fjeldså 1997, p. 30).

Manipulation of the Lake Junín's water levels also results in competition between the white-tufted grebe

(Rollandia rolland)

and the Junín grebe for food resources during the Junín grebe's breeding season (Fjeldså 2004, p. 200). During the breeding season, in years when water levels remain high, the Junín grebe and white-tufted grebe are spatially separated. White-tufted grebes use the interior of the reed marsh, and Junín grebes use the remaining at the edges of the marshlands, closer to the center of the lake (Fjeldså 1981, pp. 245, 255). Near the end of the dry season, as early as October, when water levels are lower in the lake and the marshlands can partially or completely dry out (BLI 2009b, p. 1; ParksWatch 2009, p. 2), thousands of white-tufted grebes move from the interior of the marshlands to the edges, where they compete with the Junín grebe for food (Fjeldså 1984, pp. 413-414). Competition becomes more critical the longer the water level remains low at the end of the dry season, and activities that further reduce low water levels only exacerbate this competition (Fjeldså 1981, pp. 252-253).

Water quality affects the availability of habitat for both the endemic Junín grebe and Junín rail. The water in Lake Junín has been contaminated from mining, agricultural activities and organic matter and wastewater runoff from local communities around the lake (Shoobridge 2006, p. 3; ParksWatch 2006, pp. 5, 19; Martin and McNee 1999, pp. 660-661). Heavy metal contamination throughout the lake has exceeded established thresholds for aquatic life throughout at least one-third of the lake, and has rendered the northern portion of the lake lifeless (BLI 2008, p. 4; Shoobridge 2006, p. 3; Fjeldså 2004, p. 124; Martin and McNee 1999, pp. 660-662; ParksWatch 2006, pp. 20-21). At the lake's center, lake bottom sediments are lifeless and anoxic (having low levels of dissolved oxygen) due to contaminants (Fjeldså 2004, p. 124; Martin

et al.

2001, p. 180), and the lakeshore has become polluted with toxic acidic gray sediment (O'Donnel and Fjeldså 1997, p. 30). Martin

et al.

(2001, p. 180) determined that sediments at the lake's center are contaminated with copper, zinc, and lead and are anoxic. High concentrations of dissolved copper, lead, and zinc have damaged an estimated one-third of the lake (ParksWatch 2006, pp. 2, 20; Shoobridge 2006, p. 3; Martin and McNee 1999, pp. 660-661).

There is no vegetation at the northern end of the lake (ParksWatch 2006, pp. 20-21; Fjeldså 2004, p. 124), and ongoing contamination has the potential to reduce vegetative cover in other areas of the lake, including the marshlands where these two species occur. These pollutants have severely affected animal and plant populations in the area, contributing to mortality of species around the lake including the Junín rail and the Junín grebe (ParksWatch 2006, pp. 3, 20), and are likely to reduce the health and fitness of these two species (see Factor C).

Lake Junín is a sink for several streams that transport mining wastes and other pollution downstream and into the lake (ParksWatch 2006, p. 19). The San Juan River is the primary source of water for Lake Junín, and feeds into the lake from the northern end (Shoobridge 2006, p. 3; Martin and McNee 1999, pp. 660-661; Fjeldså 1981, p. 255). Tests indicate that the San Juan

River contains trace metals including copper, lead, mercury, and zinc in excess of currently accepted aquatic life thresholds (Martin and McNee 1999, pp. 660-661). Non-point-source pollutants from agricultural fertilizers such as ammonium and nitrate concentrations are also suspended in the water column (Martin and McNee 1999, pp. 660-661). Iron oxide contamination is prominently visible near the outflow of the San Juan River (iron oxide produces a reddish tinge, which colors the water and reed borders). Vegetation near the river's outflow is completely absent (ParksWatch 2006, pp. 20-21; Fjeldså 2004, p. 124), and this portion of the lake has been rendered lifeless by the precipitation of iron oxide from mining wastewaters (BLI 2008, p. 4). The giant bulrush marshlands, which once existed in great expanses around the entire perimeter of the lake, have virtually disappeared, and at least one species of catfish

(Pygidium oroyae)

may have been extirpated from the lake (O'Donnel and Fjeldså 1997, p. 29).

Heavy metal contamination is not limited to the northern end of the lake (ParksWatch 2006, p. 20), but extends throughout the southern end (Martin and McNee 1999, p. 662), where the Junín grebe and Junín rail are now restricted (BLI 2009b, p. 1; Fjeldså 1981, p. 254; Gill and Storer in Fjeldså 2004, p. 200). In 2009, conservation organizations and civil society groups demanded action to reverse the deterioration of Lake Junín and requested an independent environmental audit and continuous monitoring of the lake (BLI 2009b p. 4). The conservation groups BLI, American Bird Conservancy (ABC), Asociación Ecosistemas Andinos (ECOAN), and INRENA adopted the Junín grebe as the symbol of wetland conservation for the high Andes (BLI 2009c, p. 1). A translocation has been a consideration for the conservation of the Junín grebe since the mid-1990s; however, no suitable habitat for the species has been located (BLI 2009b, p. 2; O'Donnel and Fjeldså 1997, pp. 30, 35). To date, none of these conservation organization's activities have been able to adequately curb the ongoing habitat degradation.

The effects of habitat alteration and destruction (such as those caused by artificially reduced water levels and water contamination) are exacerbated by unpredictable climate fluctuations (such as drought or excessive rains) (Jetz

et al.

2007, pp. 1,211, 1,213; Mora

et al.

2007, p. 1027). Peru is subject to unpredictable climate fluctuations, such as those that are related to the ENSO. Changes in weather patterns, such as ENSO cycles (El Niño and La Niña events), tend to increase precipitation in normally dry areas, and decrease precipitation in normally wet areas (Holmgren

et al.

2001, p. 89; TAO Project n.d., p. 1); exacerbating the effects of habitat reduction and alteration on the decline of a species (Jetz

et al.

2007, pp. 1211, 1213; Mora

et al.

2007, p. 1027; Plumart 2007, pp. 1-2; Holmgren

et al.

2001, p. 89; England 2000, p. 86; Timmermann 1999, p. 694), especially for narrow endemics such as the Junín grebe and Junín rail. Moreover, the Junín grebe's low breeding potential is considered to be a reflection of its adaptation to being in a highly predictable, stable environment (del Hoyo

et al.

1992, p. 195).

The Junín grebe's breeding success and population size are highly influenced by the climate, with population declines occurring during dry years, population increases during rainy years, and mortality during extreme cold weather events. Several times during the last two decades (e.g., 1983-1987, 1991-1992, 1994-1997), the Junín grebe's population declined to 100 birds or less following particularly dry years (BLI 2009b, p. 2; BLI 2008, pp. 1, 3-4; Fjeldså 2004, p. 200; Elton 2000, p. 3). There have been short-term population increases of 200 to 300 birds in years with higher rainfall amounts following El Niño events (such as the 1997-1998 and 2001-2002 breeding seasons) (Valqui pers. comm. in BLI 2009b, p. 2; PROFONANPE 2002, in Fjeldså 2004, p. 133). However, excessive rains also can increase contamination in Lake Junín, which decreases the amount of suitable habitat for the species and has adverse effects on the species' health (see Factor C). Many Junín grebes died during extremely cold conditions in 1982 (BLI 2008, p. 4). In 2007, the population declined again following another cold weather event (Hirshfeld 2007, p. 107). These ENSO cycles are ongoing, having occurred several times within the last decade (NWS 2009, p. 2), and evidence suggests that ENSO cycles have already increased in periodicity and severity (Richter 2005, pp. 24-25; Timmermann 1999, p. 694), which can exacerbate the negative impacts of habitat destruction on a species.

Habitat degradation and alteration caused by fluctuating water levels and environmental contamination are considered key factors in the Junín grebe's historical decline (Gill and Storer, pers. comm. in Fjeldså 2004, p. 200; Fjeldså 1981, p. 254). The Junín grebe has experienced a population decline of 14 percent in the past 10 years, and this decline is expected to continue as a result of deteriorating habitat and water quality (BLI 2009b, pp. 1, 6-7). Therefore, further habitat degradation is expected to continue impacting this species' already small population (see Factor E).

The habitat in and around Lake Junín is subjected to manmade activities that have altered, destroyed, and degraded the quantity and quality of habitat available to the Junín rail. These activities include: (1) Artificial manipulation of water levels; (2) water contamination; and (3) plant harvesting in the species' breeding grounds. The negative impacts of these activities are accentuated by unpredictable climate fluctuations such as droughts or excessive rains (Jetz

et al.

2007, pp. 1211, 1213; Mora

et al.

2007, p. 1027).

Lake drawdown has been known to cause water levels to fluctuate seasonally up to 2 m (6 ft) (Martin and McNee 1999, p. 659) and has at times caused complete desiccation of the marshlands by the end of the dry season (Fjeldså 2004, p. 123). The ground-nesting Junín rail breeds near the end of the dry season, in September and October, and the species relies on the dense vegetative cover of the rushes on the lake perimeter in which to build their nests (BLI 2009b, p. 2). Eddleman

et al.

(1988, p. 463) noted that water drawdown before nesting season disrupts nest-building initiation by rails. Therefore, water drawdown near the end of the dry season that results in complete desiccation of the shallow marshlands (BLI 2009b, p. 1; ParksWatch 2009, p. 2) is likely to disrupt Junín rail nest initiation.

Experts believe that the Junín rail is restricted to the marshes at the southwestern corner of the lake because of the high level of contamination at the northwestern margins of the lake (Martin and McNee 1999, p. 662). Experts also believe that pollution and artificial water level fluctuations will continue to have adverse consequences for the vegetation surrounding the lake and, therefore, the Junín rail (BLI 2007, p. 1; J. BLI 2000, p. 170; Fjeldså

in litt.,

1987, as cited in Collar

et al.

1992, p. 190). In some places, the tall marshlands, which rely on inundated soils to thrive, have virtually disappeared because the reed-beds are no longer permanently inundated (O'Donnel and Fjeldså 1997, p. 30). Moreover, as the marshes dry, livestock (primarily sheep

(Ovis aries),

but also cattle

(Bos taurus),

and some llamas

(Llama glama)

and alpacas

(Llama pacos))

move into the desiccated wetlands surroundin

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