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]

[96100-1671-0000-B6]

[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:

Proposed rule.

SUMMARY:

We, the U.S. Fish and Wildlife Service (Service), propose to list the following six South American bird species (collectively referred to as “species” for purposes of this proposed rule) as endangered under the Endangered Species Act of 1973, as amended (Act) (16 U.S.C. 1531

et seq.

): ash-breasted tit-tyrant (

Anairetes alpinus

), Juni

n grebe (

Podiceps taczanowskii

), Juni

n rail (

Laterallus tuerosi

), Peruvian plantcutter (

Phytotoma raimondii

), royal cinclodes (

Cinclodes aricomae

), and white-browed tit-spinetail (

Leptasthenura xenothorax

)—all native to Peru. The ash-breasted tit-tyrant and royal cinclodes are also native to Bolivia. This proposal, if made final, would extend the Act's protection to these species. The Service seeks data and comments from the public on this proposed rule.

DATES:

We will accept comments received or postmarked on or before March 8, 2010. We must receive requests for public hearings, in writing, at the address shown in the

FOR FURTHER INFORMATION CONTACT

section by February 19, 2010.

ADDRESSES:

You may submit comments by one of the following methods:

• Federal eRulemaking Portal:

http://www.regulations.gov

. Follow the instructions for submitting comments on Docket No. FWS-R9-IA-2009-0059.

• U.S. mail or hand-delivery: Public Comments Processing, Attn: FWS-R9-IA-2009-0059; Division of Policy and Directives Management; U.S. Fish and Wildlife Service; 4401 N. Fairfax Drive, Suite 222; Arlington, VA 22203.

We will not accept comments by e-mail or fax. We will post all comments on

http://www.regulations.gov

. This generally means that we will post any personal information you provide us (see the Public Comments section below for more information).

FOR FURTHER INFORMATION CONTACT:

Douglas Krofta, Chief, Branch of Listing, Endangered Species Program, U.S. Fish and Wildlife Service, 4401 N. Fairfax Drive, Room 420, Arlington, VA 22203; telephone 703-358-2105; facsimile 703-358-1735. If you use a telecommunications device for the deaf (TDD), call the Federal Information Relay Service (FIRS) at 800-877-8339.

SUPPLEMENTARY INFORMATION:

Public Comments

We intend that any final action resulting from this proposal will be as accurate and as effective as possible. Therefore, we request comments or suggestions on this proposed rule. We particularly seek comments concerning:

(1) Biological, commercial trade, or other relevant data concerning any threats (or lack thereof) to these species and regulations that may be addressing those threats.

(2) Additional information concerning the taxonomy, range, distribution, and population size of these species, including the locations of any additional populations of these species.

(3) Additional information on the biological or ecological requirements of these species.

(4) Current or planned activities in the areas occupied by these species and possible impacts of such activities on these species.

(5) Any information concerning the effects of climate change on these species or their habitats.

You may submit your comments and materials concerning this proposed rule by one of the methods listed in the

ADDRESSES

section. We will not consider comments sent by e-mail or fax or to an address not listed in the

ADDRESSES

section.

If you submit a comment via

http://www.regulations.gov

, your entire comment—including any personal identifying information—will be posted on the website. If you submit a hardcopy comment that includes personal identifying information, you may request at the top of your document that we withhold this information from public review. However, we cannot guarantee that we will be able to do so. We will post all hardcopy comments on

http://www.regulations.gov

.

Comments and materials we receive, as well as supporting documentation we used in preparing this proposed rule, will be available for public inspection at

http://www.regulations.gov

, or by appointment, during normal business hours, at the U.S. Fish and Wildlife Service, Endangered Species Program, 4401 N. Fairfax Drive, Room 420, Arlington, VA 22203; telephone 703-358-2171.

Background

Section 4(b)(3)(A) of the Act requires us to make a finding (known as a “90-day finding”) on whether a petition to add a species to, remove a species from, or reclassify a species on the Federal Lists of Endangered and Threatened Wildlife and Plants has presented substantial information indicating that the requested action may be warranted. To the maximum extent practicable, we make the finding within 90 days following receipt of the petition and publish our finding promptly in the

Federal Register

. If we find that the petition has presented substantial information indicating that the requested action may be warranted (a positive finding), section 4(b)(3)(A) of the Act requires us to commence a status review of the species if one has not already been initiated under our internal candidate assessment process. In addition, section 4(b)(3)(B) of the Act requires us to make a finding within 12 months following receipt of the petition (“12-month finding”) on whether the requested action is warranted, not warranted, or warranted but precluded by higher priority listing actions. Section 4(b)(3)(C) of the Act requires that a finding of warranted but precluded for petitioned species should be treated as having been resubmitted on the date of the warranted but precluded finding, and is, therefore, subject to a new finding within 1 year and subsequently thereafter until we publish a proposal to list or a finding that the petitioned action is not warranted. The Service publishes an annual notice of review (ANOR) of findings on resubmitted petitions for all foreign species for which listings were previously found to be warranted but precluded.

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 ANOR on May 21, 2004 (69 FR 29354).

Per the Service's listing priority guidelines (September 21, 1983; 48 FR 43098), our 2007 ANOR 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 it was determined that their listing continued to be warranted but precluded because of other listing actions. A listing priority of 2 indicates that the subject species face 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, categories 2 and 3 represent the Service's highest priorities.

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 which 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), the Service must submit to the

Federal Register

proposed listing rules for the ash-breasted tit-tyrant, Juni

n grebe, Juni

n rail, Peruvian plantcutter, royal cinclodes, and white-browed tit-spinetail by December 29, 2009.

Species Information and 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.

Below is a species-by-species analysis of the five factors. The species are considered in alphabetical order, beginning with the ash-breasted tit-tyrant, followed by the Juni

n grebe, Juni

n 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; Fjeldsa

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 5 inches (in) (13 centimeters (cm)) in length, with dark gray, inconspicuously black-streaked upperparts (BLI 2009o, p. 1; del Hoyo

et al

. 2004, p. 281). 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) (see Taxonomy). Juvenile plumage is duller in appearance, but 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

; this decision was soon questioned by Zimmer (1940, p. 10). 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

(Fjeldsa

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 also 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 disjunct (widely separated) areas (see Current Range) (BLI 2000, p. 392; del Hoyo

et al

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

Habitat and Life History

The ash-breasted tit-tyrant is restricted to semihumid

Polylepis

or

Polylepis - Gynoxys

woodlands, where the species is found at elevations between 12,139 and 15,092 feet (ft) (3,700 and 4,600 meters (m)) above sea level (BLI 2000, p. 392; Collar

et al

. 1992, p. 753; del Hoyo

et al

. 2004, p. 281; Fjeldsa

and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1). The genus

Polylepis

(no English common name; locally referred to as “

queuña

”) (Aucca and Ramsay 2005, p. 1), in the Rosaceae family, comprises approximately 20 species of evergreen bushes and trees (De la Via 2004, p. 10; Kessler 1998, p. 1; Kessler and Schmidt-Lebuhn 2006, pp. 1-2), 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. Go

mez, National Museum of National History-Ornithology Section-Bolivian Fauna Collection, La Paz, Bolivia, e-mail to Division of Scientific Authority, in litt. December 4, 2007, p. 1). On average,

Polylepis

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

et al

. 2004, p. 455).

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; Fjeldsa

and Kessler 1996, as cited in Fjeldsa

2002a, p. 113; Lloyd and

Marsden in press, as cited in Lloyd 2008, p. 532). Ash-breasted tit-tyrants prefer dense

Polylepis

forests (Fjeldsa

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

Gynoxys

trees (no common name), in the Asteraceae family (De la Via 2004, pp. 10; International Plant Names Index (IPNI) 2009, p. 1). 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 2.5-5 acres (ac) (1-2 hectares (ha)) (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 (Collar

et al

. 1992, p. 754; del Hoyo

et al

. 2004, p. 281). Although species-specific information is not available, tit-tyrant nests are generally finely woven, open cups, built in a bush (Fjeldsa

and Krabbe 1990, p. 468). The species may share in rearing responsibilities, as pairs of ash-breasted tit-tyrants have been observed feeding young (BLI 2009o, p. 1; Collar

et al

. 1992, p. 754).

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; del Hoyo

et al

. 2004, p. 281; Engblom

et al

. 2002, p. 58; Fjeldsa

and Krabbe 1990, p. 468; Lloyd 2008, p. 535). In winter, when invertebrate populations diminish, tit-tyrants may also forage on seeds (Fjeldsa

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 cloudforests and widespread above 9,843 ft (3,000 m) (Collar

et al

. 1992, p. 753; Fjeldsa

2002a, pp. 111-112, 115; Herzog

et al

. 2002, p. 94; Kessler 2002, pp. 97-101). Today,

Polylepis

woodlands are found only at elevations of 11,483 to 16,404 ft (3,500 to 5,000 m) (Fjeldsa

1992, p. 10). 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 (Fjeldsa

and Kessler 1996, Kessler 1995a, Kessler 1995b, and Lægaard 1992, as cited in Fjeldsa

2002a, p. 112; Herzog

et al

. 2002, p. 94; Kessler 2002, pp. 97-101; Kessler and Herzog 1998, pp. 50-51). Modeling studies by Fjeldsa

(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 (Fjeldsa

and Kessler 1996, as cited in Fjeldsa

2002a, p. 113). Of this amount, only 1 percent of the remaining

Polylepis

woodlands are found in humid areas, where denser stands occur (Fjeldsa

and Kessler 1996, as cited in Fjeldsa

2002a, p. 113) and which are preferred by the ash-breasted tit-tyrant (BLI 2009o, p. 1; Fjeldsa

2002a, p. 114; Lloyd 2008, p. 535; Smith 1971, p. 269) (see Factor A).

Current Range and Distribution

The current range of the ash-breasted tit-tyrant is estimated to be 4,595 square miles (mi

2

) (11,900 square kilometers (km

2

)) (BLI 2009o, p. 1). However, BirdLife International (2000, pp. 22, 27) defines a species' “Range” as the “Extent of Occurrence,” which is “the area contained within the shortest continuous imaginary boundary which 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 two disjunct locations, this range estimate, therefore, includes a large area of habitat where the species is not known to occur.

The species is restricted to patches of high-elevation semihumid

Polylepis

or

Polylepis - Gynoxys

woodlands of Peru and Bolivia, where ash-breasted tit-tyrant is found only at 12,139-15,092 ft (3,700-4,600 m) (BLI 2000, p. 392; Collar

et al

. 1992, p. 753; del Hoyo

et al

. 2004, pp. 170, 281; Fjeldsa

and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1). The ash-breasted tit-tyrant is known only in two disjunct areas: one location in west-central Peru and another ranging from southern Peru into northern Bolivia (BLI 2000, p. 392; del Hoyo

et al

. 2004, p. 281; ITIS 2009, p. 1).

In west-central Peru, the northern subspecies (

A. alpinus alpinus

) occurs in the Cordilleras Central and Occidental (in the Peruvian Administrative Regions of Ancash, Hua

nuco, La Libertad, and Lima) (BLI 2007, p. 1; BLI 2009g, p. 1; BLI 2009i, p. 1; BLI 2009l, p. 1; BLI 2009o, p. 1; Collar

et al

. 1992, p. 753; 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 Hua

nuco Region, in 2003 (BLI 2007, p. 5; BLI 2009i, p. 1); La Libertad Region, in 2004 (del Hoyo

et al

. 2004, p. 281); and Lima Region and again in Hua

nuco Region, in 2007 (BLI 2007, pp. 1, 5). Also in 2007, the ash-breasted tit-tyrant was also observed in a new locality in Ancash Region, Corredor Conchucos (Chutas 2007, pp. 4, 8), where a

Polylepis

reforestation project is under way to connect two protected areas where ash-breasted tit-tyrants were already known to occur, Parque Nacional Huascara

n and Zona Reservada de la Cordillera Huayhuash (Antamina Mine 2006, p. 5; MacLennan 2009, p. 1) (see Factor A).

The second location spans the Peruvian-Bolivian border—in the Peruvian Administrative Regions of Apuri

mac, Cusco, Puno, and Arequipa (from north to south) and in the Bolivian Department of La Paz. Here, the southern subspecies (

A. alpinus bolivianus

) occurs in Cordillera Oriental (Apuri

mac 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 2000, p. 392; BLI 2009a, p. 1; BLI 2009b, p. 1; BLI 2009c, p. 1; BLI 2009d, p. 1; BLI 2009e, p. 1; BLI 2009f, p. 1; BLI 2009k, p. 1; BLI 2009m, p. 1; BLI 2009n, p. 1; BLI 2009o, p. 5; Chutas 2007, p. 8; Collar

et al

. 1992, p. 753; del Hoyo

et al

. 2004, p. 281; Fjeldsa

and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1). 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 and local, with usually only 1-2 pairs per occupied woodland” (Fjeldsa

and Krabbe 1990, p. 469). It exists at such low densities in some places that it goes undetected (Collar

et al

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

Population Estimates

Population information is presented first on the range country level and then in terms of a global population estimate. The range country estimates begin with Peru, where the majority of the population resides.

Local population estimate, Peru

: Chutas (2007, p. 8) surveyed five

disjunct

Polylepis

forest patches in Peru and estimated that 461 ash-breasted tit-tyrants were located there. This included 30 birds in Corredor Conchucos (Ancash Region); 181 birds 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 Apuri

mac” (Apuri

mac Region) (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 2007, p. 1; BLI 2009o, p. 1), with an estimated 100 pairs of birds found in approximately 40 forest patches (Fjeldsa

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). There are no population estimates within Arequipa, Hua

nuco, or Lima Regions, where the ash-breasted tit-tyrant is also reported to occur (BLI 2009g, p. 1; BLI 2009i, p. 1; BLI 2009j, p. 1; BLI 2009o, p. 1).

Local population estimate, Bolivia

: Although BirdLife International reports an estimated population size of 150-300 ash-breasted tit-tyrants in Bolivia (Go

mez in litt., 2003 and 2007, as cited in BLI 2009o, p. 1), recent surveys indicate that the estimate is smaller. Over a six-year period, Go

mez (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), using song playback and point census, 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.

Global population estimate

: BirdLife International, a global organization that consults with and assimilates information from 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 2000, p. 392; BLI 2007, p. 1; BLI 2009o, p. 1). Combining the estimated number of ash-breasted tit-tyrants in Peru and Bolivia, the total population consists of at least 641 individuals (Chutas 2007, pp. 4, 8; Go

mez in litt. 2007, p. 1), consistent with the BirdLife International category of 250-999 individuals.

However, the total population size, which includes immature individuals, is not an accurate reflection of the species' effective population size (the number of breeding individuals that contribute to the next generation) (Shaffer 1981, pp. 132-133; Soule

1980, pp. 160-162). Because the ash-breasted tit-tyrant exists as two subspecies (BLI 2000, p. 392; BLI 2009a, p. 1; BLI 2009b, p. 1; BLI 2009c, p. 1; BLI 2009d, p. 1; BLI 2009e, p. 1; BLI 2009f, p. 1; BLI 2009k, p. 1; BLI 2009m, p. 1; BLI 2009n, p. 1; BLI 2009o, p. 5; Chutas 2007, p. 8; Collar

et al

. 1992, p. 753; del Hoyo

et al

. 2004, p. 281; Fjeldsa

and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1; ITIS 2009, p. 1), it is reasonable to conclude that there is little or no gene flow between the two subspecies and that the species does not breed as a single population. Therefore, even if all 641 individuals were mature, they would not breed as a single population, such that the species' effective population size is less than 641.

There are also constraints to determining the effective population size on a subspecies level. According to International Union for Conservation of Nature (IUCN) criteria, it is estimated that there are no more than 250 mature individuals in any single subpopulation of the ash-breasted tit-tyrant (IUCN 2001, pp. 8-12). However, the parameters of a subpopulation are not provided in existing research. For instance, while ash-breasted tit-tyrants occupy territories of 2.5-5 ac (1-2 ha) (BLI 2009o, p. 1), there is no information as to the taxon's ability or tendency to travel between territories or forest patches. Research on Bolivian localities indicates that gene flow occurs between some subpopulations, but not all (Go

mez 2005, p. 86). In Bolivia, where only 1 subspecies occurs, the birds are distributed in 2 metapopulations, with at least 5 subpopulations in one location and 14 subpopulations in the other (Go

mez 2005, p. 86). Peruvian population estimates are incomplete, with no estimates for the ash-breasted tit-tyrants occurring in Arequipa, Hua

nuco, La Libertad or Lima (BLI 2009g, p. 1; BLI 2009i, p. 1; BLI 2009j, p. 1; BLI 2009o, p. 1; del Hoyo

et al

. 2004, p. 281). Therefore, we can conclude that gene flow occurs at the subspecies level, but there is not sufficient information to determine the extent to which subpopulations interbreed.

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 Factors A and E) (BLI 2007, pp. 1, 4; BLI 2009o, p. 5).

Conservation Status

The ash-breasted tit-tyrant is considered “endangered” by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276855). 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 and is confined to a habitat that is severely fragmented and is also undergoing a continuing decline in extent, area, and quality (BLI 2008, p. 1; BLI 2009o, p. 4; IUCN 2001, pp. 8-12). The ash-breasted tit-tyrant occurs within the following Peruvian protected areas: Parque Nacional Huascara

n, in Ancash, and Santuario Histo

rico Machu Picchu, in Cusco, and Zona Reservada de la Cordillera Huayhuash, spanning Ancash, Hua

nuco, and Lima (BLI 2009i, p. 1; BLI 2009l, p. 1; BLI 2009n, p. 1; Chutas

et al

. 2008, p. 16). In La Paz Department, Bolivia, the species is found in Parque Nacional y a

rea Natural de Manejo Integrado Madidi, Parque Nacional y a

rea Natural de Manejo Integrado Cotapata, and the co-located protected areas of Reserva Nacional de Fauna de Apolobamba, a

rea Natural de Manejo Integrado de Apolobamba, and Reserva de la Biosfera de Apolobamba (Auza and Hennessey 2005, p. 81; BLI 2009a, p. 1; BLI 2009b, p. 1; BLI 2009c, p. 1; BLI 2009e, p. 1; BLI 2009i, p. 1; Chutas

et al

. 2008, p. 16).

Summary of Factors Affecting the Ash-breasted Tit-tyrant

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

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

Polylepis

or

Polylepis - Gynoxys

woodlands (BLI 2000, p. 392; Collar

et al

. 1992, p. 753; del Hoyo

et al

. 2004, pp. 281; Fjeldsa

and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1). Researchers believe that this habitat was historically contiguous with lower-elevation cloudforests and widespread above 9,843 ft (3,000 m) (Collar

et al

. 1992, p. 753; Fjeldsa

2002a, pp. 111, 115), but

Polylepis

woodlands occur today only between 11,483-16,404 ft (3,500-5,000 m) (Fjeldsa

1992, p. 10). As described above (see Habitat and Life History), the species prefers dense woodlands (Fjeldsa

2002a, p. 114; Smith 1971, p. 269), where the best foraging habitat occurs (De la Via 2004, p. 10), and ash-breasted tit-tyrant occurs at altitudes of 12,139-15,092 ft (3,700-4,600 m) (BLI 2000, p. 392; Collar

et al

. 1992, p. 753; del Hoyo

et al

. 2004, pp.

170, 281; Fjeldsa

and Krabbe 1990, pp. 468-469; InfoNatura 2007, p. 1).

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 one of the most threatened woodland ecosystems 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 that occur within the ash-breasted tit-tyrant's range,

Polylepis incana

and

P. pepei

(WCMC 1998a, p. 1; WCMC 1998b, p. 1). Peruvian and Bolivian

Polylepis

woodlands today are highly fragmented. In the late 1990s, Fjeldsa

and Kessler (1996, as cited in Fjeldsa

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% in Peru and 90 percent in Bolivia. Contemporary

Polylepis

woodlands are dispersed and sparse, covering an estimated area of 386 mi

2

(1,000 km

2

) and 1,931 mi

2

(5,000 km

2

) in Peru and Bolivia, respectively (Fjeldsa

and Kessler 1996, as cited in Fjeldsa

2002a, p. 113). Of the remaining

Polylepis

woodlands, only 1 percent are found in humid areas, where denser

Polylepis

forests tend to occur (Fjeldsa

and Kessler 1996, as cited in Fjeldsa

2002a, p. 113). Dense habitat is preferred by the ash-breasted tit-tyrant (BLI 2009o, p. 1; Fjeldsa

2002a, p. 114; Lloyd 2008, p. 535; Smith 1971, p. 269).

Habitat loss, conversion, and degradation throughout the ash-breasted tit-tyrant's range have been and continue to occur as a result of ongoing human activity, including (1) Clearcutting and burning; (2) extractive activities; (3) human encroachment; and (4) unpredictable climate fluctuations that exacerbate the effects of habitat fragmentation. Clearcutting 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 pastureland 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 amongst 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; Fjeldsa

2002b, p. 8; WCMC 1998a, p. 1; WCMC 1998b, p. 1). In some areas, the burns escape control, causing further habitat destruction (BLI 2009a, p. 2; BLI 2009e, pp. 1, 5). Burning and clearcutting occur throughout the ash-breasted tit-tyrant's range, including in Ancash (BLI 2009h, p. 1), Apuri

mac (BLI 2009m, p. 1), and Cusco (BLI 2009n, p. 4), in Peru; and La Paz, Bolivia (BLI 2009a, p. 2; BLI 2009c, pp. 1-2; BLI 2009d, pp. 1-2; BLI 2009e, pp. 1, 5). These activities are also ongoing within protected areas, including Parque Nacional Huascara

n, Santuario Histo

rico Machu Picchu, and Zona Reservada de la Cordillera Huayhuash (Barrio 2005, p. 564; BLI 2009l, p. 4; BLI 2009n, p. 2) (see Factor D).

As a result of the intensity of burning and grazing,

Polylepis

species are 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 (Fjeldsa

2002a, p. 112; Fjeldsa

2002b, p. 8). Grazing and trampling by domesticated animals further limit forest regeneration (Fjeldsa

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 (Engblom

et al

. 2002, p. 56; Purcell

et al

. 2004, p. 458). The loss of nutrient-rich soils leads to habitat degradation, which reduces the ability of the habitat to support dense stands of

Polylepis

woodlands (Fjeldsa

2002b, p. 8; Jameson and Ramsay 2007, p. 42; Purcell

et al

. 2004, p. 458).

Ash-breasted tit-tyrant 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 the species' range (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 and Ramsay 2005, p. 287). Many locals manage woodlands for firewood extraction (Engblom

et al

. 2002, p. 56), and community-based

Polylepis

conservation programs fostered by the Peruvian nongovernmental organization Asociacio

n Ecosistemas Andinos (ECOAN) have been under way in Peru and Bolivia since 2004, encompassing Cordilleras Vilcanota and Vilcabamba (Cusco Region), highlands of the Apuri

mac Region (Aucca and Ramsey 2005, p. 287; ECOAN no date (n.d.), p. 1; Lloyd 2009, p. 10), and in the Ancash Region (MacLennan 2009, p. 2). Known as the “Vilcanota Project” or ECOAN Projects (Aucca and Ramsey 2005, p. 287; ECOAN n.d., p. 1), local communities enter into and enforce management agreements aimed at the primary causes for

Polylepis

deforestation: burning, grazing, and wood-cutting. These projects foster local, sustainable use of resources (Aucca 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) (see the Factor A analyses for royal cinclodes and white-browed tit-spinetail for additional examples).

Polylepis

wood is also harvested for local commercial use, including within protected areas (BLI 2009a, p. 2; WCMC 1998a, p. 1) (Factor D). At one site, near Abra Ma

laga (Cusco Region), wood is 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 and Ramsey 2005, p. 287; BLI 2009a, p. 2). Commercial-scale activities, such as clearcutting, logging, tourism, and infrastructure development, are ongoing throughout this species' range, and alter otherwise sustainable resource use practices (Aucca and Ramsay 2005, p. 287; Engblom 2000, p. 2; Engblom

et al

. 2002, p. 56; MacLennan 2009, p. 2; Purcell and Brelsford 2004, pp. 156-157; Purcell

et al

. 2004, pp. 458-459; WCMC 1998a, p. 1). Commercial-scale resource use is exacerbated by ongoing human encroachment, discussed below.

Mining in

Polylepis

habitat occurs in the Peruvian Regions of Ancash and Hua

naco and in the Bolivian Department of La Paz (BLI 2009b, p. 1; BLI 2009d, p. 1; BLI 2009g, p. 1). Ancash (Peru) is home to the largest zinc and copper mine “in the world,” with a monthly average production rate of 231,485 pounds (105,000 metric tons) of minerals per day and a 186-mile (mi) (300 kilometer (km)) 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

). Mining occurs in ash-breast 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). Antamina Mine has undertaken habitat conservation programs within the areas affected by mineral extraction, similar to the ECOAN

Polylepis

conservation programs, investing millions of dollars in programs ranging from education and tourism, to organic agriculture and sustainable development. However, tourism has had negative effects in other areas where the ash-breasted tit-tyrant occurs, including Ancash, Hua

nuco, and Lima, Peru, and La Paz, Bolivia (Barrio 2005, p. 564; BLI 2009e, p. 5) (see below). The Antamina Mining Company conservation program also supports the planned reforestation of 123,552 ac (50,000 ha) of

Polylepis

forest that will connect two protected areas, Parque Nacional Huascara

n and Zona Reservada de la Cordillera Huayhuash (Antamina Mine 2006, p. 5). To date, the project has succeeded in restoring 371 ac (150 ha) 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 (Chutas 2007, p. 8).

Human encroachment and concomitant increasing human population pressures exacerbate the destructive effects of ongoing human activities throughout the ash-breasted tit-tyrant's habitat. Mining and hydroelectric projects open new 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 the ash-breasted tit-tyrant's range (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 a

rea Natural de Manejo Integrado Cotapata (BLI 2009b, p. 2) (see Factor D). Road building, mining, and other large-scale resource exploitations are considered to have major impacts on the habitat, as compared to exploitation by local communities (Purcell and Brelsford 2004, p. 157).

Ecotourism within protected areas where the ash-breasted tit-tyrant occurs (such as in the Zona Reservada de la Cordillera Huayhuash in Peru, and in the Apolobamba protected areas in Bolivia) is considered a growing problem (Barrio 2005, p. 564; BLI 2009e, p. 5) (see Factor D). 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). Recently, an accelerated rate of

Polylepis

forest destruction has been attributed to clearcutting 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 494 ac (200 ha) 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). With this research, it was estimated that only 1,285 ac (520 ha) of

Polylepis

forest 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 thisrate of destruction could result in extirpation of the remaining

Polylepis

forest in La Paz within the next 30 years (Purcell and Brelsford 2004, pp. 157).

Larger concentrations of people put greater demand on the natural resources in the area. 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 down additional patches of

Polylepis

forests to plant crops, even on steep hillsides 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 from Bolivia to Peru.

Habitat destruction is often caused by a combination of human activities that promote habitat degradation. In the Cordillera de Vilcanota (Cusco, Peru), where an estimated 181 birds are found (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 7.4 ac (3 ha); 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 2.5 ac (1 ha)) and scattered trees, separated from larger woodland tracts (greater than 25 ac (10 ha)) by distances of 98-4,921 ft (30-1,500 m) (Lloyd and Marsden in press, as cited in Lloyd 2008, p. 532). Given that the species territory ranges from 2.5-5 ac (1-2 ha) and that the ash-breasted tit-tyrant appears to be unable to persist in forest remnants smaller than 2.5 ac (1 ha) (BLI 2009o, p. 1), these patch sizes have met or are approaching the lower threshold of the species' ecological requirements. Moreover, 10 percent of the remaining forest patches showed a decline in forest density over this time-period.

Thus, habitat degradation also has serious impacts in

Polylepis

woodlands (Jameson and Ramsay 2007, p. 42), especially given the species' preference for dense woodlands (Fjeldsa

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 the ash-breasted tit-tyrant's range (BLI 2009f, p. 1; BLI 2009n, p. 4; Fjeldsa

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 (Fjeldsa

2002a, p. 112, 120; Fjeldsa

2002b, p. 8) and in the historical decline of

Polylepis

-dependent bird species, including the ash-breasted tit-tyrant (Fjeldsa

2002a, p. 116). Researchers consider the species' population to be declining in close association with the continued habitat loss and degradation (BLI 2007, pp. 1, 4; BLI 2008, p. 1; BLI 2009o, p. 1). Therefore, further habitat loss will continue to impact the species' already small population size (see Factor E).

Peru is subject to unpredictable climate fluctuations that exacerbate the effects of habitat fragmentation, such as those that are related to the El Niño Southern Oscillation (ENSO). According to the U.S. Dept. of Commerce-National Oceanic and Atmospheric Administration (NOAA), 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).

If we consider that wildlife habitat is not only defined by substrates (vegetation, soil, water), but also atmospheric conditions, then changes in air temperature and moisture can effectively change a species' habitat. 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). Global climate change and other periodic climatic patterns (e.g., El Niño and La Niña) can cause or exacerbate such negative impacts on a broad range of terrestrial ecosystems and Neotropical bird populations (England 2000, p. 86; Holmgren

et al

. 2001, p. 89; Plumart 2007, pp. 1-2; Timmermann 1999, p. 694).

Unpredictable climate fluctuations negatively impact populations undergoing habitat fragmentation. In the face of an unpredictable climate, the risk of population decline due to habitat fragmentation is heightened. Mora

et al

. (2007, p. 1027) found that the combined effects of habitat fragmentation and climate change (in this case, warming) had a synergistic effect, rather than additive. 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. Jetz

et al

. (2007, p. 1211) investigated the effects of climate change on 8,750 land bird species, including the ash-breasted tit-tyrant, that are exposed to ongoing manmade land cover changes (i.e., habitat loss). They determined that a narrow endemic, such as the ash-breasted tit-tyrant, is likely to suffer greater impacts from climate change, especially where projected range contractions are driven by manmade land conversion activities (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; and, by 2100, it is predicted that about 18 to 42 percent of the species' range is likely to be lost as a direct result of global climate change (Jetz

et al

. 2007, Supplementary Table 2, p. 73).

In 1999, Timmermann (1999, p. 694) predicted that climate change events would increase the periodicity and severity of droughts and excessive rainfalls, such as those caused by El Niño and La Niña events. Evidence suggests that this is the case in Peru (Richter 2005, p. 24-25). 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). In Peru, the Andean highlands, and

Polylepis

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

et al

. 2008, p. 1). 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 where woodlands have undergone disturbance, such as fire and grazing (Villalba and Veblen 1997, pp. 121-123; Villalba and Veblen 1998, pp. 2624, 2637).

With years of extremely high rainfall followed by years of extremely dry weather (Block and Richter 2007, p. 1), fire hazard is increased from the biomass accumulated 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). In the case of the ash-breasted tit-tyrant, burning is considered to be a key factor preventing

Polylepis

regeneration (Fjeldsa

2002a, p. 112, 120; Fjeldsa

2002b, p. 8). 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 the species does not recover well from even a single fire event (Cierjacks

et al

. 2007, p. 176). An accelerated fire cycle would exacerbate this situation.

Activities that destroy and alter habitat are ongoing within protected areas. This is further discussed under Factor D.

Summary of Factor A

The ash-breasted tit-tyrant is dependent on

Polylepis

habitat, with a preference for dense woodlands.

Polylepis

habitat throughout the ash-breasted tit-tyrant's range has been and continues to be altered and destroyed as a result of human activities, including clearcutting and burning for agriculture, grazing lands, tourism, and industrialization; extractive activities, including firewood, timber, and mineral extraction; and human encroachment and concomitant increased pressure on natural resources. Researchers estimate that 1 percent of the dense woodlands preferred by the species remains, and that all remaining habitat is fragmented and degraded. The ash-breasted tit-tyrant currently occupies an area of approximately 4,595 mi

2

(11,900 km

2

) and appears to be unable to persist in forest remnants smaller than 2.5 ac (1 ha). Forest fragments in some portions of the ash-breasted tit-tyrant's range are approaching the lower threshold of the species' ecological requirements. The historical decline of habitat suitable for this 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 Peru and Bolivia continues to reduce the quantity, quality, distribution, and regeneration of remaining patches. Human activities that degrade, alter, and destroy habitat are ongoing throughout the species' range, including within protected areas (see also Factor D). Current research indicates that climate fluctuations exacerbate the risks to species that are already undergoing range reduction due to habitat alteration. Climate models predict that this species' habitat will continue to decline. Experts consider the species' population decline to be commensurate with the declining habitat (Factor E). Therefore, we find that destruction and modification of habitat are threats to the continued existence of the ash-breasted tit-tyrant throughout its range.

B. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes

We are not aware of any information currently available that indicates that overutilization of the species for commercial, recreational, scientific, or educational purposes has occurred or is occurring at this time. As a result, we are not considering overutilization to be a threat to the continued existence of the ash-breasted tit-tyrant.

C. Disease or Predation

We are not aware of any scientific or commercial information that indicate disease or predation poses a threat to this species. As a result, we are not considering disease or predation to be a

threat to the continued existence of the ash-breasted tit-tyrant.

D. Inadequacy of Existing Regulatory Mechanisms

This analysis of regulatory mechanisms is discussed on a country-by-country basis, beginning with Peru.

Peru

: The ash-breasted tit-tyrant is considered “endangered” by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276855). This Decree prohibits hunting, take, transport, and trade of protected species, except as permitted by regulation. As hunting, take, transport, and trade are not currently threats to the ash-breasted tit-tyrant (Factor B), this regulation does not mitigate any current threats to this species.

The Peruvian national protected area system includes several categories of habitat protection. Habitat may be designated as any of the following: (1) Parque Nacional (National Park, an area managed mainly for ecosystem conservation and recreation ); (2) Santuario (Sanctuary, for the preservation of sites of notable natural or historical importance); (3) Reserva Nacional (National Reserve, for sustainable extraction of certain biological resources); (4) Bosque de Proteccio

n (Protection Forest, to safeguard soils and forests, especially for watershed conservation); (5) Zona Reservada (Reserved Zone, for temporary protection while further study is under way to determine their importance); (6) Bosque Nacional (National Forest, to be managed for utilization); (7) Reserva Comunal (Communal Reserve, for local area use and management, with national oversight); and (8) Cotos de Caza (Hunting Reserve, for local use and management, with national oversight) (BLI 2008, p. 1; Rodri

guez and Young 2000, p. 330). National reserves, national forests, communal reserves, and hunting reserves are managed for the sustainable use of resources (IUCN 1994, p. 2). The designations of National Parks, Sanctuaries, and Protection Forests, are established by supreme decree that supersedes all other legal claim to the land and, thus, these areas tend to provide more habitat protection. All other protected areas are established by supreme resolution, which is viewed as a less powerful form of protection (Rodri

guez and Young 2000, p. 330).

Protected areas have been established through regulation in at least three sites occupied by the ash-breasted tit-tyrant in Peru: Parque Nacional Huascara

n (Ancash), and Santuario Histo

rico Machu Picchu (Cusco); and Zona Reservada de la Cordillera Huayhuash (spanning Ancash, Hua

nuco, and Lima) (Barrio 2005, p. 563; BLI 2009i, p. 1; BLI 2009l, p. 1; BLI 2009n, p. 1). Habitat destruction and alteration, including burning, cutting, and grazing are ongoing within Parque Nacional Huascara

n and Santuario Histo

rico Machu Picchu (BLI 2009l, p. 4; BLI 2009n, p. 2; Engblom

et al

. 2002, p. 58), where resources are supposed to be managed for conservation (Rodri

guez and Young 2000, p. 330). Reserved zones are intended to be protected pending further study (Rodri

guez and Young 2000, p. 330). However, burning for habitat conversion and maintenance of pastures for grazing and increasing ecotourism are ongoing within Zona Reservada de la Cordillera Huayhuash (Barrio 2005, p. 564). Therefore, the occurrence of the ash-breasted tit-tyrant within protected areas in Peru does not protect the species, nor does it mitigate the threats to the species from ongoing habitat loss (Factor A) and concomitant population decline (Factor E).

Recent studies by the Peruvian Society for Environmental Law (SPDA) have concluded that there are approximately 5,000 laws and regulations directly or indirectly related to environmental protection and natural resource conservation in Peru. However, many of these are not effective because of limited implementation and/or enforcement capability (Muller 2001, pp. 1-2).

Bolivia

: The 1975 Law on Wildlife, National Parks, Hunting and Fishing (Decree Law No. 12,301 1975, pp. 1-34) has the fundamental objective of protecting the country's natural resources. This law governs the protection, management, utilization, transportation, and selling of wildlife and their products; the protection of endangered species; habitat conservation of fauna and flora; and the declaration of national parks, biological reserves, refuges, and wildlife sanctuaries, tending to the preservation, promotion, and rational use of these resources (Decree Law No. 12,301 1975, pp. 1-34; eLAW 2003, p. 2). Although this law designates national protection for all wildlife, there is no information as to the actual protections this confers to ash-breasted tit-tyrants. Law No. 12,301 (1975, pp. 1-34) also placed into public trust all national parks, reserves, refuges, and wildlife sanctuaries. However, there is no specific information as to the governmental protections afforded within the protected areas to either the ash-breasted tit-tyrant or its habitat. Given the ongoing habitat destruction throughout the species' range in Bolivia, this law does not protect the species, nor does it mitigate the threats to the species from ongoing habitat loss (Factor A) and concomitant population decline (Factor E).

Bolivia passed an overarching environmental law in 1992 (Law No. 1,333 1992), with the intent of protecting and conserving the environment and natural resources. However, there is no specific legislation to implement these laws (eLAW 2003, p. 1). Therefore, we cannot determine that this law protects the species or mitigates the threats to the species from ongoing habitat loss (Factor A) and concomitant population decline (Factor E).

In Bolivia, habitat is protected either on the national or departmental level through the following designations: (1) Parque (Park, for strict and permanent protection of representative of ecosystems and provincial habitats, as well as plant and animal resources, along with the geographical, scenic and natural landscapes that contain them); (2) Santuario (Sanctuary, for the strict and permanent protection of sites that house endemic plants and animals that are threatened or in danger of extinction); (3) Monumento Natural (Natural Monument, to preserve areas such as those with distinctive natural landscapes or geologic formations, and to conserve the biological diversity contained therein); (4) Reserva de Vida Silvestre (Wildlife Reserve, for protection, management, sustainable use and monitoring of wildlife); (5) Area Natural de Manejo Integrado (Natural Area of Integrated Management, where conservation of biological diversity is balanced with sustainable development of the local population; and (6) Reserva Natural de Inmovilizacio

n (“Immobilized” Natural Reserve, a temporary (5-year) designation for an area that requires further research before any official designations can be made and during which time no natural resource concessions can be made within the area) (Supreme Decree No. 24,781 1997, p. 3). Within parks, sanctuaries and natural monuments, extraction or consumption of all resources are prohibited, except for “scientific research, eco-tourism, environmental education, and activities of subsistence of original towns, properly described and authorized.” National protected areas are under the management of the national government, while departmental protected areas are managed at the department level (eLAW 2003, p. 3; Supreme Decree No. 24,781 1997, p. 3).

The ash-breasted tit-tyrant occurs within several protected areas in the Department of La Paz, Bolivia: Parque Nacional y a

rea Natural de Manejo

Integrado Madidi, Parque Nacional y a

rea Natural de Manejo Integrado Cotapata, and the co-located protected areas of Reserva Nacional de Fauna de Apolobamba, a

rea Natural de Manejo Integrado de Apolobamba, and Reserva de la Biosfera de Apolobamba (Auza and Hennessey 2005, p. 81; BLI 2009a, p. 1; BLI 2009b, p. 1; BLI 2009c, p. 1; BLI 2009e, p. 1). Although national parks are intended to be strictly protected, the two parks in which the species occurs (Parque Nacional y a

rea Natural de Manejo Integrado Madidi and Parque Nacional y a

rea Natural de Manejo Integrado Cotapata) are also designated as areas of integrated management, which are managed for the biological conservation balanced with the sustainable development of the local population (Supreme Decree No. 24,781 1997, p. 3). Grazing and firewood extraction are ongoing within Parque Nacional y a

rea Natural de Manejo Integrado Cotapata (BLI 2009b, p. 2; BLI 2009c, p. 2). Commercial logging has occurred within Parque Nacional y a

rea Natural de Manejo Integrado Madidi (BLI 2009a, p. 2; WCMC 1998a, p. 1). Uncontrolled clearing, extensive agriculture, grazing, and “irresponsible” tourism are ongoing within the Apolobamba protected areas (Auza and Hennessey 2005, p. 81; BLI 2009e, p. 5). Habitat degradation and destruction from grazing, forest fires, and timber extraction are ongoing in other protected areas, such as Tunari National Park (Department of Cochabamba, Bolivia), where suitable habitat exists for this species (De la Vie 2004, p. 7). Therefore, the occurrence of the ash-breasted tit-tyrant within protected areas in Bolivia does not protect the species, nor does it mitigate the threats to the species from ongoing habitat loss (Factor A) and concomitant population decline (Factor E).

Summary of Factor D

Peru and Bolivia have enacted various laws and regulatory mechanisms to protect and manage wildlife and their habitats. The ash-breasted tit-tyrant is “endangered” under Peruvian law and occurs within several protected areas in Peru and Bolivia. As discussed under Factor A, the ash-breasted tit-tyrant prefers dense woodlands, which have been reduced by an estimated 99 percent in Peru and Bolivia, and the remaining habitat is fragmented and degraded. Habitat throughout the species' range has been and continues to be altered as a result of human activities, including clearcutting and burning for agriculture, grazing lands, and industrialization; extractive activities, including, firewood, timber, and mineral extraction; and human encroachment and concomitant increased pressure on natural resources. Despite the species' “endangered” status in Peru and Bolivian laws intended to protect all wildlife and natural resources, these activities are ongoing within protected areas, indicating that the laws governing wildlife and habitat protection in both countries are either inadequate or inadequately enforced to protect the species or to mitigate ongoing habitat loss (Factor A) and population declines (Factor E). Therefore, we find that the existing regulatory mechanisms are inadequate to mitigate the current threats to the continued existence of the ash-breasted tit-tyrant throughout its range.

E. Other Natural or Manmade Factors Affecting the Continued Existence of the Species

An additional factor that affects the continued existence of the ash-breasted tit-tyrant is the species' small population size. As discussed above (see Population Estimates), the global population estimate is not an accurate reflection of the species' effective population size because gene flow does not occur between the subspecies. At the same time, there is insufficient information on the subspecies or subpopulation level (in terms of numbers of individuals and breeding structure) to estimate the effective population size at the subspecies level. However, with an estimated global population size in the mid- to upper-hundreds (BLI 2000, p. 392; BLI 2007, p. 1; BLI 2009o, p. 1), and the most recent estimate of 641 individuals (Chutas 2007, pp. 4, 8; Go

mez in litt. 2007, p. 1), the ash-breasted tit-tyrant is considered to have a “very small population” size (BLI 2000, p. 392; BLI 2008, p. 1; BLI 2009o, p. 1).

Small population size renders a species vulnerable to any of several risks, including inbreeding depression, loss of genetic variation, and accumulation of new mutations. Inbreeding can have individual or population-level consequences either by increasing the phenotypic expression (the outward appearance or observable structure, function, or behavior of a living organism) of recessive, deleterious alleles (harmful gene sequences) or by reducing the overall fitness of individuals in the population (Charlesworth and Charlesworth 1987, p. 231; Shaffer 1981, p. 131). Small, isolated wildlife populations are also more susceptible to environmental fluctuations and demographic shifts (Pimm

et al

. 1988, pp. 757, 773-775; Shaffer 1981, p. 131), such as reduced reproductive success of individuals and chance disequilibrium of sex ratios. Species tend to have a higher risk of extinction if they occupy a small geographic range and occur at low density (Purvis

et al

. 2000, p. 1949).

The ash-breasted tit-tyrant population declined at a rate between 10 and 19 percent in the past 10 years, and this decline is expected to continue in close association with continued habitat loss and degradation (see Factor A) (BLI 2009o, p. 1). Extinction risk is heightened in small, declining populations by an increased vulnerability to the loss of genetic variation due to inbreeding depression and genetic drift (changes in relative frequency of gene sequences). This, in turn, compromises a species' ability to adapt genetically to changing environments (Frankham 1996, p. 1507) and reduces fitness, thus increasing extinction risk (Reed and Frankham 2003, pp. 233-234). Once a population is reduced below a certain number of individuals, it tends to rapidly decline towards extinction (Franklin 1980, pp. 147-148; Gilpin and Soule

1986, p. 25; Holsinger 2000, pp. 64-65; Soule

1987, p. 181).

Complications arising from the species' small population size are exacerbated by the species' fragmented distribution. The ash-breasted tit-tyrant is currently confined to restricted and severely fragmented forest patches in the high Andes of Peru and Bolivia (BLI 2000, p. 392; BLI 2007, pp. 1; BLI 2008, p. 1; BLI 2009o, p. 1; Collar

et al

. 1992, p. 753; Fjeldsa

and Kessler 1996, as cited in Fjeldsa

2002a, p. 113; del Hoyo

et al

. 2004, p. 281; InfoNatura 2007, p. 1) , where it is estimated that only 1 percent of the dense woodlands preferred by the species remain (Fjeldsa

2002a, p. 114; Smith 1971, p. 269) (see Habitat and Life History). Habitat fragmentation can cause genetic isolation and heighten the risks to the species associated with short-term genetic viability. Species with a small population size, combined with a restricted and severely fragmented range, are exposed to increased vulnerability to adverse natural events and manmade activities that destroy individuals and their habitat (Holsinger 2000, pp. 64-65; Primack 1998, pp. 279-308; Young and Clarke 2000, pp. 361-366).

Summary of Factor E

The ash-breasted tit-tyrant has a small population size that renders it vulnerable to genetic risks that negatively impact the species' viability. The species occurs in two disjunct

populations, where habitat is highly fragmented and continues to be altered by human activities (Factor A). The restricted and fragmented range, as well as its small population size, increases the species' vulnerability to extinction, through demographic or environmental fluctuations. Based on its small population size and fragmented distribution, we have determined that the ash-breasted tit-tyrant is particularly vulnerable to the threat of adverse natural events (e.g., genetic, demographic, or environmental) and human activities (e.g., deforestation, habitat alteration, and infrastructure development) that destroy individuals and their habitat. The genetic and demographic risks associated with small population sizes are exacerbated by ongoing human activities that continue to curtail the species' habitat throughout its range. The species' population has declined and is predicted to continue declining commensurate with ongoing habitat loss (Factor A). Therefore, we find that the species' small population size, in concert with its fragmented distribution and its heightened vulnerability to adverse natural events and manmade activities, are threats to the continued existence of the ash-breasted tit-tyrant throughout its range.

Status Determination for the Ash-Breasted Tit-Tyrant

The ash-breasted tit-tyrant, a small New World tyrant flycatcher, exists in two disjunct areas in Peru and Bolivia. Preferring dense, semihumid

Polylepis

or

Polylepis

-mixed woodlands, the ash-breasted tit-tyrant occupies a narrow range of distribution, at elevations between 12,139 and 15,092 ft (3,700 and 4,600 m). The species has a highly restricted and severely fragmented range (approximately 4,595 mi

2

(11,900 km

2

)), and is known only in two disjunct areas: one location in west-central Peru (in the Peruvian Administrative Regions of Ancash, Hua

nuco, La Libertad, and Lima) and another location ranging from southern Peru (Apuri

mac, Cusco, Puno, and Arequipa Regions) into northern Bolivia (in the Department of La Paz). The known population of the ash-breasted tit-tyrant is estimated to be 641 individuals.

We have carefully assessed the best available scientific and commercial information regarding the past, present, and potential future threats faced by the ash-breasted tit-tyrant and have concluded that there are three primary factors that threaten the continued existence of the ash-breasted tit-tyrant: (1) Habitat destruction, fragmentation, and degradation; (2) limited size and isolation of remaining populations; and (3) inadequate regulatory mechanisms.

Human activities that degrade, alter, and destroy habitat are ongoing throughout the ash-breasted tit-tyrant's range. Widespread deforestation and the conversion of forests for grazing, agriculture, and human settlement have led to the fragmentation and degradation of habitat throughout the range of the ash-breasted tit-tyrant (Factor A). Researchers estimate that only 1 percent of the dense

Polylepis

woodlands preferred by the species remain extant. Limited by the availability of suitable habitat, the species occurs today only in some of these fragmented and disjunct locations. Ash-breasted tit-tyrant habitat continues to be altered by human activities, such as burning, grazing, extractive activities, and human encroachment, which result in the continued degradation, conversion, and destruction of habitat and reduce the quantity, quality, distribution, and regeneration of remaining forest patches.

The ash-breasted tit-tyrant population is small, rendering the species particularly vulnerable to the threat of adverse natural events (e.g., genetic, demographic, or environmental) and human activities (e.g., deforestation and habitat alteration) that destroy individuals and their habitat. Ongoing human activities that curtail the species' habitat throughout its range exacerbate the genetic and demographic risks associated with small population sizes (Factor E). The population has declined 10-19 percent in the past 10 years (see Population Estimates), and is predicted to continue declining commensurate with ongoing habitat loss (Factor A). Habitat loss was a factor in the ash-breasted tit-tyrant's historical population decline (see Historical Range and Distribution), and the species is considered to be declining today in association with the continued reduction in habitat (Factors A and E). Moreover, current research indicates that narrow endemics, such as the ash-breasted tit-tyrant, are especially susceptible to climate fluctuations, because of the synergistic effect these fluctuations have on declining populations that are also experiencing range reductions due to human activities (Factor A).

Despite the species' “endangered” status in Peru and its occurrence within several protected areas in Peru and Bolivia (Factor D), human activities that degrade, alter, and destroy habitat are ongoing throughout the species' range, including within protected areas. Therefore, regulatory mechanisms are either inadequate or ineffective at curbing the threats to the ash-breasted tit-tyrant of habitat loss (Factor A) and corresponding population decline (Factor E).

Section 3 of the Act defines an “endangered species” as “any species which is in danger of extinction throughout all or a significant portion of its range” and a “threatened species” as “any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.” Based on the immediate and ongoing threats to the ash-breasted tit-tyrant throughout its entire range, as described above, we determine that the ash-breasted tit-tyrant is in danger of extinction throughout all of its range. Therefore, on the basis of the best available scientific and commercial information, we are proposing to list the ash-breasted tit-tyrant as an endangered species throughout all of its range.

II. Juni

n grebe (

Podiceps taczanowskii

)

Species Description

The Juni

n grebe is a highly social, flightless water bird in the

Podicipedidae

family that is endemic to a single location (Lake Juni

n) in Peru. Other common names for the species (in English) are: Juni

n flightless grebe, puna grebe, and Taczanowski's grebe. This species is also known by two Spanish names: “

zampulli

n del Juni

n

” or “

zambullidor de Juni

n

” (del Hoyo

et al

. 1992, p. 195; Fjeldsa

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 Juni

n grebe is about 13.78 in (35 cm) in length, and its weight ranges from 0.66 to 1.04 pounds (0.30 to 0.47 kilograms) (BLI 2009b, p. 1; UNEP-WCMC 2009, p. 1). The Juni

n 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 Juni

n 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 Juni

n grebe is endemic to the open waters and marshlands of Lake Juni

n, located at 13,390 ft (4,080 m) above sea level in the Peruvian Administrative Region of Juni

n (BLI 2003, p. 1; BLI 2009b, p. 1). The 57-mi

2

(147-km

2

) lake, also known as “

Chinchaycocha

” or “

Lago de Juni

n

,” is large but fairly shallow (BLI 2003, p. 1; BLI 2009a, p. 1; BLI 2009b, p. 1; 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 (Fjeldsa

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 watermilfoil (

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 Fjeldsa

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

) (Fjeldsa

1981, pp. 244, 246). Both cattail species can reach nearly 6.6 ft (2 m) 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 (BLI 2009b, p. 1; ParksWatch 2009, p. 2).

Lake Juni

n 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 altitude, aquatic birds, and local endemic species, such as the Juni

n grebe and the Juni

n rail (

Laterallus tuerosi

; also the subject of this proposed 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 (Fjeldsa

1981, pp. 44, 246; O'Donnel and Fjeldsa

1997, p. 29). The Juni

n grebe nests in the protective cover of the marshlands during the breeding season (Fjeldsa

1981, p. 247; Tello 2007, p. 3), 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 (Fjeldsa

1981, p. 245). The species is believed to have a deferred sexual maturation (Fjeldsa

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). Juni

n grebes occasionally produce a replacement clutch if their original nest is disturbed (Fjeldsa

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 Juni

n grebe is likely a long-lived species (Fjeldsa

2004, p. 201), and its breeding success and population size are highly influenced by the climate (BLI 2008, pp. 1, 3-4; BLI 2009b, p. 2; Elton 2000, p. 3; Fjeldsa

2004, p. 200; Hirshfeld 2007, p. 107) (see Factor A).

The Juni

n 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 (Fjeldsa

1981, pp. 247-248; Tello 2007, p. 3). Fish (primarily pupfish (

Orestias

spp.)) account for over 90 percent of the grebe's diet (Fjeldsa

1981, pp. 251-252). Pupfish become scarce when the marshlands dry during periods of reduced water levels, and the Juni

n 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 Juni

n grebe was historically known to be endemic to Lake Juni

n, in the Peruvian Administrative Region of Juni

n (Fjeldsa

1981, p. 238; Fjeldsa

2004, p. 200; Fjeldsa

and Krabbe 1990, p. 70; INRENA 1996, p. 1). Experts believe that the species was previously distributed throughout the entire 57-mi

2

(147-km

2

) lake (BLI 2003, p. 1; BLI 2009a, p. 1; Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200). In 1938, the Juni

n grebe was encountered throughout the entire lake (Morrison 1939, p. 645). The Juni

n grebe is now absent from the northwest portion of Lake Juni

n due to mine waste contamination and a severe decline in population (Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200).

Current Range and Distribution

The Juni

n grebe continues to be endemic to the 57-mi

2

(147-km

2

) Lake Juni

n, located at 13,390 ft (4,080 m) above sea level in the Peruvian High Andes (BLI 2003, p. 1; BLI 2009a, p. 1; BLI 2009b, p. 1). Although BirdLife International (2009b, p. 1) reports the current estimated range of the species as 55 mi

2

(143 km

2

), their definition of a species' range is the total area within its extent of occurrence (see Current Range and Distribution of the ash-breasted tit-tyrant) (BLI 2000, pp. 22, 27). Noting that Lake Juni

n is only a 57-mi

2

(147-km

2

) lake (BLI 2003, p. 1; BLI 2009a, p. 1) and that the Juni

n grebe is restricted to the southern portion of the lake (Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200), its current range is actually smaller than the figure reported by BirdLife International. The entire population of this species is located within a protected area, the Juni

n National Reserve (BLI 2008, p. 2; BLI 2009a, p. 1; BLI 2009b, p. 1; ParksWatch 2009, p. 4).

Population Estimates

The current population of the Juni

n 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 (Fjeldsa

1981, p. 254). Field studies in 1938 indicated that the Juni

n grebe was “extremely abundant” throughout Lake Juni

n (Morrison 1939, p. 645). Between 1961 and 1979 the population fell from greater 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 Fjeldsa

1997, p. 30; Fjeldsa

1981, p.

254). Surveys during the mid-1980s estimated a total of 250 individuals inhabiting the southern portion of Lake Juni

n (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 Juni

n grebes were present on Lake Juni

n (O'Donnell and Fjeldsa

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; T. Valqui in litt., as cited in BLI 2009b, p. 2). In 1998, more than 250 Juni

n grebes were counted in a 1.5-mi

2

(4-km

2

) area in the southern portion of Lake Juni

n, suggesting a total population of 350 to 400 birds (T. 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 overly optimistic (Fjeldsa

in litt. 2003, as cited in BLI 2009b, p. 2). Fjeldsa

(in litt. 2003, as cited in BLI 2009b, p. 2) postulated that perhaps only half that number would have been mature individuals. These population fluctuations are strongly linked to precipitation (see Factor A).

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

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200) (See Factors, A, C, and E).

Conservation Status

The Juni

n grebe is considered “critically endangered” by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276853). The IUCN categorizes the Juni

n 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 2008, p. 1; BLI 2009b, pp. 1, 3). The single known population of the Juni

n grebe occurs wholly within one protected area in Peru, the Juni

n National Reserve (BLI 2009b, pp. 1-2).

Summary of Factors Affecting the Juni

n Grebe

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

The Juni

n grebe is endemic to Lake Juni

n, 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 2008, p. 1; BLI 2009a, p. 1; Fjeldsa

1981, p. 247; Tello 2007, p. 3). The current estimated range of the species is 55 mi

2

(143 km

2

) (BLI 2009b, p. 1). However, as described under Current Range and Distribution, its actual range is smaller, because the species is restricted to the southern portion of the lake (BLI 2009b, p. 1; Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200). Breeding season begins in November (Fjeldsa

1981, pp. 44, 246; O'Donnel and Fjeldsa

1997, p. 29). Juni

n grebes build their nests (BLI 2008, p. 1; Fjeldsa

1981, p. 247; Tello 2007, p. 3) and obtain their primary prey, pupfish, in the expansive offshore flooded marshlands that may extend into the lake up to 1-3 mi (2-5 km) from shore (Fjeldsa

2004, p. 200; O'Donnel and Fjeldsa

1997, pp. 29-30).

The quality of Juni

n grebe habitat and the species' reproductive success is highly influenced by water levels and the water quality of the lake. Water levels in the lake are affected by manmade activities (such as hydropower generation) that are exacerbated by unpredictable climate fluctuations (such as drought or excessive rain). Water quality in Lake Juni

n has been compromised by contamination.

The Upamayo Dam, located at the northwest end of the lake, has been in operation since 1936, and lake water is used to power the 54-megawatt Malpaso hydroelectric plant (Martin

et al

. 2001, p. 178; ParksWatch 2006, p. 5). Dam operations have caused seasonal water level fluctuations of as much as 6 ft (2 m) in Lake Juni

n (Martin and McNee 1999, p. 659). Under normal conditions, water levels are lower in the dry season and the marshlands can become partially or completely dry (BLI 2009b, p. 1; ParksWatch 2009, p. 2). The floodgates of the dam are often opened during the dry season (June to November) (BLI 2009b, p. 1; 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 (Fjeldsa

2004, p. 123).

Reduced water levels directly impact the Juni

n grebe's breeding success, by reducing the amount of available nesting habitat (BLI 2008, p. 1; Fjeldsa

2004, p. 200). The giant bulrush marshlands, upon which the Juni

n grebe relies for nesting and foraging habitat, have virtually disappeared from some sections of the lake (O'Donnel and Fjeldsa

1997, p. 29). When the marshlands are completely desiccated, the Juni

n grebe does not breed at all (Fjeldsa

2004, p. 123).

Reduced water levels also impact the species by reducing the Juni

n grebe's primary prey, pupfish (Fjeldsa

2004, p. 200) (see Habitat and Life History). The perimeter of the flooded marshlands provides the primary recruitment habitat for fish in the lake during extremely dry years, including 1983-1987, 1991, and 1994-1997 (Fjeldsa

2004, p. 200; O'Donnel and Fjeldsa

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 requirements of the Upamayo Dam, and the giant bulrushes that previously grew tall and provided extensive cover for this species for breeding and feeding have virtually disappeared, reducing both nesting and foraging habitat for the Juni

n grebe. The reduction in nesting and foraging habitat are believed to contribute to mass mortality of Juni

n grebes during extreme drought years (O'Donnel and Fjeldsa

1997, p. 30).

Manipulation of the Lake Juni

n's water levels also results in competition between the white-tufted grebe (

Rollandia rolland

) and the Juni

n grebe for food resources during the Juni

n grebe's breeding season (Fjeldsa

2004, p. 200). Under normal conditions, the expansive offshore marshlands may extend into the lake up to 1-3 mi (2-5 km) from shore (O'Donnel and Fjeldsa

1997, p. 29). In years when water levels remain high, the Juni

n grebe and white-tufted grebe are spatially segregated during the breeding season, with white-tufted grebes utilizing the interior of the reed marsh and Juni

n grebes remaining at the edges of the marshlands, closer to the center of the lake (Fjeldsa

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 Juni

n grebe for food

(Fjeldsa

1984, pp. 413-414). As the breeding season for the Juni

n grebe begins in November (Fjeldsa

1981, pp. 44, 246; O'Donnel and Fjeldsa

1997, p. 29), Juni

n grebes build floating nests and breed on the margins of marshlands (BLI 2008, p. 1; Fjeldsa

1981, p. 247; Tello 2007, p. 3), and a plentiful supply of fish becomes more important (O'Donnel and Fjeldsa

1997, p. 29). 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 accentuate this competition (Fjeldsa

1981, pp. 252-253).

Water quality affects the availability of habitat for the endemic Juni

n grebe. The water in Lake Juni

n has been contaminated from mining waste, agricultural runoff, and organic matter from the land surrounding the lake. There are several mining operations (lead, copper, and zinc) north of Lake Juni

n, and wastewater from the mines flows untreated into the lake via the Ri

o San Juan (Fjeldsa

1981, p. 255; Martin and McNee 1999, pp. 660-661; ParksWatch 2006, p. 2; Shoobridge 2006, p. 3). Agricultural insecticides wash into Lake Juni

n from surrounding fields and through drainage systems from villages around the lake (ParksWatch 2006, pp. 5, 19). Organic matter originating from local communities is piped untreated into the lake, resulting in eutrophication (a process whereby excess nutrients facilitate excessive plant growth, which ultimately reduces the amount of dissolved oxygen in the water, harming oxygen-dependent organisms) (ParksWatch 2006, p. 5; Shoobridge 2006, p. 3).

Lake Juni

n is a sink for several streams that transport mining wastes and other pollution downstream and into the lake (ParksWatch 2006, p. 19). The Ri

o San Juan is the primary source of water for Lake Juni

n and feeds into the lake from the northern end (Fjeldsa

1981, p. 255; Martin and McNee 1999, pp. 660-661; Shoobridge 2006, p. 3). Tests indicate that the Ri

o San Juan 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 visible near the outflow of the Ri

o San Juan because iron oxide produces a reddish tinge to the water and reed borders. Vegetation near the river's outflow is completely absent (Fjeldsa

2004, p. 124; ParksWatch 2006, pp. 20-21), 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 and upon which the Juni

n grebe relies for nesting and foraging habitat, have virtually disappeared and at least one species of catfish (

Pygidium oroyae

) may have been extirpated from the lake (O'Donnel and Fjeldsa

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 Juni

n grebe is now restricted (BLI 2003, p. 1; BLI 2009b, p. 1; Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200). Near the center of the lake, the bottom has been described as “lifeless,” due to sedimentation of iron oxides (Fjeldsa

1981, pp. 255-256; Fjeldsa

2004, p. 124). Martin

et al

. (2001, p. 180) determined that sediments at the lake's center are enriched with copper, zinc, and lead and are anoxic (having low levels of dissolved oxygen). High concentrations of dissolved copper, lead, and zinc have damaged an estimated one-third of the lake, increasing turbidity of the lake, and exceeding established aquatic life thresholds (Martin and McNee 1999, pp. 660-661; ParksWatch 2006, pp. 2, 20; Shoobridge 2006, p. 3). This has severely affected animal and plant populations in the area, contributing to mortality of species, including the Juni

n grebe, around the lake (ParksWatch 2006, pp. 3, 20) (see Factor C).

In 2009, conservation organizations and civil society groups demanded action to reverse the deterioration of Lake Juni

n and requested an independent environmental audit and continuous monitoring of the lake (BLI 2009b p. 4; BLI 2009c, p. 1). The conservation groups BLI, American Bird Conservancy (ABC), Asociacio

n Ecosistemas Andinos (ECOAN), and INRENA adopted the Juni

n grebe as the symbol of wetland conservation for the high Andes (BLI 2009c, p. 1). Although translocation has been a consideration for the conservation of the Juni

n grebe since the mid-1990s, no suitable habitat for the species has been located (O'Donnel and Fjeldsa

1997, pp. 30, 35; BLI 2008, p. 5; BLI 2009b, p. 2). None of these conservation organization's activities have been effective at curbing the ongoing habitat degradation (see also Factor D).

The effects of habitat alteration and destruction (such as those caused by artificially reduced water levels and water contamination) 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). Peru is subject to unpredictable climate fluctuations, such as those that are related to the El Niño Southern Oscillation (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); thereby exacerbating the effects of habitat reduction and alteration on the decline of a species (England 2000, p. 86; Holmgren

et al

. 2001, p. 89; Jetz

et al

. 2007, pp. 1211, 1213; Mora

et al

. 2007, p. 1027; Parmesan and Mathews 2005, p. 334; Plumart 2007, pp. 1-2; Timmermann 1999, p. 694), especially for narrow endemics (Jetz

et al

. 2007, p. 1213) such as the Juni

n grebe (see also Factor E). Moreover, the Juni

n 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 Juni

n 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 population has declined to 100 birds or less following particularly dry years (BLI 2008, pp. 1, 3-4; BLI 2009b, p. 2; Elton 2000, p. 3; Fjeldsa

2004, p. 200). 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) (PROFONANPE 2002, as cited in Fjeldsa

2004, p. 133; T. Valqui pers. comm., as cited in BLI 2009b, p. 2). However, excessive rains also increase contamination in Lake Juni

n, which decreases the amount of suitable habitat for the species (as described above) and has adverse effects on the species' health (see Factor C). Many Juni

n 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). 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 will 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 species' historical decline (Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200). The species has experienced a population decline of 14 percent in the past 10 years, and is expected to continue to decline 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 size (see Factor E).

Summary of Factor A

The habitat in and around Lake Juni

n, where the Juni

n grebe is endemic, has been and continues to be altered and degraded as a result of human activities, including artificial water level fluctuations to generate hydropower and water contamination caused by mining waste, agricultural and organic runoff from surrounding lands, and wastewater from local communities. The Juni

n grebe is dependent on the quantity and quality of lake water for breeding and feeding. Water levels in Lake Juni

n are manipulated to generate electricity, which leads to dramatic fluctuations in water levels of up to 6 ft (1.8 m). The Juni

n grebe relies on the protective cover of flooded marshlands for nesting. As water drawdown occurs near the end of the dry season and the inception of the Juni

n grebe's mating season, portions of the marshlands may dry out completely. Reductions in water levels decrease the availability of suitable breeding and foraging habitat, and decrease the availability of the Juni

n grebe's primary prey, forcing competition with the white-tufted grebe for food. Drought years have a negative impact on the Juni

n grebe, resulting in severe population fluctuations due to poor breeding success and limited recruitment of juveniles into the adult population. Severed dry conditions can cause total breeding failure (see also Factor E).

Although the population appears to rebound during wetter years (i.e., following El Niño events) (see Habitat and Life History and Population Estimate), excessive rain decreases the suitable habitat for the species, as pollution washes into the water from around the lake and the upstream rivers that feed the lake, increasing contamination levels in Lake Juni

n. This increased contamination also affects the Juni

n grebe's health and has resulted in mortality of the species (see Factor C). Severe water contamination has rendered the northwest portion of the lake lifeless, devoid of aquatic and terrestrial species. Experts believe that the Juni

n grebe once inhabited the entire Lake, but the species is now confined to the southern portion of the lake due to water contamination (Historical Range and Distribution). Elevated levels of heavy metals may reduce the fitness and overall viability of the Juni

n grebe (Factor C), which would heighten risks associated with short- and long-term genetic viability (Factor E). Therefore, we find that destruction and modification of habitat are threats to the continued existence of the Juni

n grebe throughout its range.

B. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes

We are not aware of any information currently available that indicates that overutilization of Juni

n grebe for commercial, recreation, scientific, or education purposes has occurred or is occurring at this time. Fjeldsa

(1981, pp. 254-255) notes that local hunters are not interested in grebes as food because they have “too little meat.” As a result, we are not considering overutilization to be a threat to the continued existence of the Juni

n grebe.

C. Disease or Predation

Disease: Although no specific disease threat has been identified for the Juni

n grebe, contamination of Lake Juni

n has contributed directly and indirectly to Juni

n grebe mortality and has potentially reduced the overall fitness and health of the species. As discussed under Factor A, lead, copper, and zinc mining residues (Fjeldsa

1981, p. 255; Martin and McNee 1999, pp. 660-661; Shoobridge 2006, p. 3), agricultural runoff, organic matter, and wastewater are discharged directly into Lake Juni

n (ParksWatch 2006, pp. 5, 19; Shoobridge 2006, p. 3). High concentrations of environmental contaminants (including ammonium, copper, iron oxide, lead, mercury, nitrate, and zinc) have been detected throughout the lake (Fjeldsa

1981, pp. 255-256; Fjeldsa

2004, p. 124; Martin and McNee 1999, pp. 660-662; ParksWatch 2006, pp. 20-21) and exceed established thresholds for aquatic life (Martin and McNee 1999, pp. 660-661; ParksWatch 2006, p. 20). Chemical waste has rendered the northern portion of the lake lifeless due to eutrophication (BLI 2008, p. 4; Shoobridge 2006, p. 3) and the sediments in the center of the lake anoxic (containing no dissolved oxygen) (Martin

et al

. 2001, p. 180). High concentrations of suspended particulate matter increases the turbidity of the water, making it less penetrable to sunlight and resulting in die-off of aquatic plants and algae (ParksWatch 2006, p. 20). Chemical waste has damaged at least one third of the lake and has severely affected animal and plant populations in the area (O'Donnel and Fjeldsa

1997, p. 29; ParksWatch 2006, pp. 3, 20; Shoobridge 2006, p. 3). The northern portion of the lake is completely devoid of vegetation (Fjeldsa

2004, p. 124; ParksWatch 2006, pp. 20-21), and the giant bulrush marshlands, which once existed in great expanses around the entire perimeter of the lake and upon which the Juni

n grebe relies for nesting and foraging habitat, have virtually disappeared. At least one species of catfish (

Pygidium oroyae

) may have been extirpated from the lake (O'Donnel and Fjeldsa

1997, p. 29). During years of heavy rainfall, the lake is filled, and the lakeshore becomes polluted with “toxic acid gray sediment” that has caused large-scale mortality of cattle (approximately 2,000 in 1994) and birds, apparently due to lead poisoning (O'Donnel and Fjeldsa

1997, p. 30). Lead poisoning from the presence of mine wastes is a common cause of mortality in waterbirds, and is medically described as an intoxication resulting from absorption of hazardous levels of lead into body tissues (Friend and Franson 1999, p. 317).

Water contamination has directly affected the health of the Juni

n grebe population. As predators of aquatic organisms, the Juni

n grebe occupies a mid-tertiary level position in the food chain and is prone to bioaccumulation of pesticides, heavy metals, and other contaminants that are absorbed or ingested by its prey (Fjeldsa

1981, pp. 255-256; Fjeldsa

2004, p. 123). Green plants form the first trophic, or feeding, level; they are the primary producers. Herbivores form the second trophic level, while carnivores form the third and even fourth trophic levels (The University of the Western Cape 2009, p. 1). Moreover, species such as the Juni

n grebe, which inhabit high trophic levels, are strictly dependent upon the functioning of a multitude of ecosystem processes. The loss or absence of species at lower trophic levels can result in cascading ecosystem effects, causing imbalances in the food web at all higher trophic levels (The University of the Western Cape 2009, p. 1). In parts of the lake, increased turbidity has caused die-off of aquatic plants and algae, disrupting the food chain (ParksWatch 2006, p. 20). Studies indicate that lead mining effluents severely reduce or eliminate primary prey populations of

fish and aquatic invertebrates, either directly through lethal toxicity, or indirectly through toxicity to their prey species (Demayo

et al

. 1982, as cited in Eisler 1988, p. 5). Analysis of feathers and bone tissue of Juni

n grebes and of pupfish, the species' primary prey, indicate that both the grebe and its prey contain elevated lead levels (Fjeldsa

1981, pp. 255-256).

Drought conditions exacerbate the effects of water contamination and bioaccumulation of contaminants in aquatic species. From 1989 to 1992, an extensive drought occurred in the Lake Juni

n area. During that time, many dead Juni

n grebes and other waterbirds were found along the edges of the lakeshore (T. Valqui and J. Barrio in litt. 1992, as cited in Collar

et al

. 1992, p. 45, 190). In 1992, one of the driest years in decades, up to 10 dead grebes per month were reported around the lake. Three Juni

n grebe carcasses were found along 1.2 mi (2 km) of shoreline in one month alone (T. Valqui and J. Barrio in litt. 1992, as cited in Collar

et al

. 1992, p. 45). Experts consider the cause of death to have been either heavy metal contamination, which increased in concentration as water levels decreased (T. Valqui and J. Barrio in litt. 1992, as cited in Collar

et al

. 1992, p. 45), or reduced prey availability (Fjeldsa

2004, p. 124). Reduced prey availability is exacerbated by manmade activities that are reducing the water levels of the lake, increasing competition among sympatric grebe species (different species that occupy the same range) and decreasing the marshlands that provide primary spawning habitat for the pupfish, the grebe's primary prey species (Factor A).

Persistent exposure to contaminants can contribute to a decline in fitness for long-lived, mid-trophic level species, which is inherited by offspring and can impact embryonic development, juvenile health, or viability (Rose 2008, p. 624). The excessive contaminant load in Lake Juni

n could also allow opportunistic bacterial and viral infections to overcome individuals. According to Fjeldsa

(1981, p. 254), the Juni

n grebe bears a heavy infestation of stomach nematodes (parasitic roundworms), especially as compared to other grebe species. Stomach contents of Juni

n grebes that have been examined had an average of 16.7 nematodes, compared with no nematodes in silver grebes and 1.6 nematodes in white-tufted grebes. Fjeldsa

(1981, p. 254) postulates that the higher nematode infestation in Juni

n grebes may be an indicator of poor health.

Predation: Predators around Lake Juni

n include the Andean fox (

Pseudalopex culpaues

), the long-tailed weasel (

Mustela frenata

), Pampas cat (

Onicifelis colocolo

), and hog-nosed skunk (

Conepatus chinga

) (ParksWatch 2009, p. 4). However, nest sites of the Juni

n grebe are generally inaccessible to mammalian predators (Fjeldsa

1981, p. 254). The only raptor likely to take a grebe on Lake Juni

n is the Cinereus harrier (

Circus cinereus

), which primarily feeds in white-tufted grebe habitats. Moorhens (

Gallinula chloropus

), which also inhabit the lake (ParksWatch 2009, p. 3; Tello 2007, p. 2), are egg stealers and may steal Juni

n grebe eggs for food (Fjeldsa

1981, p. 254). However, there is no direct evidence of predation upon the Juni

n grebe.

Summary of Factor C

Environmental contamination poses direct and indirect threats to the Juni

n grebe's overall health and survival. The species' trophic level also exposes it to bioaccumulation of toxins accumulated in the tissue of prey species. Research indicates that the species has elevated lead levels and carries a high load of nematodes, a possible indicator of overall poor health. Juni

n grebes have died as a direct result of contaminant poisoning or reduction in the pupfish, which has also been found to carry elevated lead levels. Therefore, we find that disease is a threat to the continued existence of the Juni

n grebe. However, there is no available evidence to indicate that predation is causing declines in Juni

n grebe populations or otherwise contributing to the species' risk of extinction. Therefore, we find that predation is not a threat to the Juni

n grebe.

D. Inadequacy of Existing Regulatory Mechanisms

The Juni

n grebe is listed as “critically endangered” by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276853). This Decree prohibits hunting, take, transport, and trade of protected species, except as permitted by regulation. As hunting, take, transport, and trade do not currently threaten the Juni

n grebe, this regulation does not mitigate any current threats to this species.

Peru has several categories of national habitat protection, which were described above as part of the Factor D analysis for the ash-breasted tit-tyrant (BLI 2008, p. 1; IUCN 1994, p. 2; Rodri

guez and Young 2000, p. 330). The Juni

n grebe population occurs wholly within one protected area: the Juni

n National Reserve (Juni

n, Peru) (BLI 2009b, pp. 1-2). The Juni

n National Reserve has an area of 133,437 ac (53,000 ha), bordering Lake Juni

n and its adjacent territories (Wege and Long 1995, p. 264). In Peru, National Reserves are also created for the sustainable extraction of certain biological resources (BLI 2008, p. 1; Rodri

guez and Young 2000, p. 330). Established in 1974, through Supreme Decree No. 0750-74-AG, the stated objectives of the Juni

n National Reserve include: integrated conservation of the local ecosystem, its associated flora and wildlife; preservation of the scenic beauty of the lake; and support of socioeconomic development in the area through the sustainable use of its renewable natural resources (BLI 2009a, p. 2; Hirshfeld 2007, p. 107). Most of the lakeshore is designated a “Direct Use Zone,” which allows fishing, grazing, and other educational, research, and recreational activities (ParksWatch 2006, p. 12). Although designation of this reserve has heightened awareness of the ecological problems at Lake Juni

n (BLI 2009c, p. 1), it has not reduced or eliminated the primary threats to the Juni

n grebe: water fluctuations and contamination (Factor A), contamination resulting in poor health (Factor C), and small population size (Factor E). Therefore, the existence of this species within a protected area has not reduced or mitigated the threats to the species.

The Juni

n National Reserve was designated a Ramsar site under the Convention on Wetlands of International Importance (Ramsar Convention) in 1997 (BLI 2009a, p. 2; Hirshfeld 2007, p. 107; INRENA 1996, pp. 1-14). The Ramsar Convention, signed in Ramsar, Iran, in 1971, is an intergovernmental treaty which provides the framework for national action and international cooperation for the conservation and wise use of wetlands and their resources. There are presently 159 Contracting Parties to the Convention (including Lake Juni

n), with 1,874 wetland sites, totaling more than 457 million ac (185 million ha), designated for inclusion in the Ramsar List of Wetlands of International Importance (Ramsar 2009, p. 1). Peru acceded to Ramsar in 1992. It has 13 sites on the Ramsar list, comprising 16.8 million ac (6.8 million ha) (Ramsar 2009, p. 5). In an examination of 5 Ramsar sites, experts noted that Ramsar designation may provide nominal protection (protection in name only) by increasing both international awareness of a site's ecological value and stakeholder involvement in conservation (Jellison

et al

. 2004, pp. 1, 4, 19). However, activities that negatively impact the Juni

n grebe are

ongoing within this Ramsar wetland, including water fluctuations and contamination (Factor A), contamination resulting in poor health (Factor C), and small population size (Factor E). Therefore, the Ramsar designation has not mitigated the impact of threats on the Juni

n grebe.

In 2002, the Peruvian Government passed an emergency law to protect Lake Juni

n. This law makes provisions for the cleanup of Lake Juni

n, and places greater restrictions on extraction of water for hydropower and mining activities (J. Fjeldsa

in litt. 2003, as cited in BLI 2007, p. 3). However, this law has not been effectively implemented, and conditions around the lake may even have worsened after passage of this law (BLI 2009c, p. 1). The Ministry of Energy and Mining has implemented a series of Environmental Mitigation Programs (PAMA) to combat mine waste pollution in the Juni

n National Reserve (ParksWatch 2006, p. 21; ParksWatch 2009 p. 3). The PAMAs were scheduled to have been completed by 2002, but extensions have been granted, indicating that many of the mines currently in operation are still functioning without a valid PAMA. Reductions in pollution are reported because some mine companies have begun to utilize drainage fields and recycle residual water. However, analysis of existing PAMAs indicate that they do not address specific responsibilities for mining waste discharged into the Ri

o San Juan and delta, nor do they address deposition of heavy metal-laced sediments in Lake Juni

n (ParksWatch 2006, p. 21; ParksWatch 2009, p. 3). Recent information indicates that mining waste contamination in the lake continues to be a source of pollution (ParksWatch 2006, pp. 20-21; Fjeldsa

2004, p. 124; BLI 2009b, p. 1). Therefore, this law is not effective at mitigating the threat of habitat degradation (Factor A), health issues associated with contamination (Factor C) and small population size of the species (Factor E).

There are approximately 5,000 laws and regulations directly or indirectly related to environmental protection and natural resource conservation in Peru. Recent studies by the Peruvian Society for Environmental Law (SPDA) have concluded that many of these are not effective because of limited implementation and/or enforcement capability (Muller 2001, pp. 1-2).

Summary of Factor D

Peru has enacted various laws and regulatory mechanisms for the protection and management of wildlife and their habitats. The Juni

n grebe is “critically endangered” under Peruvian law, and its entire population occurs within one protected area. As discussed under Factor A, the Juni

n grebe's distribution, breeding success and recruitment, and food availability on Lake Juni

n has been curtailed, and are negatively impacted due to habitat destruction that is caused by artificial water fluctuations and water contamination from human activities. These habitat-altering activities are ongoing throughout the species' range, which is wholly encompassed within one protected area. Thus, despite the species' critically endangered status and presence within a designated protected area, laws governing wildlife and habitat protection in Peru are inadequately enforced or ineffective at protecting the species or mitigating ongoing habitat degradation (Factor A), impacts from contaminants, and concomitant population declines (Factor E). Therefore, we find that the existing regulatory mechanisms are inadequate to mitigate the threats to the continued existence of the Juni

n grebe throughout its range.

E. Other Natural or Manmade Factors Affecting the Continued Existence of the Species

An additional factor that affects the continued existence of the Juni

n grebe is the species' small population size. The current population of the Juni

n grebe is estimated to be 100-300 individuals, however, only an “extremely small number of adults remain” (BLI 2008, p. 1; BLI 2009b, pp. 1, 3). The number of adults in a population are important because these individuals contribute to the next generation (Shaffer 1981, pp. 132-133; Soule

1980, pp. 160-162). The Juni

n grebe underwent a severe population decline in the latter half of the 20th century, with extreme population fluctuations (Fjeldsa

1981, p. 254) (see Population Estimates). For example, in 1993, the population size declined to below 50 individuals, of which fewer than half were breeding adults (BLI 2008, p. 3; BLI 2009b, p. 2). Even if the estimate of 100-300 individuals is correct, the number of mature individuals is likely to be far smaller, perhaps only half (Fjeldsa

in litt. 2003, as cited in BLI 2009b, p. 2). Therefore, 100-300 individuals overestimates the species' effective population size (the number of breeding individuals that contribute to the next generation) (Shaffer 1981, pp. 132-133; Soule

1980, pp. 160-162).

Small population size renders species vulnerable to genetic risks that can have individual or population-level genetic consequences, such as inbreeding depression, loss of genetic variation, and accumulation of new mutations, and may affect the species' viability by increasing its susceptibility to demographic shifts or environmental fluctuations, as explained in more detail above in the Factor E analysis for the ash-breasted tit-tyrant (Charlesworth and Charlesworth 1987, p. 238; Pimm

et al

. 1988, pp. 757, 773-775; Shaffer 1981, p. 131). Small population size also leads to a higher risk of extinction and, once a population is reduced below a certain number of individuals, it tends to rapidly decline towards extinction (Frankham 1996, p. 1507; Franklin 1980, pp. 147-148; Gilpin and Soule

1986, p. 25; Holsinger 2000, pp. 64-65; Purvis

et al

. 2000, p. 1949; Reed and Frankham 2003, pp. 233-234; Soule

1987, p. 181). In addition, species that inhabit a small geographic range, occur at low density, occupy a high trophic level, and exhibit low reproductive rates tend to have a higher risk of extinction than species that are not limited by the same risk factors (Purvis

et al

. 2000, p. 1949).

Complications arising from the species' small population size are exacerbated by the species' restricted range and threat of disease (Factor C). The Juni

n grebe is known only from a single Andean lake, Lake Juni

n, in central Peru (BLI 2000, p. 45; BLI 2009b, p. 1; Collar

et al

. 1992, p. 43). Although the species was believed to have been previously distributed throughout the entire 57-mi

2

(147-km

2

) lake (Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200; Morrison 1939, p. 645), it is now restricted to the southern portion of Lake Juni

n (BLI 2009b, p. 1; Fjeldsa

1981, p. 254; F. Gill and R.W. Storer, pers. comm. as cited in Fjeldsa

2004, p. 200). The population has declined by at least 14 percent in the last 10 years and is expected to continue to decline, as a result of declining water quality and extreme water level fluctuations (BLI 2009b, pp. 1, 4, 6-7) (Factor A). We consider that the risks associated with small population size will continue to impact this species and may accelerate, if habitat destruction continues unabated. Environmental contamination poses direct and indirect threats to the Juni

n grebe's overall health and survival, including the presence of toxins in both the Juni

n grebe and its primary prey species and mass die-offs that are linked to contamination or reduction in prey species (Factor C). A species' small population size, combined with its restricted range and threat of disease, increases the species'

vulnerability to adverse natural events and manmade activities that destroy individuals and their habitat (Holsinger 2000, pp. 64-65; Primack 1998, pp. 279-308; Young and Clarke 2000, pp. 361-366).

Summary of Factor E

The Juni

n grebe has a small population size that renders it vulnerable to genetic risks that negatively impact the species' long-term viability and, possibly, its short-term viability. The species has a restricted range and occurs in habitat that continues to undergo degradation and curtailment due to human activities (Factor A). Environmental contaminants have caused die-offs of the species and have likely reduced the overall general health of the Juni

n grebe population (Factor C). The small population size, as well as its restricted range and health issues associated with contamination, increases the species' vulnerability to extinction, through demographic or environmental fluctuations. Based on its small population size, restricted range, and threat of disease, we have determined that the Juni

n grebe is particularly vulnerable to the threat of adverse natural events (e.g., genetic, demographic, or environmental) and human activities (e.g., water level manipulation) that destroy individuals and their habitat. The genetic and demographic risks associated with small population sizes are exacerbated by ongoing human activities that continue to curtail the species' habitat throughout its range. The species' population has declined and is predicted to continue declining due to an ongoing reduction in water quality and extreme water level fluctuations (Factor A). Therefore, we find that the species' small population size, in concert with its restricted range, threat of disease, and its heightened vulnerability to adverse natural events and manmade activities, are threats to the continued existence of the Juni

n grebe throughout its range.

Status Determination for the Juni

n Grebe

The Juni

n grebe, a flightless grebe, is endemic to Lake Juni

n, found at 13,390 ft (4,080 m) above sea level in Peru, where it resides year-round. The species relies on the open waters and marshland margins of the lake for feeding and on the protective cover of the marshland margins for nesting during the breeding season. The species has a highly restricted range (approximately 55 mi

2

(143 km

2

)) and is currently known only in one location in central Peru. The species' population size is estimated as 100-300 individuals, although the number of mature individuals may be limited to half this amount.

We have carefully assessed the best available scientific and commercial information regarding the past, present, and potential future threats faced by the Juni

n grebe and have concluded that there are four primary factors that threaten the continued existence of the Juni

n grebe: (1) Habitat destruction, fragmentation, and degradation; (2) disease; (3) limited size and isolation of remaining populations; and (4) inadequate regulatory mechanisms.

Human activities that degrade, alter, and destroy habitat are ongoing throughout the Juni

n grebe's range. Lake waters are artificially manipulated to produce hydropower, resulting in reductions in water levels that impact the species' nesting and foraging sites. Manipulation of water levels for hydropower production reduces prey populations, causes increased food competition with white-tufted grebes, and results in the abandonment of breeding in drought years. Reduced water levels have permanently destroyed segments of giant bulrush communities, compromising the amount of suitable flooded marshland available for nesting (Factor A). Mining, agricultural, and organic materials have contaminated the water, causing eutrophication and anoxia in portions of the lake and the accumulation of trace minerals in lake bottom sediments. This has had direct effects on the Juni

n grebe, destroying habitat in the northwest portion of the lake so that the species' range is restricted to only the southern portion of Lake Juni

n and causing Juni

n grebe mortality during times of drought (Factors A and C). Contaminants have also reduced or eliminated submerged and emergent vegetation throughout the lake, decreasing pupfish spawning habitat and reducing prey availability (Factor A).

Juni

n grebe habitat continues to be altered by human activities, conversion, and destruction of habitat, which reduce the quantity, quality, distribution, and regeneration of habitat available for the Juni

n grebe on Lake Juni

n. Habitat loss was a factor in the Juni

n grebe's historical population decline (see Historical Range and Distribution). Population declines have been correlated with water availability, and droughts have caused severe population fluctuations that have likely compromised the species' long-term viability. The Juni

n grebe population is small, rendering the species vulnerable to the threat of adverse natural (e.g., genetic, demographic) and human activity (e.g., water extraction and contaminants from mining) events that destroy individuals and their habitat. (Factor E). The Juni

n grebe's reproductive success and life cycle relies on the availability of sufficient water in Lake Juni

n. During drought years, nesting and reproduction decline.

Although the population appears to rebound during wetter years (such as following excessive rains from El Niño events (see Population Estimate and Factor A), excessive rains also bring additional contaminants into the lake as runoff from lands surrounding the lake and upstream rivers. Research indicates that both the Juni

n grebe and its primary prey species, the pupfish, have accumulated toxins resulting in elevated lead levels. Environmental contaminants have caused die-offs of the species and have likely reduced the general health of the Juni

n grebe population (Factor C). The population has declined 14 percent in the past 10 years (see Population Estimates), and this decline is predicted to continue commensurate with ongoing threats from habitat destruction and water contamination (Factor A).

Despite the species' “critically endangered” status in Peru and its occurrence entirely within a protected area, the lake continues to be destroyed and degraded as a result of human activities that alter the lake's water levels and compromise water quality (Factors A and C). Therefore, regulatory mechanisms are either inadequate or ineffective at mitigating the existing threats to the Juni

n grebe and its habitat (Factor D).

Section 3 of the Act defines an “endangered species” as “any species which is in danger of extinction throughout all or a significant portion of its range” and a “threatened species” as “any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.” Based on the immediate and ongoing threats to the Juni

n grebe throughout its entire range, as described above, we determine that the Juni

n grebe is in danger of extinction throughout all of its range. Therefore, on the basis of the best available scientific and commercial information, we are proposing to list the Juni

n grebe as an endangered species throughout all of its range.

III. Juni

n rail (

Laterallus tuerosi

)

Species Description

The Juni

n rail is a secretive bird of the

Rallidae

family that is endemic to a single lake (Lake Juni

n) in Peru. The species is also referred to as the Juni

n black rail (Fjeldsa

1983, p. 281) and is locally known as “

gallinetita de Juni

n

”

(Supreme Decree 034-2004-AG 2004, p. 27684). This rail measures 4.7-5.1 in (12-13 cm) in length, and has a dark slate-colored head, throat and underparts. Its belly and vent (anal aperture) are black, with heavily-barred white primary feathers along the back and side. 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

The Juni

n rail was first taxonomically described as

Laterallus spilonotus

after Gould's 1841 description of the Galapagos crake (Fjeldsa

1983, p. 281; ITIS 2009b, p. 1). Fjeldsa

(1983) later described it as a subspecies of the black rail (

Laterallus jamaicensis tuerosi

) (Fjeldsa

1983, pp. 277-282; Fjeldsa

and Krabbe 1990, p. 146; ITIS 2009a, p. 1), noting that the bird's morphology may suggest that it is a distinct species (Fjeldsa

1983, p. 281).

Laterallus jamaicensis

has since been split into

L. jamaicensis

and

L. tuerosi

(BLI 2009b, p. 1). ITIS continues to list the species as the subspecies

L. j

.

tuerosi

based on Fjeldsa

's work in 1983 (ITIS 2009a, p. 1). BirdLife International considers this rail a full species based on morphological differences (BLI 2009b p. 1). Furthermore, the black rail,

Laterallus jamaicensis

occurs at much lower elevations (i.e., 0 to 4,429 ft (0 to 1,350 m) above sea level) (Collar

et al

. 1992, p. 190; BLI 2000, p. 170; BLI 2007, p. 1). Based on the morphological differences and the species' distinct and disjunct ranges, we consider the Juni

n 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 Juni

n rail have ever been collected (near Ondores) (Fjeldsa

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 (Fjeldsa

in litt., 1992, as cited in Collar

et al

. 1992, p. 190).

Habitat and Life History

The Juni

n rail inhabits Lake Juni

n at 13,390 ft (4,080 m) above sea level in the Andean highlands of Peru (Juni

n Region). The Juni

n rail occurs in the dense, interior marshlands where rushes (

Juncus

spp.) predominate or in more open mosaics of rushes, mosses (division Bryophyta), and low herbs (Fjeldsa

1983, p. 281). Lake Juni

n, home to the Juni

n grebe that is also the subject of this proposed rule, 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 2006, p. 2; ParksWatch 2009, pp. 1, 4). Giant bulrushes and totorilla dominate the extensive marshlands surrounding the lake (BLI 2009b, p. 1; Fjeldsa

1983, p. 281; ParksWatch 2009, p. 1). 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 2003, p. 1; 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). A more detailed discussion of the flora and fauna of the lake are provided above as part of the analysis of the Habitat and Life History of the Juni

n grebe.

There is little information regarding the ecology of the Juni

n rail. The species appears to be completely dependent on the wide marshlands located around the southeast shoreline of the lake for nesting, foraging, and year-round residence (BLI 2009b, p. 2; Collar

et al

. 1992, p. 190; Fjeldsa

1983, p. 281) (see also Current Range and Distribution). Similar to all rails, the Juni

n rail is furtive and remains well-hidden in the marshes surrounding the lake (BLI 2009b, p.2). The Juni

n 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 Juni

n 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 Juni

n rail is endemic to Lake Juni

n (Fjeldsa

1983, p. 278; BLI 2009b, p. 2). The species may have been historically common in the rush-dominated marshlands surrounding the entire lake (Fjeldsa

1983, p. 281). In addition to the species' specific habitat preferences (see Current Range and Distribution), it is believed that the Juni

n rail is now restricted to the marshes at the southwest corner of the lake because of the high level of water contamination that flows into the northwest margins of the lake via the Ri

o San Juan (Martin and McNee 1999, p. 662).

Current Range and Distribution

The Juni

n rail is restricted to the southwest shore of the lake, and is currently known in only two localities (near the towns of Ondores and Pari) (BLI 2009b, p. 2; Collar

et al

. 1992, p. 190; Fjeldsa

1983, p. 281). The current estimated range of the species is 62 mi

2

(160 km

2

) (BLI 2009b, p. 1). However, this is likely an overestimate of the species' actual range for several reasons. First, BirdLife International's definition of a species' range results in an overestimate of the actual range (see Current Range and Distribution of the ash-breasted tit-tyrant) (BLI 2000, pp. 22, 27). Second, the species' range was calculated based on the availability of presumed suitable habitat for the Juni

n rail. It has long been assumed that the rail potentially occupies the entire marshland area surrounding Lake Juni

n (Fjeldsa

1983, p. 281). The total marshland area has been estimated by BirdLife International to be 58 mi

2

(150 km

2

) (BLI 2000, p. 170; BLI 2007, p. 1; BLI 2008, p. 3; BLI 2009b, p. 1). However, the species has never been confirmed outside the two known localities on the southwest shore of the lake. Moreover, a better understanding of the “

puna

” habitat, as well as the habitat specificity (the specific habitat needs) of other rail species, indicates that these may be the only two localities for this species.

Despite the apparently uniform appearance of the “

puna

,” the habitat provides a complex mosaic of niches that leads to the patchy distribution of many bird species throughout the region, indicating that the species have specialized habitat requirements that are only satisfied locally (Fjeldsa

and Krabbe 1990, p. 32). The species' distribution is highly localized around the lake. The Juni

n rail apparently prefers the dense, interior marshlands comprised primarily of rushes (

Juncus

spp.) and mosaics of rushes, mosses (division Bryophyta), and low herbs in more open marsh areas (Fjeldsa

1983, p. 281). High habitat specificity is consistent with related rail species. Studies of the closely related California black rail (

Laterallus jamaicensis coturniculus

) indicate that this species is a habitat specialist, whereby the emergent vegetation used for cover, water depth, and access to upland vegetation, are all important factors in the black rail's habitat use (Flores and Eddleman 1995, p. 362). Therefore, the Juni

n rail's actual range is clearly smaller than the figure that continues to be reported by BirdLife International since 2000 (BLI 2000, p. 170; BLI 2007, p. 1; BLI 2008, p. 3; BLI 2009b, p. 1).

Population Estimates

Rigorous population estimates have not been made (Fjeldsa

1983, p. 281), and the species' elusiveness makes it difficult to locate (BLI 2009b, p. 2). In 1983, the Juni

n rail was characterized as possibly common, based on local fishers' sightings of groups of up to a dozen birds at a time (Fjeldsa

1983, p. 281). The species continues to be reported as “fairly common,” assuming that it occurs throughout the marshland surrounding the lake (BLI 2007, p. 1; BLI 2009b, p. 1). The BirdLife International estimate that this species' population size falls within the population range category of 1,000-2,499 (BLI 2000, p. 170; BLI 2007, p. 1; BLI 2009b, p. 1). This estimate is an extrapolation that continues to be based on the assumption that the species “may be fairly common in the entire c. 58 mi

2

(150 km

2

) of available marshland” around Lake Juni

n (BLI 2000, p. 170; BLI 2007, p. 1; BLI 2008, p. 3; BLI 2009b, p. 1). As indicated in the analysis of this species' Current Range and Distribution, 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 Juni

n rail is not common throughout Lake Juni

n's marshland, the actual population size may be much lower.

The species has experienced a population decline of between 10 and 19 percent in the past 10 years (BLI 2009b, p. 2). The population is considered to be declining in close association with continued habitat loss and degradation (see Factors A, C, and E) (BLI 2008, p. 1).

Conservation Status

The Juni

n rail is considered “endangered” by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276855). The IUCN categorizes the Juni

n rail as “Endangered” because it is known only from a small area of marshland (i.e., near Ondores and Pari) around a single lake, where habitat quality is declining (BLI 2008, p. 3). The single known population of the Juni

n rail occurs wholly within one protected area in Peru, the Juni

n National Reserve (BLI 2008, p. 1; BLI 2009b, pp. 1-2).

Summary of Factors Affecting the Juni

n Rail

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

The Juni

n rail is endemic to Lake Juni

n, where it resides year-round and is restricted to two localities within the shallow marshlands encircling Lake Juni

n (BLI 2008, p. 3; BLI 2009b, p. 2; Fjeldsa

1983, p. 278). The current estimated range of the species, 62 mi

2

(160 km

2

) (BLI 2009b, p. 1), is an overestimate of this species' range for the reasons outlined above as part of the analysis of this species' Current Range and Distribution. The species is known only from two discrete locations, near Ondores and Pari, on the southwest shore of the lake. Breeding occurs near the end of the dry season, in September and October, and the birds build their nests on the ground within the dense vegetative cover of the rushes that make up the marshland perimeter of the lake (BLI 2000, p. 170; BLI 2007, p. 1; BLI 2009b, p. 2).

The habitat in and around Lake Juni

n is subjected to manmade activities that have altered, destroyed, and degraded the quantity and quality of habitat available to the Juni

n 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). The Upamayo Dam went into operation at the northwest end of Lake Juni

n in 1936 to generate electricity using hydropower (Martin

et al

. 2001, p. 178; ParksWatch 2006, p. 5). Under normal conditions, water levels are lower during the dry season, and the marshlands can become partially or completely desiccated (BLI 2009b, p. 1; ParksWatch 2009, p. 2). The dam is often opened during the dry season, to generate power (June to November) (BLI 2009b, p. 1; ParksWatch 2009, p. 2), leading to further drawdown of the lake. Lake drawdown has been known to cause water levels to fluctuate seasonally up to 6 ft (2 m) (Martin and McNee 1999, p. 659) and has at times caused complete desiccation of the marshlands by the end of the dry season (Fjeldsa

2004, p. 123). The ground nesting Juni

n 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). A similar species, the California black rail, may tolerate decreases in water depth, but only if the substrate remains moist enough to support sufficient wetland vegetation (Flores and Eddleman 1995, p. 362). Eddleman

et al

. (1988, p. 463) noted that water drawdown before nesting season disrupts nest 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 Juni

n rail nest initiation.

Experts believe that the Juni

n rail is restricted to the marshes at the southwest corner of the lake because of the high level of contamination at the northwest 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 Juni

n rail (BLI 2000, p. 170; BLI 2007, p. 1; J. Fjeldsa

in litt., 1987, as cited in Collar

et al

. 1992, p. 190). Indeed, 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 Fjeldsa

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 surrounding the lake to graze. Overgrazing is a year-round problem around Lake Juni

n because the entire lakeshore is zoned for grazing by a large number of livestock (approximately 60,000-70,000 head) (ParksWatch 2006, pp. 12, 19). During the dry season, the hoofed stock moves into the marshlands to graze, compacting the soil and trampling the vegetation (ParksWatch 2006, p. 31). Increased access to the wetlands during the end of the dry season, which coincides with the inception of the Juni

n rail's nesting season, likely disrupts the rail's nesting activities or leads to nest trampling. Therefore, activities that increase lakeshore access, such as water drawdown, decrease the amount of available habitat for the Juni

n rail (for nesting and feeding) and are likely to negatively impact the Juni

n rail's reproduction (through trampling) and mating habits (through disturbance) (BLI 2009b, p. 1).

Water quality is another factor influencing the quality of habitat available to the Juni

n rail. The degraded water quality in Lake Juni

n was fully discussed as part of the Factor A analysis for the Juni

n grebe and is summarized here. The water in Lake Juni

n has been contaminated from mining (Martin and McNee 1999, pp. 660-661; ParksWatch 2006, p. 2; Shoobridge 2006, p. 3), agricultural activities (Martin and McNee 1999, pp. 660-661; ParksWatch 2006, p. 2;

Shoobridge 2006, p. 3), and from organic matter and wastewater runoff from local communities around the lake (ParksWatch 2006, pp. 5, 19; Shoobridge 2006, p. 3). Water pollution has resulted in heavy metal contamination throughout the lake, exceeding established thresholds for aquatic life throughout at least one-third of the lake (Martin and McNee 1999, pp. 660-661; O'Donnel and Fjeldsa

1997, p. 29; ParksWatch 2006, pp. 3, 20; Shoobridge 2006, p. 3), and rendering the northern portion of the lake lifeless (BLI 2008, p. 4; Shoobridge 2006, p. 3; Fjeldsa

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 due to contaminants (Fjeldsa

2004, p. 124; Martin

et al

. 2001, p. 180), and the lakeshore has become polluted with “toxic acid gray sediment” (O'Donnel and Fjeldsa

1997, p. 30). There is no vegetation at the northern end of the lake (Fjeldsa

2004, p. 124; ParksWatch 2006, pp. 20-21), and ongoing contamination has the potential to reduce vegetative cover in other areas of the lake, including the marshlands where the Juni

n rail occurs. In addition, these pollutants have severely affected animal and plant populations in the area, contributing to mortality of species around the lake (ParksWatch 2006, pp. 3, 20) and have the potential to reduce the health and fitness of the Juni

n rail (see Factor C).

Local residents also harvest and burn cattails from the marshland habitat, which the Juni

n rail depends upon. Cattails are harvested for use in construction (i.e., to assemble rafts, baskets, and mats) and as forage for livestock (ParksWatch 2006, p. 23). Cattails are also burned to encourage shoot renewal (ParksWatch 2006, p. 23) and for hunting the montane guinea pig (

Cavia tschudii

), which seeks cover in the cattail marshes and is part of the local diet. Burning cattail communities has a negative and long-lasting impact on species that use the cattails as permanent habitat (INRENA 2000, as cited in ParksWatch 2006, p. 22; Eddleman

et al

. 1988, p. 464), including the Juni

n rail, which relies on the dense vegetative cover of the marshlands for year-round residence and nesting (BLI 2000, p. 170; BLI 2007, p. 1; BLI 2009b, p. 2).

The negative impacts of habitat alteration and destruction (such as artificially reduced water levels, water contamination, and cattail harvesting and burning) 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). Peru is subject to unpredictable climate fluctuations, such as those that are related to the El Niño Southern Oscillation (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). ENSO events exacerbate the effects of habitat reduction and alteration on the decline of a species (England 2000, p. 86; Holmgren

et al

. 2001, p. 89; Jetz

et al

. 2007, pp. 1211, 1213; Mora

et al

. 2007, p. 1027; Parmesan and Mathews 2005, p. 334; Plumart 2007, pp. 1-2; Timmermann 1999, p. 694), particularly for narrow endemics (Jetz

et al

. 2007, p. 1213) such as the Juni

n rail (see also Factor E). As discussed above, droughts increase access to the wetlands where Juni

n rails live and breed. Excessive rain increases contamination in the water and causes soil toxicity (see Factor C). ENSO cycles are ongoing, having occurred several times within the last decade (NWS 2009, p. 2). Evidence suggests that ENSO cycles have already increased in periodicity and severity (Richter 2005, pp. 24-25; Timmermann 1999, p. 694), which will, thus, exacerbate the negative impacts on a species.

Summary of Factor A

The habitat in and around Lake Juni

n, where the Juni

n rail is endemic, has been and continues to be altered and degraded as a result of human activities, including artificial water level fluctuations to generate hydropower, water contamination caused by mining waste, agricultural and organic runoff from surrounding lands, and wastewater from local area communities. The Juni

n rail is dependent on the marshland habitat surrounding the lake for breeding and feeding. Water levels in Lake Juni

n are manipulated to generate electricity, which leads to dramatic fluctuations in water levels of up to 6 ft (1.8 m). The Juni

n rail nests on the ground, within the protective cover of the marshlands. As water drawdown occurs near the end of the dry season and during the inception of the Juni

n rail's mating season, portions of the marshlands may dry out completely, affecting the availability of suitable breeding and foraging habitat. This species' population decline has been linked to deteriorating habitat quality (see also Factor E). Overgrazing, cattail harvest, and burning are ongoing around the lakeshore, and water drawdown increases access to the marshlands. Severe water contamination in the northwest portion of the lake has rendered it lifeless, and experts believe that water contamination limits the Juni

n rail's foraging and breeding activities to the southern portion of the lake. The effects of artificially reduced water levels and water contamination are accentuated by droughts or excessive rains caused by El Niño events. Reduced water levels near the end of the dry season (during Juni

n rail nesting season) expose the species to greater vulnerability to predation (see Factor C), which also heightens the risks to the species that are associated with short- and long-term genetic viability (Factor E). Therefore, we find that destruction and modification of habitat are threats to the continued existence of the Juni

n rail throughout its range.

B. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes

We are not aware of any information currently available that indicates that overutilization of Juni

n rail for commercial, recreation, scientific, or education purposes has occurred or is occurring at this time. As a result, we are not considering overutilization to be a threat to the continued existence of the Juni

n rail.

C. Disease or Predation

Disease: Although no specific disease threat has been identified for the Juni

n rail, contamination of Lake Juni

n exposes the Juni

n rail to mortality and a reduction the overall fitness and health of the species. The effects of water contamination on the health of species inhabiting Lake Juni

n were discussed as part of the analysis of Factor C for the Juni

n grebe and are summarized here. In Lake Juni

n, mining activities (Martin and McNee 1999, pp. 660-661; Shoobridge 2006, p. 3), and agricultural runoff, organic matter, and wastewater (ParksWatch 2006, pp. 5, 19; Shoobridge 2006, p. 3) have contaminated the entire lake with high concentrations of dissolved chemicals (Fjeldsa

2004, p. 124; Martin and McNee 1999, pp. 660-662; ParksWatch 2006, pp. 20-21). Environmental contaminants exceed current established thresholds for aquatic life (Martin and McNee 1999, pp. 660-661; ParksWatch 2006, p. 20) and have rendered the northern portion of the lake lifeless from eutrophication (BLI 2008, p. 4; Shoobridge 2006, p. 3). Due to severe contamination, the sediments in the center of the lake are anoxic (Martin

et al

. 2001, p. 180), and the lake's turbidity has increased (ParksWatch 2006, p. 20). Chemical waste has damaged at least one third of the lake, severely affecting animal and

plant populations in the area (O'Donnel and Fjeldsa

1997, p. 29; ParksWatch 2006, pp. 3, 20; Shoobridge 2006, p. 3) and completely eliminating vegetation from the northern portion of the lake (Fjeldsa

2004, p. 124; ParksWatch 2006, pp. 20-21). It is also believed that contamination may, in fact, be responsible forthe possible extirpation of at least one fish species (a catfish) (O'Donnel and Fjeldsa

1997, p. 29).

Contamination from mining waste may have direct and indirect impacts on the fitness and health of the Juni

n rail. As described above as part of the Factor C analysis for the Juni

n grebe, a waterbird that is sympatric with the Juni

n rail, mine waste contamination may have caused heavy metal poisoning (T. Valqui and J. Barrio in litt. 1992, as cited in Collar

et al

. 1992, pp. 45, 190) or reduced prey availability (Fjeldsa

2004, p. 124), leading to Juni

n grebe mortality during an extensive drought from 1989 to 1992. Large-scale bird mortality has occurred on the lake, apparently due to lead poisoning from mining effluents—a common cause of mortality in waterbirds (Friend and Franson 1999, p. 317; O'Donnel and Fjeldsa

1997, p. 30). Heavy metals in the water column and the lake's sediments, where this species feeds, would have negative health consequences for the Juni

n rail, as in the case for the Juni

n grebe and other waterbirds that inhabit the lake. Excessive contaminant load can contribute to a decline in fitness and vigor for long-lived, mid-trophic level species (Rowe 2008, p. 624), such as the Juni

n rail. Increased turbidity of the water has resulted in die-offs of aquatic plants and algae, which disrupts the food chain (ParksWatch 2006, p. 20). Higher trophic level species (discussed in more detail as part of the Factor C analysis for the Juni

n grebe), such as the Juni

n rail, are more susceptible to disruptions in the food chain at lower trophic levels (Fjeldsa

2004, p. 123; The University of the Western Cape 2009, p. 1) and prone to bioaccumulation because they ingest pesticides, heavy metals, and other contaminants that are present in their prey (Demayo

et al

. 1982, as cited in Eisler 1988, p. 5; Fjeldsa

2004, p. 123). Drought conditions exacerbate the effects of water contamination and bioaccumulation for species at higher trophic levels (Demayo

et al

. 1982, as cited in Eisler 1988, p. 5; Fjeldsa

2004, p. 123).

Predation: Predators around Lake Juni

n include the Andean fox (

Pseudalopex culpaues

), the long-tailed weasel (

Mustela frenata

), Pampas cat (

Onicifelis colocolo

), and hog-nosed skunk (

Conepatus chinga

) (ParksWatch 2009, p. 4). Juni

n rails are preyed upon by pampas cats (BLI 2008, p. 4; BLI 2009b, p 2). Under normal conditions, water levels are lower in the dry season and the marshlands can become partially or completely dry (BLI 2009b, p. 1; ParksWatch 2009, p. 2) reducing protective cover and allowing predators to more easily locate the rail. When the floodgates of the Upumayo Dam are opened during the dry season (June to November) (BLI 2009b, p. 1; ParksWatch 2009, p. 2), drawdown has led to complete desiccation of the marshlands by the end of the dry season (Fjeldsa

2004, p. 123). The ground nesting Juni

n rail breeds near the end of the dry season, in September and October, and builds their nests in the dense vegetative cover of the rushes on the lake perimeter (BLI 2009b, p. 2). Water drawdown and periods of drought increases the bird's vulnerability to predation because nesting grounds become exposed and larger areas of the marsh are accessible to predators (ParksWatch 2006, p. 23). Predation increases the risk of extirpation due to the species' already small population size. In addition, species that inhabit a small geographic range, occur at low density, occupy a high trophic level, and exhibit low reproductive rates tend to have a higher risk of extinction than species that are not limited by the same risk factors (Purvis

et al

. 2000, p. 1949) (Factor E).

Summary of Factor C

Environmental contaminants (Factor A) in Lake Juni

n may have negative consequences on the health of the Juni

n rail, given that extensive environmental contamination in Lake Juni

n has resulted in mortality of flora and fauna that inhabit the lake and its margins. The species' trophic level also exposes it to bioaccumulation of toxins accumulated in the tissue of prey species. There is documented evidence that other waterbirds occupying the same habitat have died as a direct result of contaminant poisoning or reduction of the availability of prey species. Therefore, we find that disease is a threat to the continued existence of the Juni

n rail.

Predation by the pampas cat results in the direct removal of individuals from the population and can remove potentially reproductive adults from the breeding pool. Ongoing habitat destruction (through reduced water levels and contamination) continues to degrade the quality of habitat available to the Juni

n rail (Factor A) and the species' habitat becomes more accessible to predators during droughts and water drawdowns. Predation renders the species particularly vulnerable to local extirpation due to its small population size (Factor E). Therefore, we find that predation, exacerbated by ongoing habitat destruction (Factor A), are threats to the continued existence of the Juni

n rail throughout its range.

D. Inadequacy of Existing Regulatory Mechanisms

The Juni

n rail is listed as “endangered” by the Peruvian Government under Supreme Decree No. 034-2004-AG (2004, p. 276855). This Decree prohibits hunting, take, transport, and trade of protected species, except as permitted by regulation. As hunting, take, transport, and trade do not currently threaten the Juni

n rail, this regulation does not mitigate any current threats to this species.

Peru has several categories of national habitat protection, which were described above as part of the Factor D analysis for the ash-breasted tit-tyrant (BLI 2008, p. 1; IUCN 1994, p. 2; Rodri

guez and Young 2000, p. 330). The single Juni

n rail population occurs wholly within the Juni

n National Reserve (Juni

n, Peru) (BLI 2009b, pp. 1-2), which encompasses the lake and surrounding land and was established in 1974 by Supreme Decree 0750- 74-AG (BLI 2009a, p. 2; Wege and Long, p. 264). Peruvian National Reserves are created for the sustainable extraction of certain biological resources (BLI 2008, p. 1; Rodri

guez and Young 2000, p. 330), and most of the lakeshore is designated a “Direct Use Zone,” allowing fishing, grazing, and oth

This text is long and has been trimmed here. Open the source document for the complete record.