BEFORE THE SECRETARY OF THE INTERIOR
PETITION TO LIST A DISTINCT POPULATION SEGMENT OF THE BOREAL TOAD (ANAXYRUS BOREAS BOREAS) AS ENDANGERED OR THREATENED UNDER THE ENDANGERED SPECIES ACT
Photo by J. N. Stuart
CENTER FOR BIOLOGICAL DIVERSITY
CENTER FOR NATIVE ECOSYSTEMS
and
BIODIVERSITY CONSERVATION ALLIANCE
May 25, 2011
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Notice of Petition ______
Ken Salazar, Secretary U.S. Department of the Interior 1849 C Street NW Washington, D.C. 20240
Rowan Gould, Acting Director U.S. Fish and Wildlife Service 1849 C Street NW Washington, D.C. 20240
Steve Guertin, Regional Director U.S. Fish and Wildlife Service, Mountain-Prairie Region 134 Union Blvd. Lakewood, CO 80228
U.S. Fish and Wildlife Service Western Colorado Ecological Services Field Office 764 Horizon Drive, Building B Grand Junction, CO 81506-3946
PETITIONERS
David Noah Greenwald Endangered Species Program Director Center for Biological Diversity PO Box 11374 Portland, OR 97211 [email protected]
Collette L. Adkins Giese Herpetofauna Staff Attorney Center for Biological Diversity 8640 Coral Sea Street NE Minneapolis, MN 55449-5600 [email protected]
Megan Mueller Senior Staff Biologist Center for Native Ecosystems 1536 Wynkoop Street, Suite 303 Denver, CO 80202 [email protected] 2
Erik Molvar Executive Director Biodiversity Conservation Alliance P.O. Box 1512 Laramie, WY 82073 Biodiversity Conservation Alliance [email protected]
Submitted this 25th day of May, 2011
Pursuant to Section 4(b) of the Endangered Species Act (“ESA”), 16 U.S.C. §1533(b); Section 553(e) of the Administrative Procedure Act, 5 U.S.C. § 553(e); and 50 C.F.R. §424.14(a), the Center for Biological Diversity, Center for Native Ecosystems, and Biodiversity Conservation Alliance hereby petition the Secretary of the Interior, through the United States Fish and Wildlife Service (“FWS”), to list a distinct population segment of the boreal toad (Anaxyrus boreas boreas) as threatened or endangered and to designate critical habitat to ensure recovery. Specifically, a population of genetically unique boreal toads in the Southern Rocky Mountains, Utah, northeastern Nevada and southern Idaho, hereby referred to as the “Eastern population,” should be listed (see Section XI, Map 1 for proposed boundaries of this distinct population segment). In the alternative, the petition seeks to list boreal toads in the Southern Rocky Mountain as endangered or threatened (see Section XI, Map 3 for proposed boundaries of this distinct population segment). Should boreal toads in the Eastern population or in the Southern Rocky Mountains population be described as separate species while this petition is being considered, we hereby petition for those species.
The Center for Biological Diversity (“CBD”) is a non-profit, public interest environmental organization dedicated to the protection of native species and their habitats through science, policy, and environmental law. CBD is supported by over 320,000 members and on-line activists throughout the United States. CBD and its members are concerned with the conservation of imperiled species, including the boreal toad, and the effective implementation of the ESA.
The Center for Native Ecosystems (“CNE”) is a non-profit, public interest organization dedicated to conserving and recovering native species and ecosystems in the Greater Southern Rockies region. CNE represents more than 500 members in Colorado, Utah and Wyoming. We use the best available science to forward our mission through participation in policy, public outreach and organizing, administrative processes, legal action, and education. CNE staff and members have a long-standing interest in the conservation of the boreal toad and its habitat in the region at issue in this petition. We have participated on the boreal toad recovery team, worked to influence the management of boreal toad habitat on public lands, and engaged in a variety of other activities aimed at advancing boreal toad conservation.
Biodiversity Conservation Alliance (“BCA”) is a nonprofit organization dedicated to protecting wildlife and wild places in Wyoming and surrounding states, primarily on public lands.
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I. EXECUTIVE SUMMARY
During the last several decades, dramatic declines and disappearances of amphibian populations have been observed and documented worldwide. One species that has experienced such declines is the boreal toad (Anaxyrus boreas boreas). Although once considered a common garden toad in the western U.S., the boreal toad is rare across its range and is entirely absent from numerous areas where it occurred historically.
The boreal toad in the southern Rocky Mountains and surrounding areas warrants listing as a threatened or endangered species under the Endangered Species Act. Boreal toads are present in less than one percent of historic breeding areas in the southern Rockies. Only a handful of large populations remain and most remaining populations are threatened by the deadly chytrid fungus, habitat destruction, and inadequate regulatory mechanisms.
The boreal toad – more specifically, the Eastern population and the Southern Rocky Mountains population – meet at least three of the factors for determining whether a species is endangered or threatened in all or a significant portion of its range:
The present or threatened destruction, modification, or curtailment of the boreal toad’s habitat or range
The boreal toad is severely threatened by activities that destroy, modify, or curtail its habitat. These activities include timber management, livestock grazing, pesticide application, water management, recreation, residential and commercial development, and road building. As just one example, livestock activity in and around a breeding pond on the Targhee National Forest caused the death of hundreds of boreal toads from trampling and the disturbance of microhabitats (Bartelt 1998, 2000).
Disease
Chytridmycosis has devastated boreal toad populations in the southern Rocky Mountains and has now been detected in Utah (National Wildlife Health Center 2001; Thomas et al. 2004). This disease is caused by chytrid fungus, a microscopic, parasitic fungus that attacks the keratin and skin of amphibians and has caused 90-100 percent mortality rates in metamorphosed amphibians (McGee & Keinath 2004, p. 44). Populations of boreal toads infected with chytrid fungus have declined to near extinction within one year, and there are no documented cases of an infected population recovering following infection.
Inadequacy of Existing Regulatory Mechanisms
Existing regulatory mechanisms are inadequate to protect the boreal toad. Boreal toads are listed as state endangered species in Colorado and New Mexico but these designations lack necessary protection for boreal toad habitat. Voluntary conservation agreements for the boreal seek to guide management actions in the southern Rocky Mountains and Utah but no discernable impact on population trends in the region can be attributed to these actions.
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In combination, these factors demonstrate that a distinct population segment of the boreal toad warrants listing as a threatened or endangered species under the ESA. A prompt decision on ESA listing is required to ensure that this population is not beyond recovery before listing takes place.
Specifically, the U.S. Fish and Wildlife Service should recognize an Eastern population of boreal toads from the Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho. This population includes members of the evolutionarily significant “Eastern clade” identified by Goebel et al. (2009) and subsequently confirmed by Switzer et al. (2009). In the alternative, CBD, CNE, and BCA petition to list a distinct population segment of boreal toads in the Southern Rocky Mountains.
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Table of Contents
I. INTRODUCTION ...... 7
II. NATURAL HISTORY AND BIOLOGY OF THE BOREAL TOAD ...... 8
A. Taxonomy and Species Description ...... 8
B. Distinct Population Segments ...... 8
C. Distribution ...... 17
D. Habitat and Elevation Range ...... 18
E. Biology ...... 19
F. Population Status ...... 20
THREATS ANALYSIS
III. Present or Threatened Destruction, Modification, or Curtailment of Habitat or Range .. 22
IV. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes ...... 26
V. Disease or Predation ...... 27
A. Disease ...... 27
B. Predation ...... 28
VI. Inadequacy of Existing Regulatory Mechanisms ...... 29
VII. Other Natural and Anthropogenic Factors ...... 37
VIII. CRITICAL HABITAT...... 41
IX. CONCLUSION ...... 41
X. LITERATURE CITED ...... 42
XI. MAPS ...... 56
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I. INTRODUCTION
Boreal toads were once considered widely distributed and common amphibians in the western United States. But boreal toads in the Southern Rocky Mountains and elsewhere have experienced dramatic population declines over the past few decades.
Because of this decline, the FWS on July 22, 1994 issued a 90-day finding indicating that a petition submitted in September of 1993 by the Biodiversity Legal Foundation (later incorporated into CBD) and Dr. Peter Hovingh presented substantial information that the petitioned action may be warranted, and the FWS initiated a 12-month status review. 59 Fed. Reg. 37439.
On March 23, 1995, the FWS announced a 12-month finding that listing the Southern Rocky Mountains population of the boreal toad as an endangered species was warranted but precluded by other higher priority actions and placed the toad on the “candidate list.” 60 Fed. Reg. 15281.
Section 4(b)(3)(B) of the ESA directs that, when the FWS makes a ‘‘warranted but precluded’’ finding on a petition, it is to treat the petition as resubmitted annually on the date of the finding. 16 U.S.C. § 1533(b)(3)(B). On September 29, 2005, the FWS made its resubmitted 12-month finding, which evaluated new information and reevaluated previously acquired information. The FWS determined that the Southern Rocky Mountains population was discrete based on geographical separation from other populations of the boreal toad. 70 Fed. Reg. 56882. But the FWS concluded that the Southern Rocky Mountains population was not significant under the four factors outlined in the DPS Policy, 61 Fed. Reg. 4722 (Feb. 7, 1996). 70 Fed. Reg. 56883-84. In particular, FWS concluded that the Southern Rocky Mountains population was not significantly different from other populations of boreal toads based on its review of available genetic data. As a consequence, the FWS removed the Southern Rocky Mountains population of the boreal toad from the candidate list. 70 Fed. Reg. 56880.
Since then, two studies have concluded that boreal toads in the Southern Rockies are part of an evolutionarily significant “clade” that includes boreal toads in Utah, northeastern Nevada, and southern Idaho (Goebel et al 2009; Switzer et al. 2009). These studies further conclude that this clade contains as much genetic diversity as previous recognized species within the genus. The Eastern clade defined by Goebel et al. 2009 is a subject of this petition and is referred to here as the “Eastern population” of boreal toads. These studies and other facts also establish that the Southern Rocky Mountains population of boreal toads is significant under the DPS Policy.
In the five years since the FWS removed the Southern Rocky Mountains population from the candidate list, boreal toads in the Southern Rocky Mountains have continued to decline. The only large remaining population occurs in Colorado. The boreal toad is nearly extirpated in southern Wyoming and was likely extirpated in New Mexico prior to a recent reintroduction effort. The primary reason for the decline in the Southern Rockies appears to be related to infection by the chytrid fungus Batrachochytrium dendrobatidis (Bd). Populations of boreal toads infected with chytrid fungus have declined to near extinction within one year, and there are no documented cases of an infected population recovering following infection. There is a risk
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that these devastating impacts may soon be observed throughout the range of the Eastern population, as chytrid fungus has now been observed in Utah. In addition, loss of habitat is contributing to the decline of boreal toads across the range of the Eastern population. Habitats used by boreal toads are subjected to a variety of land management activities that harm habitat, including timber harvesting and livestock grazing.
Based on these scientific developments and ongoing threats, FWS should immediately list the Eastern population or Southern Rockies population of boreal toads as a distinct population segment under the ESA.
II. NATURAL HISTORY AND BIOLOGY OF THE BOREAL TOAD
A. Taxonomy and Species Description
The boreal toad (Anaxyrus boreas boreas) is a subspecies of the western toad (Anaxyrus boreas), which is an amphibian that occurs throughout much of the western United States (Stebbins 2003; Frost 2007). In 2008, the genus was changed from Bufo to Anaxyrus. The change reflects reclassification of genus Bufo in North America, as adopted by the Society for Study of Amphibians and Reptiles (Crother 2008). The Anaxyrus boreas species group currently comprises four species in western North America including the broadly distributed A. boreas, and three localized species, Anaxyrus nelsoni, Anaxyrus exsul and Anaxyrus canorus (Goebel et al. 2009, p. 1). Variation within the Anaxyrus boreas species group is poorly studied and may mask a number of cryptic species (Crother et al. 2003).
Boreal toads may reach a length (snout to vent) of 11 centimeters (4 inches) (Hammerson 1999). They possess warty skin, oval parotid glands, and often have a distinctive light mid- dorsal stripe. During the breeding season, males develop a dark patch on the inner surface of the innermost digit. Unlike other species in the genus, the boreal toad has no vocal sac and, therefore, no mating call (Hammerson 1999). The eggs are black and are deposited in long double layer jelly strings with one to three rows of eggs (Hammerson 1999). Tadpoles are black or dark brown.
B. Distinct Population Segments
The Endangered Species Act provides for the listing of distinct population segments (“DPSs”) of vertebrate species. FWS will consider a population a DPS if it is “discrete” in relation to the remainder of the species to which it belongs and “significant” to the species to which it belongs. See Policy Regarding the Recognition of Distinct Vertebrate Segments Under the Endangered Species Act (“DPS Policy”), 61 Fed. Reg. 4725. According to the DPS Policy, a population is “discrete” if it is “markedly separated from other populations” because of “physical, physiological, ecological, or behavioral factors” or it is “delimited by international governmental boundaries within which differences in control of exploitation, management of habitat, conservation status, or regulatory mechanisms exist that are significant in light of section 4 (a)(1)(D).” Id. A population need not have “absolute reproductive isolation” to be recognized as discrete. 61 Fed. Reg. 4724. A population is considered “significant” based on, but not limited to, the following factors: 1) “persistence of the discrete population in an unusual or
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unique ecological setting;” 2) “loss of the discrete population would result in a significant gap in range;” 3) the population “represents the only surviving natural occurrence of an otherwise widespread population that was introduced;” or 4) the population “differs markedly in its genetic characteristics.” 61 Fed. Reg. 4725.
On September 29, 2005, the FWS concluded that the Southern Rocky Mountains population was not significant under the four factors outlined in the DPS Policy. 70 Fed. Reg. 56883-84. As explained more fully below, the FWS erroneously determined that the Southern Rocky Mountains population did not persist in an ecological setting unusual or unique for the taxon based on its finding that the population utilizes habitats similar to other populations of boreal toad outside of the Southern Rocky Mountains population. 70 Fed. Reg. 56883. The FWS erroneously determined that the loss of the Southern Rocky Mountains population would not represent a significant gap in the range of the taxon based on its finding that it represents a relatively small proportion of the overall subspecies range. 70 Fed. Reg. 56883. Next, the FWS found that the boreal toad in the Southern Rocky Mountains population is not the only surviving natural occurrence of a taxon. 70 Fed. Reg. 56883. Finally, the FWS erroneously found that the Southern Rocky Mountains population does not differ markedly from other populations in genetic characteristics. 70 Fed. Reg. 56883. The FWS explained that genetic studies have shown that specimens from the Southern Rocky Mountains population group with specimens from nearby populations of boreal toad. 70 Fed. Reg. 56884. The FWS acknowledged the need for additional studies to clarify genetic relationships within and between boreal toad populations. 70 Fed. Reg. 56884.
For the reasons explained below, the Eastern population and Southern Rocky Mountains population of the boreal toad are discrete and significant and qualify for listing as a distinct population segment.
Discreteness
The Eastern population and Southern Rocky Mountain population are discrete because each is “markedly separate” from other populations of boreal toads. See 61 Fed. Reg. 4725 (DPS Policy).
The FWS has already determined that the Southern Rocky Mountains population is physically separated from other boreal toad populations. 70 Fed. Reg. 56882. The Red Desert and dry plains in southwest and central Wyoming serve as effective barriers between toads in northwest Wyoming and southeast Wyoming, and toads in Colorado are separated from those in Utah by at least 200 km and the dry intermountain basin of the Green River (Goebel et al. 2009, p. 221). See also 70 Fed. Reg. 56882.
The DPS Policy provides that “quantitative measures or genetic . . . discontinuity may provide evidence of this separation.” 61 Fed. Reg. 4725. As explained more fully below, two comprehensive genetics studies identify a clade of boreal toads in the Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho. These studies demonstrate that this clade – the Eastern population – is genetically unique from other boreal toad populations, which
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provides compelling evidence of discreteness under the DPS Policy (see Section XI, Map 2 for boundaries of the eastern clade).
Moreover, it is likely that all breeding populations of boreal toads within the Eastern population are isolated. Switzer et al. (2009, p. 25) found strong evidence that most of the breeding populations of boreal toads examined are isolated from one another, with very little gene flow. Similarly, molecular data suggest that gene flow among most Utah populations is extremely limited (Hogrefe 2001). Researchers have concluded that boreal toads in southern Utah are disjunct (Ross et al. 1995, p. 188).
Gene flow is probably precluded by the large distances and lack of migration corridors between habitats (Hogrefe et al. 2005, p.4). Based on the dispersal distances in the scientific literature, NatureServe (2010) concludes that occurrences are separated by 8 km within a common 1st, 2nd or 3rd order drainage, and by 5 km between drainages. Separation barriers include intensive residential or commercial development dominated by buildings and pavement, high traffic volume highways, and mountain ranges with passes above 12,500 ft (3810 m) (NatureServe 2010).
It is possible – but unlikely – that there is some genetic exchange between toads near the northwestern border of the Eastern population and other boreal toad populations, including: 1) populations in the Great Basin in Nevada; 2) populations to the north in Idaho; and 3) populations along the border of Idaho and northwestern/north central Wyoming in the Middle Rockies Ecoregion (see Section XI, Map 11). But as explained below, available information suggests that movement between these populations is likely to be limited.
In Nevada, the boundary of the Eastern population is not well-defined based on the genetic sampling done by Goebel et. al. (2009) and Switzer et al. (2009), as Goebel’s study included only one sample in northeastern Nevada, and Switzer’s study did not include samples in Nevada. A recent study of western toad genetics in Nevada suggests that Nevada harbors several distinct clades of Anaxyrus boreas, three of which are proposed as new species (Tracy et al. in prep.). But this study did not include data on boreal toads from the eastern Great Basin in northeastern Nevada and western Utah, with the exception of one sample from a location in northeastern Nevada (near the location of Goebel et al. 2009’s Nevada sample). This sample did not clearly fit into the clades identified by Tracey et al. (in prep.) in the Great Basin (D. Tracy, pers. comm., March 2011). Without comparison with additional samples east of Nevada, it cannot be determined whether this sample fits into the Eastern clade (D. Tracy, pers. comm., March 2011). However, available information on the geologic history of this region suggests that populations of Anaxyrus boreas in the Eastern Great Basin in Nevada may have separated from adjacent drainages during the Pleistocene (Noles 2010). According to Noles (2010), given what is currently known about geologic history and western toad phylogeography in the Great Basin, it is reasonable to suspect that the Bonneville Basin contains a western toad lineage that is discernable from those in adjacent basins to the west. As such, the western edge of the Bonneville Basin can be used for the western edge of the Eastern DPS (see Section XI, Map 12.)
Although there may be limited gene flow with populations to the north of the Eastern population in Idaho (in the area that Goebel et al. 2009 identified as the northwest clade, and that
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Switzer et al. designated as clade 3-2), the Snake River Plain likely forms a barrier that limits movement (see Section XI, Map 13). The Snake River Plain is made up of xeric plains and low hills, and its native vegetation is mostly sagebrush steppe with some barren lava fields and saltwood/greasewood (U.S. EPA 2011; Griffith 2010). In addition, much of the Snake River Plain consists of areas of intensive agricultural, residential and commercial development. (U.S. EPA 2011; Griffith 2010; see Section XI, Map 16). It is unlikely that boreal toads are able to regularly successfully disperse across the majority of the Snake River Plain. Similarly, a large dissected lava plateau covered in sagebrush steppe vegetation, likely forms a barrier that limits gene flow between toads in the Eastern population in southeastern Idaho and northwestern Utah from those in the southwest corner of Idaho (U.S. EPA 2011, Griffith 2010) (see Section XI, Map 13). There are no reliable records of boreal toad occurrence in this dissected lava plateau.
It is also possible that there is limited gene flow between the eastern clade and populations along the border of Idaho and northwestern/northcentral Wyoming in the Middle Rockies Ecoregion. However, these populations are at least partially separated by the Snake River through Hell’s Canyon. The canyon is ten miles across and averages 5,500 feet deep. It is 8,000 feet deep at its deepest point. The canyon is arid, and the Snake River carries substantial volumes of fast flowing, cold water. This canyon likely reduces gene flow between the eastern clade and populations along the border of Idaho and northwestern/northcentral Wyoming.
Further, even if there is a low level of gene flow with populations outside the Eastern population, this does not mean that the Eastern population lacks discreteness. Under the DPS Policy, it is not appropriate “to require absolute reproductive isolation as a prerequisite to recognizing a distinct population segment. This would be an impracticably stringent standard, and one that would not be satisfied even by some recognized species that are known to sustain a low frequency of breeding with related species.” 61 Fed. Reg. 4724. As the DPS Policy further explains, discreteness “does not require absolute separation of a DPS from other members of its species, because this can rarely be demonstrated in nature for any population of organisms. This standard adopted [by the DPS Policy] is believed to allow entities recognized under the Act to be identified without requiring an unreasonably rigid test of distinctness.” 61 Fed. Reg. 4724.
Significance
Marked Differences in Genetic Characteristics
The primary reason why the Eastern population is “significant” is because it differs markedly from other boreal toad populations in its genetic characteristics, which is one of the factors for determining significance recognized in the DPS Policy. See 61 Fed. Reg. 4725. Goebel et al. (2009) and Switzer et al. (2009) have identified boreal toads in the Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho as being evolutionarily significant. Goebel et al. (2009. p. 223) goes so far as to suggest that the “eastern major group” could be recognized as a distinct species. And Switzer et al. (2005, p. 20) explains that the boreal toads in the Southern Rocky Mountains, Utah, and southern Idaho are “significantly different” from other boreal toad populations. As explained above, the boundaries for the Eastern population are based on biogeographic features and the rough boundaries suggested by Goebel et al. (2009) and Switzer et al. (2009) (see Section XI, Maps 1 and 2).
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In 2009, Goebel and others published the results of their phylogenetic analysis of the Anaxyrus boreas species group. The goal of the study was to provide a broader molecular analysis of the boreas group than had been previously done (Goebel et al. 2009, p. 211). They examined mtDNA of toads from across the distribution to put the regional studies into larger context and to examine diversity within the whole group. In contrast to previous studies, Goebel et al. (2009, p. 211) included specimens from the eastern portion of the range. In total, they examined 288 samples from 58 collection sites. To identify relationships among more divergent lineages, they analyzed slowly evolving genes (12S ribosomal DNA and a portion of cytochrome oxidase I) and rapidly evolving DNA data (the control region and restriction sites of the whole mtDNA) with parsimony and Bayesian analyses (Goebel et al. 2009, p. 211).
The researchers identified three major haplotype groups as clades (Goebel et al. 2009, p. 215). They refer to the three lineages as the Northwest, Eastern, and Southwest clades; the clade name corresponds to their respective geographic regions. The Eastern clade, which is a subject of this petition, is currently part of Anaxyrus boreas boreas.
The Eastern clade consists of three strongly supported haplotype groups, including toads at the northern end of the Great Basin at the border of Utah and Nevada (E-NBasin), toads in the Southern Rocky Mountains of Colorado including the Uinta Mountains of Utah (E-Rocky Mountains), and a third group of toads from southern Utah that is sister to all other toads in the Eastern clade (E-SUT) (Goebel et al. 2009, p. 216). Southern Utah (E-SUT) is a disjunct population discovered in 1994 by Ross et al. (1995). The group at the northern end of the Great Basin (E-NBasin) is similarly divergent, but haplotypes from the NW-central and NW-middle Rocky Mountains also occur in the region (Goebel et al. 2009, p. 216). The Rocky Mountains (E-Rocky Mountains) clade was discovered largely from the geographically disjunct region in Colorado and southeastern Wyoming (the Southern Rocky Mountains population), but a single haplotype from this clade was also discovered in the Uinta Mountains of Utah (Goebel et al. 2009, p. 216). Each of these haplotype groups represents important diversity within the Eastern population that must be preserved.
Although the study by Goebel et al. (2009) does not delimit new species, the researchers explain that many divergent mtDNA lineages are in fact species and provide a better reflection of species diversity than the current taxonomy (Goebel et al. 2009, p. 223).
Building on the Goebel study, Switzer and others (2009) conducted phylogenetic and population genetic analysis of Anaxyrus boreas and three related species using mitochondrial DNA sequence data and nuclear microsatellite genotype data. The study was specifically focused on testing the evolutionary significance of the Southern Rocky Mountains population (Switzer et al. 2009, p. 2).
The researchers analyzed 470 bp of mitochondrial sequence data from 540 specimens and 890 microsatellite genotypes (12 loci) from throughout the ranges of Anaxyrus boreas, A. canorus, A. exsul and A. nelson (Switzer et al. 2009, p. 2). Phylogenetic analyses did not recover the Southern Rocky Mountains population as a monophyletic group, but rather as a part of a more widespread clade comprised of haplotypes from throughout Colorado, Utah and southern
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Idaho and southern Wyoming. The vast majority of individuals (>98 percent) from the Southern Rocky Mountains population region had a single haplotype that was also found in four Utah populations. Clustering of breeding populations in neighbor-joining trees derived from the microsatellite data also grouped the Southern Rocky Mountains population with populations from Utah and southern Idaho (Switzer et al. 2009, p. 2).
The researchers concluded that the Southern Rocky Mountains population is part of an evolutionary lineage that includes populations in Utah and southern Idaho, and they identified a clade that includes populations of boreal toads from Colorado, Utah, southern Idaho, and southern Wyoming (Switzer et al. 2009, p. 18). This clade was recovered as a well supported monophyletic group by both the parsimony and Bayesian phylogenetic analyses. A similar, but not identical, pattern of clustering was observed in the microsatellite neighbor-joining trees. To be sure, all of their analyses provide strong support for the Southern Rocky Mountains population being part of a more widespread evolutionary lineage that includes populations from Utah and southern Idaho (Switzer et al. 2009, p. 25). The researchers found that this clade is “one of the most strongly supported evolutionary lineages recovered” (Switzer et al. 2009, p. 18).
Switzer et al. (2009) explains that their results are “largely congruent” with the results of Goebel et al. (2009). The clade identified by Goebel et al. (2009) includes northeastern Nevada, while the clade identified by Switzer et al. (2009) does not because they had no samples from this region. Recognizing this difference, Switzer et al. (2009, p. 26) explains that the clade that they identify likely also contains boreal toads in northeastern Nevada.
With two comprehensive genetic studies independently reaching nearly identical results, it is evident that boreal toads in the Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho represent a significant entity. Loss of the genetic diversity within this evolutionary lineage would be a significant loss. On the basis of this factor alone, the Eastern population is significant under the DPS Policy.
The Goebel et al. (2009) study also confirms the genetic significance of the Southern Rocky Mountains population. (See Section XI, Map 3, which shows the boundaries of the Southern Rocky Mountains Population.) Within the eastern clade identified by Goebel et al. (2009) are three divergent groups, including the E-Rocky Mountain clade. The E-Rocky Mountain clade was discovered largely from the Southern Rocky Mountain population but a single haplotype of this clade was also discovered in the Uinta Mountains of Utah. Because of the complete geographic isolation of the toads in the Southern Rocky Mountain population, Goebel et al. (2009) explains that the closely related haplotype in the Uinta Mountains, Utah, is due to incomplete lineage sorting, commonly found in recently isolated groups. The lead author, Anna Goebel, explains that her research shows that boreal toads the Southern Rocky Mountains are their own evolutionary unit (Boreal Toad Recovery Team Research Updates 2009). To be sure, Goebel (2005, p. 213) explains that boreal toads in the Southern Rocky Mountains comprise more diversity than currently recognized species, such as A. exsul or A. nelsoni.
Although Switzer et al. (2009) conclude that the Southern Rocky Mountains population of boreal toads is part of a more widespread evolutionary lineage that includes populations in Utah and southern Idaho, their data does not show that the Southern Rocky Mountains
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population is not significant under the DPS Policy. Even though they did not find the Southern Rocky Mountains to be monophyletic, monophyly is not a necessary criterion for significance under the DPS Policy.
As such, the best available science shows that the genetic characteristics of boreal toads in the Eastern population and Southern Rocky Mountains population differ markedly from that of boreal toads elsewhere in the range.
Significant Gap in the Range
The loss of the Eastern population would result in a “significant gap” in the range of the species. See 61 Fed. Reg. 4725 (DPS Policy). The loss of this population would reduce the range of boreal toads at its southeast extension, from south central Wyoming, through the mountainous regions of Colorado, into extreme New Mexico, through the mountainous regions of northern and southern Utah, and into the northern Great Basin, including northeastern Nevada and southern Idaho. The remaining range in the conterminous United States extends from the Pacific Northwest, northern California, Idaho, western and central Nevada, and western Wyoming. The geographic area within the boundaries of the Eastern population represents roughly 21% percent of the total gross conterminous U.S. range of the Anxyrus boreas species group – the area of the total gross range of the Anaxyrus boreas species group in the contiguous U.S. is roughly 767,100 sq. mi. and the portion of the International Union for the Conservation of Nature (“IUCN”) gross range map that was identified as the range of the significant entity by Switzer et al. (2009) and Goebel et al. (2009) is roughly 161,422 square miles (see Section XI, Map 4). A loss of over 20 percent should be considered a significant gap.
Likewise, Petitioners disagree with the FWS’s finding that the loss of the Southern Rocky Mountains population would not result in a significant gap in the range of the boreal toad. See 70 Fed. Reg. 56883. The geographic area within the boundaries of the Southern Rocky Mountains population represents roughly five percent of the total gross conterminous U.S. range of the Anxyrus boreas species group – the area of the total gross range of the Anaxyrus boreas species group in the contiguous U.S. is roughly 767,100 sq. mi. and the portion of the IUCN gross range map within the Southern Rocky Mountains is roughly 38,894 square miles (see Section XI, Map 5). A loss of five percent could be considered a significant gap, as demonstrated by the fact that FWS concluded in an August 2004 draft proposed rule that the loss of the Southern Rocky Mountains population would result in a significant gap.
Unusual Ecological Setting
The Eastern population and the Southern Rocky Mountains population are also significant because each persists in an ecological setting unusual or unique for the taxon. Generally speaking, western toad habitat is relatively spatially contiguous in the northern and northwestern portions of the species range and becomes progressively less spatially continuous moving south and east (see Section XI, Map 6). The Eastern population (and the Southern Rocky Mountains populations within it) constitutes the southeastern portion of the range, where the habitat is relatively discontinuous. In southern California and Nevada, where habitat is similarly discontinuous, several Anaxyrus species, Anaxyrus boreas subspecies, and distinct
14 clades have been identified. This may be a consequence of increased isolation of areas of Anaxyrus habitat in the southern portion of the range and ecological differences between the habitats occupied by such populations and those elsewhere in the range.
Moreover, the Eastern population can be divided into four distinct ecological settings: the Southern Rocky Mountains (Colorado, southern Wyoming, northern New Mexico), the Wasatch and Uintah Mountains (central Utah), the Paunsagunt Plateau (isolated population on southern tip of Utah boreal toad distribution), and the area of transition between ecoregions where the Northern and Central Basin and Range, Middle Rocky Mountains and Wasatch and Uintah Mountains come together (southeastern Idaho, northwestern Utah and northeastern Nevada). As explained below, each of these settings constitutes an unusual or unique ecological setting both relative to one another and relative to the ecological settings found throughout the rest of the range of the boreal toad.
These unusual ecological settings are described using information on Level III and IV ecoregions (U.S. EPA 2011; Griffith 2011). Ecoregions denote areas of general similarity in ecosystems and in the type, quality and quantity of ecological resources, identified through the analysis of patterns of biotic and abiotic phenomena, including geology, physiography, vegetation, climate, soils, land use, wildlife and hydrology (U.S. EPA 2011; Griffith 2010).
Southern Rocky Mountains. Boreal toads in the Southern Rocky Mountains in Colorado, southern Wyoming, and northern New Mexico are within the Southern Rockies ecoregion (see Section XI, Map 7). The Southern Rockies ecoregion is ecologically different from other ecoregions occupied by the boreal toad elsewhere in its range. These differences are evident when comparing the Southern Rockies ecoregion with two other ecoregions occupied by the boreal toad: the Middle Rockies ecoregion and the Wasatch and Uintah Mountains ecoregion, two of the closest (and likely most similar) ecoregions outside of the Southern Rockies occupied by Anaxyrus boreas.
The Southern Rockies ecoregion differs substantially from the Middle Rockies ecoregion. The Southern Rockies ecoregion constitutes a large block of relatively high elevation habitat compared to the Middle Rockies. The average minimum and maximum elevations in the Southern Rockies are higher than those in the Middle Rockies. The Southern Rockies is cooler in the summer and warmer in the winter than the Middle Rockies, and the Southern Rockies receive lower average annual precipitation. The vegetation in the Southern Rockies exhibits a pattern of elevational banding unlike the distribution of vegetative communities in the Middle Rockies. In addition, the Southern Rockies ecoregion has much less lodgepole pine forest than in the Middle Rockies. Finally, boreal toad habitat is generally less continuous in the Southern Rocky Mountains than it is in the Middle Rocky Mountains. (Griffith et al. 2010, Chapman et al. 2006, U.S. EPA 2011)
The Southern Rockies ecoregion also differs from the Wasatch and Uintah Mountain ecoregion in Utah. The Southern Rockies ecoregion’s minimum, maximum, and mean annual temperatures are higher than those of the Wasatch and Uintah mountains ecoregion. The amount of precipitation differs between these two ranges, and the Wasatch and Uintah mountains have more frost-free days. In addition, aspen, chaparral, juniper-pinyon and oak are more common at
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middle elevations in the Wasatch and Uintah Mountains (U.S. EPA 2011; Griffith 2010; Chapman et al. 2006; Woods et al. 2001).
The ecological differences between the Southern Rockies ecoregion and the remaining ecoregions (other than the Wasatch and Uintah Mountains and Middle Rockies compared here) are even greater.
The uniqueness of the Southern Rockies ecoregion demonstrates the significance of the Southern Rocky Mountains population. Likeness, the presence of this unique ecological setting within the Eastern population also demonstrates that the broader Eastern population is significant.
Wasatch and Uintah Mountains (central Utah). Boreal toads in central Utah are within the Wasatch and Uintah Mountains ecoregion (see Section XI, Map 8). As explained above, there are numerous differences between the Wasatch and Uintah Mountains ecoregion and the Southern Rockies ecoregion. Furthermore, when compared to the Middle Rocky Mountains, the Wasatch and Uintah Mountains include areas of much higher elevation that get less annual precipitation, have more frost-free days, and are warmer in the winter. Further, the vegetation in the Wasatch and Uintah Mountains exhibits a pattern of elevational banding unlike the pattern the Middle Rockies, and there is much less lodgepole pine forest than in the Middle Rockies. (U.S. EPA 2011; Griffith 2010; Chapman et al. 2004; Woods et al. 2001). Finally, boreal toad habitat is much less continuous in the Wasatch and Uintah Mountains than in the Middle Rocky Mountains (see Section XI, Map 6). Thus, the Wasatch and Uintah mountains differ significantly from the two closest and likely most similar regions that support Anaxyrus boreas. The differences between the Wasatch and Uintah Mountains ecoregions and the remaining ecoregions that support Anaxyrus boreas are likely even greater.
The presence of this unique ecological setting within the Eastern population demonstrates that the broader Eastern population is significant.
Paunsagunt Plateau (isolated population on southern tip of Utah boreal toad distribution). The isolated population in southern Utah is found on a Plateau near the boundary between the Wasatch and Uintah Mountains ecoregion and the Colorado Plateaus ecoregion (see Section XI, Map 9). This area includes three Level IV ecoregions occupied by boreal toads: High Plateaus, Escarpments, and Semi-Arid Benchlands and Canyonlands (see Section XI, Map 9). This area falls within an ecotone that transitions between the relatively high elevation plateau (with relatively high levels of precipitation; cold winters; and spruce, fir and pine forests) and progressively lower elevations (with more arid and warmer climates, and vegetation consisting primarily of pin-juniper woodlands and shrublands). (U.S. EPA 2011; Griffith 2010; Woods et al. 2001) No other population of boreal toad exists along a similar ecotone.
The presence of this unique ecological setting within the Eastern population demonstrates that the broader Eastern population is significant.
Northern and Central Basin and Range/Middle Rocky Mountains Transition Zone (in southeastern Idaho, northwestern Utah and northeastern Nevada). Boreal toad
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populations in southeastern Idaho, northwestern Utah and northeastern Nevada are located in an area of transition between: 1) the Northern and Central Basin and Range, Middle Rocky Mountains, and Wasatch and Uintah Mountains ecoregions, and 2) relatively continuous boreal toad habitat in the Middle Rockies and naturally patchy habitat in the Northern and Central Basin and Range and the Wasatch and Uintah Mountains.
This area differs from the rest of the Northern and Central Basin and Range in that the boreal toad habitat in this area is less naturally fragmented and isolated than the boreal toad habitat in the rest of the Basin and Range (see Section XI, Map 10). In addition, this area is somewhat higher in elevation than the rest of the Basin and Range (U.S. EPA 2011; Griffith 2010; Bryce et al. 2003; McGrath et al. 2002). The ecological differences between this area and the remaining ecoregions occupied by Anaxyrus boreas across its range are greater than the differences between this area and the Northern and Central Basin and Range ecoregions. Finally, these populations are along the margins of the Bonneville Basin. Hydrological isolation of the Bonneville Basin from other basins in the Great Basin in Nevada during the Pleistocene (Noles 2010) may have resulted in differences in ecological characteristics between the Bonneville Basin and those elsewhere in the Great Basin, including differences in amphibian assemblages. This area differs from the Middle Rockies in that it is lower in elevation, warmer, and drier (U.S. EPA 2011; Griffith 2010; Bryce et al. 2003; McGrath et al. 2002; Chapman et al. 2004), as well as being more naturally fragmented and isolated (see Section XI, Map 6).
Given that boreal toads in the Eastern population occupy four ecoregions including the Southern Rocky Mountains ecoregion that differ from each other as well as from those areas occupied by boreal toads in the rest of its range, the Eastern population and the Southern Rocky Mountains population must be said to exist in ecological settings that are unique or usual for the species.
In sum, the best available data demonstrates that the Eastern population and the Southern Rocky Mountains population are both discrete and significant. As such, FWS should recognize a distinct population segment of boreal toads.
C. Distribution
The range of the boreal toad subspecies is coastal Alaska south through British Columbia, western Alberta, Washington, Oregon, northern California, Nevada, Idaho, western Montana, western and south central Wyoming, the mountains of Utah and Colorado, and extreme northern New Mexico. 70 Fed. Reg. 56881. The Eastern population of boreal toads includes boreal toads in the Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho. The Southern Rocky Mountains region extends from south central Wyoming, throughout the mountainous portions of Colorado, and into extreme northern New Mexico.
In Colorado, boreal toads are found at dozens of sites but only one population is now considered viable according to the definition in the Colorado recovery plan (T. Jackson, pers. comm., March 2011). The boreal toad is very rare or extirpated in southern Wyoming (Keinath & Bennett 2000, p.4). It was presumed extirpated in New Mexico (NatureServe 2010), until one population was reintroduced in the Carson National Forest (Pierce, pers. com. 2010). In Utah,
17 boreal toad populations are likely still distributed throughout much of the historic Utah range (Thompson et al. 2004). But documented extant populations in Utah are irregularly distributed within the former distribution (Hogrefe et al. 2005, p. 5), and, as of 2009, only two populations could be considered viable under the conservation plan’s definition (UDWR 2009). Boreal toads are known to be present along the Utah and Idaho border and in scattered locations across south- central Idaho (Barrett et al. 2011; McDonald 1996; Shrive & Peterson 2001; Lorenz & Bailey 2005). The southeastern Idaho population of toads has been found at only two different sites in just one watershed and is highly imperiled (Koch & Peterson 2005). No published information is available on the historic or current distribution in northeastern Nevada.
D. Habitat and Elevation Range
There are three main habitat components required for boreal toads: 1) shallow wetlands for breeding, 2) terrestrial habitats for foraging that provide vegetative cover, and 3) burrows for winter hibernation (BTRT 2001). Boreal toads may migrate several kilometers from breeding ponds to winter hibernacula, but in most cases this distance is much less. Therefore all of the habitat components described above should be within 2.5 km of breeding ponds to provide optimal habitat for boreal toads (McGee & Keinath 2004, p. 42). The necessity for this habitat juxtaposition restricts the pool of available habitat, since there are relatively limited sites that combine suitable wetland habitat adjacent to suitable terrestrial habitat (McGee & Keinath 2004, p. 42).
Based on information from the Southern Rockies and Utah, boreal toads in the Eastern population primarily occupy slow moving streams, beaver ponds, small lakes, reservoirs, stock ponds, wet meadows, seeps, creek pools, marshy areas, wet meadows, and associated woodlands (Fridell et al. 2000, Thompson and Chase 2001; Campbell 1970a; Hammerson 1999). Habitat use patterns after breeding are likely dependent on characteristics of the upland environment and may differ between the sexes (Campbell 1970b, Campbell 1976). Female toads may use habitats that are drier and more distant from breeding habitats compared to males (Jones et al. 1998). Any activities that destroy, modify, or curtail habitat are likely to contribute to the continued decline of the boreal toad. These include livestock grazing, timber management, pesticide application, recreation, residential and commercial development, and road building.
Burrows represent critical microhabitats for boreal toad and other amphibians (Carey 1978; Smits 1984). Burrows are important for maintaining stable body temperatures despite extreme ambient temperatures. Smits (1984) found that toads always remained in the deepest burrow locations during winter, resulting in relatively low and stable body temperatures. During summer, burrows may be used to prevent water loss and dehydration. Boreal toads seek shelter under logs or rocks or in small mammal burrows or other below-ground spaces (Campbell 1970c; Jones et al. 1998; Fridell et al. 2000). Activities that can crush or otherwise harm burrows, such as livestock grazing and timber management, are detrimental to the boreal toad.
The western toad is generally considered to occupy relatively higher elevation habitats compared to other western amphibians. In Colorado, boreal toads are most often observed between 2,250 and 3,600 m (Campbell 1970a; Hammerson 1982; Livo and Yeakley 1997). In southeastern Wyoming, historic records previously ranged up to 3,200 m but records of current
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occurrence currently do not exceed 2,925 m (Livo and Yeakely 1997). Populations of boreal toad in northwestern Utah occupy habitats at considerably lower elevations (Thompson 2004, p. 343). The minimum elevation of boreal toad in Utah is approximately 1,570 m (Hogrefe 2005, p. 7).
E. Biology
In the Southern Rocky Mountains, adult boreal toads emerge from winter refugia when snowmelt has cleared an opening from their burrows and daily temperatures remain above freezing (Campbell 1970a, Campbell 1970b).
Breeding occurs during a 2- to 4-week period from mid-May to mid-June at lower elevations, and as late as mid-July at higher elevations (Hammerson 1999; Carey et al. 2005, p. 224). During the breeding season, males actively search for females, clasp female and male toads indiscriminately, and do not defend territories (Olson et al. 1986). Males do not give mating calls and only vocalize release calls when clasped by other males (Olson et al. 1986).
After mating, adults often disperse to upland, terrestrial habitats, where they are mostly diurnally active in early and late summer (Campbell 1970a; Carey 1978), foraging primarily on ants, beetles, spiders, and other invertebrates (Schonberger 1945; Campbell 1970a). Late in the summer, home ranges will expand, generally in the direction of wintering habitats (Campbell 1970a), which include cavities among streamside boulders, ground squirrel burrows, and beaver lodges and dams (Hammerson 1999).
Carey et al. (2005, p. 224) reported an overall mean clutch size of 6,661 eggs for 3 populations studied in Colorado. Eggs hatch 1 to 2 weeks after being laid. Egg and tadpole development is temperature-dependent, and reproductive efforts may fail if tadpoles do not have sufficient time to metamorphose before the onset of winter (Carey et al. 2005). Persistent, shallow bodies of water are critical to breeding success, and if the breeding site dries before metamorphosis is complete, desiccation of the tadpoles or eggs will occur (Carey et al. 2005).
Tadpoles filter suspended plant material or feed on bottom detritus (NatureServe 2010). They typically metamorphose by late July to late August, but at higher elevations metamorphosis may not be complete until late September (BTRT 2001). Recently metamorphosed toadlets aggregate within a few meters of the water, and move into nearby moist habitats later in summer.
Survival of embryos from laying to hatching is normally high but catastrophic mortality has been observed (Blaustein and Olson 1991). Desiccation of egg masses appears to be the single largest source of egg mortality (Carey et al. 2005, p. 227). Survival of tadpoles and juveniles is very low, with predation and adverse environmental conditions primarily responsible for mortality at these lifestages (Campbell 1970a; Carey et al. 2005, p. 227-28). Samollow (1980) estimated that 95 to 99 percent die before reaching their second year of life.
The minimum age of breeding boreal toads in Colorado is about 4 years in males and 6 years in females (Hammerson 1999). Olson (1991) found that females may skip 1 to 3 years between breeding attempts; female boreal toads rarely if ever breed two years in a row (Carey et
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al. 2005, p. 226). Adults often live more than nine years (Hammerson 1982, Campbell 1976) and maximum life span is estimated to be about 12 years (BTRT 2001).
F. Population Status
Boreal toads were once considered widely distributed and common amphibians in the western United States. Currently, the boreal toad shows signs of significant declines in population size and distribution across its range in western North America, and especially in the southern Rocky Mountains (Corn et al. 1989; Carey 1993; Corn 1994; Keinath and Bennet 2000; BTRT 2001). Available information about the status of the Eastern population (and the Southern Rocky Mountains population more specifically) is summarized below.
Southern Rocky Mountains
The boreal toad was formerly widespread and numerous in southern Wyoming, Colorado, and northern New Mexico (McGee & Keinath 2004, p. 28). But survey efforts over the past 25 years indicate that boreal toad populations in the Southern Rockies have sharply declined (McGee & Keinath 2004, p. 27; Ross et al. 1995; Corn et al. 1997). Since the 1970s, greater than 90 percent of historical occurrences in Colorado and Wyoming have been extirpated, and it appears that New Mexico populations were completely extirpated (Corn et al. 1989; Hammerson 1989, 1992, 1999; Carey 1993) prior to recent reintroduction efforts. Large breeding populations in the Southern Rocky Mountains are now confined to a few areas in Colorado, including Rocky Mountain National Park and several wilderness areas on Forest Service lands (Keinath & Bennett 2000, p. 6). The number of occurrences remains greatly reduced, and few of these populations are large. Declines are still occurring, even in pristine areas (Muths 2003).
In southern Wyoming, boreal toads were historically present in the Medicine Bow, Sierra Madre, and Laramie ranges (McGee and Keinath 2004, p. 27). Keinath and Bennett (2000, p. 4) concluded the southern Wyoming population seems nearly extirpated from its historic range. They explain that there have been no recent, confirmed observations in the southern Laramie Range. A few small breeding populations may remain in the Medicine Bow National Forest and Sierra Madre Mountains, but in the late 1990s there were only two observations of boreal toads in the area. (Keinath & Bennett 2000, p. 6-7; McGee & Keinath 2004, p. 29).
In Colorado, the boreal toad was still considered fairly common in the 1980s (Hammerson and Langlois 1981). But even then, evidence of dramatic declines had already been noted. Carey (1993) observed the disappearance of 11 populations of boreal toads between 1974 and 1982 in the West Elk Mountains. Subsequent surveys have shown no re-colonization of these former breeding sites. In 1991, Hammerson (1992) surveyed 377 sites in Colorado, and observed only a single population of boreal toads. Surveys of 38 historic breeding locations in eight national forests in Colorado covering Boulder, Chaffee, Delta, Gunnison, Jackson, Larimer, Mesa, and Summit counties from 1982 to 1992 revealed only one occupied site in Chaffee County (Jackson 2004, p. 9).
Subsequent studies on occupied boreal toad sites in Colorado have found that chytrid fungus and other threats are widespread. In 2006-2007, boreal toads occurred at about 80 known
20 breeding sites in Colorado (Jackson 2008), and 53 of the 80 monitored sites were tested for chytrid fungus. Only 37 were free of the deadly fungus. Of these chytrid-free sites, eight sites lacked evidence of breeding or have experienced poor hatching success and survival. Only one population in Colorado is now considered viable according to the definition in the Colorado recovery plan (T. Jackson, pers. comm., March 2011).
In New Mexico, the boreal toad historically occupied three lakes in north-central Rio Arriba County (Pierce 2006, p. 10). Over the past several decades, the species has precipitously declined in New Mexico and was not found in 1993 or 2000-2002 (Pierce 2006, p. 10). The boreal toad was presumed extirpated in New Mexico (Degenhardt et al. 1996; Stuart and Painter 1994; New Mexico Department of Game and Fish 1988; BTRT 2001), until a population was reintroduced to one of the three historically occupied lakes in recent years. Breeding has been documented at the site, but it is unclear yet whether this reintroduction was a success because chytrid fungus has been discovered at the site (Pierce, pers. com. 2010).
Utah
In Utah, the boreal toad was apparently widespread and abundant historically (Ross et al. 1995, p. 187). Tanner (1931) described it as “the common species in the canyons and mountains of central and northern Utah.” Woodbury (1952) described it as a “common garden toad.” Hardy (1938) wrote that it was “common in the Colorado River drainage in Sevier and Wayne counties” in southern Utah. There are records of boreal toad occurrence at approximately 203 localities in Utah (Hogrefe et al. 2005, p. 5).
Between 2005 and 2009, only two boreal toad populations in Utah met the criteria for viability as defined by Utah’s conservation plan (Grouse Creek and Uintah Mountains) (UDWR 2009). The Grouse Creek population was viable in 2006 and 2007 but was no longer viable in 2009 (UDWR 2009). In 2009, only one population (Uintah Mountains) could be defined as viable. In addition, a small number of populations with documented breeding have not been monitored for sufficient time to determine viability (UDWR 2009).
None of the reintroductions in Utah have resulted in establishment of viable populations yet. In 2009, only one toad was observed on Paunsagunt Plateau in Utah, and the 2009 Utah boreal toad monitoring report states that the Paunsagunt Plateau population “remains critically low and may be in jeopardy of extirpation.” In the Uinta National Forest in Utah, the only recent record of boreal toads is one population in the Mud Creek bay area near Strawberry Reservoir, despite the fact that historical records are known from many locations across the Forest (USDA Forest Service 2008, p. 26).
Northeastern Nevada and Southern Idaho
Little has been published on the population status of boreal toads in northeastern Nevada and southern Idaho, but the few available reports explain that boreal toads in these areas have suffered significant population declines. Koch and Peterson (2005) explain that the southeast Idaho population of toads is narrowly distributed and highly imperiled. Wendte and others (2005) found that the boreal toad occupies only half of 34 historical sites that they surveyed in
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the northern Great Basin and conclude that the species has declined in and around the northern Great Basin. The area of land in northeastern Nevada that is within the range of the Eastern population is small and includes only a fraction of the Eastern population.
THREATS ANALYSIS
Section 4 of the Endangered Species Act and its implementing regulations set forth the procedures for adding species to the federal list of endangered and threatened species. 16 U.S.C. § 1533; 50 C.F.R. Part 424. FWS may determine a species to be endangered or threatened due to one or more of the five factors described in section 4(a)(1) of the Act. Each of these factors is discussed below.
Importantly, FWS has already determined that the Southern Rocky Mountains population of the boreal toad is in danger of extinction (60 Fed. Reg. 15281) and its status has deteriorated since that finding was made in 1995.
III. Present or Threatened Destruction, Modification, or Curtailment of Habitat or Range
The Eastern population of boreal toads is primarily found on public land within state forests, national forests, and lands administered by the Bureau of Land Management, Bureau of Reclamation, and National Park Service. 60 Fed. Reg. 15281. The use of these lands ranges from recreational to intensive timber and grazing management and watershed alteration activities. As discussed below, any activities that destroy, modify, or curtail habitat are likely to contribute to the continued decline of the boreal toad.
Livestock Grazing
Riparian areas provide critical breeding, foraging, and over wintering habitats for boreal toads and are used as dispersal corridors for juvenile toads (McGee & Keinath 2004, p. 32). Given access to water and typically richer vegetation in riparian areas, these habitats are also preferred areas for livestock grazing (McGee & Keinath 2004, p. 32). Grazing allotments for both cattle and sheep are common in the area occupied by the Eastern population (see Section XI, Map 14).
Livestock grazing is one of the most widespread land management practices in western North America and it has been associated with a wide range of negative impacts on habitat and vertebrate taxa, including amphibians (Fleischner 1994; Dickman 1968; Corn and Fogelman 1984). Trampling by livestock may be a significant source of mortality for all amphibian life stages, especially for tadpoles and metamorphs that lack mobility and congregate near water margins (Hogrefe et al. 2005, p. 15). Bartelt (1998, 2000) observed that livestock activity in and around a breeding pond on the Targhee National Forest caused significant mortality for boreal toads from trampling and the disturbance of microhabitats. Bartelt observed that hundreds of toads had been directly killed by trampling and hundreds more died afterward as a result of desiccation because the vegetation they had been using for cover was trampled to the point that it
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no longer provided moist microhabitats. Similar impacts have also been observed in Utah (Hogrefe 2005; UDWR 2008).
Grazing also has indirect effects on boreal toads. Grazing may reduce the number of insect prey that amphibians depend on (Fleischner 1994; Reaser 1996). Prairie dog and other rodent control programs associated with livestock production may reduce the number of burrows available for winter hibernation (Sharps and Uresk 1990). Compaction of soils by livestock in riparian areas may eliminate the ability for amphibians to burrow underground in order to prevent desiccation or freezing (Duellman and Trueb 1986; Swanson et al. 1996). Overutilization of cover makes adults in tall herbaceous vegetation near wetlands susceptible to predators such as ravens (USDA Forest Service 2006b). Livestock grazing also adds excess nutrients to waterways and thereby degrades water quality (Hogrefe et al. 2005, p. 15; McGee & Keinath 2004, p. 32). Reduced survival of eggs and tadpoles can result from increased siltation, water temperatures, and fecal contamination (BTRT 1998).
Grazing can also contribute to the decline of beaver populations by precluding the production of forage necessary to sustain beaver populations (USDA Forest Service 2006c). Greater amounts of beaver activity in the past promoted boreal toad habitat but as beaver population declines occurred, so did habitat for the boreal toad (USDA Forest Service 2008d).
Timber Harvest
The impact of timber harvest on boreal toads depends greatly on the timing, method, spatial extent, configuration and location of harvest activities relative to boreal toad habitats (Maxwell 2000). Direct effects from timber harvest include mortality of toads crushed by equipment used during harvest activities (McGee & Keinath 2004, p. 32; Berg 2005). Boreal toads are particularly vulnerable to impacts of timber harvesting when the harvest activities occur within their dispersal range from breeding sites, and during the late summer when adults migrate into upland forested habitats (Id.). Clearcuts may influence boreal toad use of migration corridors due to the lack of moisture and increased heat within the clearcut (Bartelt 2000). Soil compaction from harvesting activities may reduce the availability of rodent burrows used by boreal toads as over wintering hibernacula (BTRT 2001). Prescribed burning may eliminate slash piles and downed woody materials that are used by boreal toads as refugia (BTRT 1998).
Disturbance of stream habitats from sedimentation is one of the greatest impacts of timber harvest on amphibian species (McGee & Keinath 2004, p. 32). Timber harvest activities typically include the development and maintenance of roads, which may also increase erosion and sedimentation in adjacent streams. These impacts have the potential to affect boreal toads most significantly during the larval life stage when they are limited to aquatic habitats. Timber management activities can also spread nuisance species and thereby indirectly reduce the habitat quality for the boreal toad (USDA Forest Service 2008c).
In general, any timber harvest activities that negatively affect the quality or quantity of wetlands within the current range of boreal toads can be harmful to this species (McGee & Keinath 2004, p. 32). Because many boreal toads in the Eastern population occur in forest
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habitats, timber harvest could be having significant population impacts (Corn and Bury 1989; Dodd 1991).
Energy and Minerals Management
Potential effects that may occur as the result of energy and minerals management include habitat loss and fragmentation resulting from construction of new roads, well pads, pumps and other facilities, utility lines (above and below ground), and related increases in human presence (vehicle traffic and construction activity) (BLM 2005). For example, hard rock mining claims are common in the area occupied by the Eastern population (see Section XI, Map 15).
Water Management
Water management projects have frequently had detrimental impacts on amphibian populations, especially in the arid areas of the western United States (Hogrefe et al 2005, p. 19). Stoddard et al. (2005) found that a substantial proportion of the streams within the range of the Eastern population have been negatively impacted by disturbance associated with water management and other types of disturbance to streams and associated riparian areas. Impacts due to water management include: 1) direct loss of habitat; 2) habitat fragmentation; and 3) detrimental alteration of natural hydrologic regimes.
Direct loss of habitat is caused by a variety of projects, including draining or filling of wetlands, water diversion for municipal or agricultural purposes, and inundation due to dam construction and reservoir filling (Hogrefe et al 2005, p. 19). Dams and large reservoirs may represent impassable barriers to boreal toad movement and thereby bisect a previously connected boreal toad metapopulation. Areas that have been de-watered due to wetland destruction or water diversion may also represent barriers to toad dispersal.
Stream channelization and bank stabilization may cause the loss or degradation of suitable riparian habitats (Hogrefe et al 2005, p. 19). Indirect effects due to this sort of activity may include decreased sediment retention, water quality degradation, and loss of the natural hydrologic processes that create oxbows and flooded wetlands (BTRT 2001).
Projects that alter natural hydrologic regimes could significantly decrease rates of reproduction and recruitment due to increased egg, larval, and metamorph mortality (Semlitsch 2002). For example, projects that unnaturally reduce the hydroperiod of wetlands may not allow sufficient time for development and metamorphosis prior to pond drying (Hogrefe et al 2005, p. 19). Conversely, projects that artificially lengthen the hydroperiod of wetlands can also threaten amphibian populations by allowing increased densities of invertebrate predators and the colonization and establishment of predaceous fishes (Hogrefe et al 2005, p. 19; Scott 1996; Skelly 1996). The replacement of ephemeral wetlands with developed water impoundments has also resulted in the loss of amphibian habitats (McGee and Keinath 2004, p. 37). In Utah, reservoir construction has likely inundated historic boreal toad habitats in several areas (Hogrefe et al 2005, p. 19). Wetland losses have occurred throughout Utah (Lee 2001) and are expected to continue.
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Pollutants
Boreal toads are exposed to many pollutants that are known to be harmful to amphibians (Berril et al. 1993; Hayes et al. 2002). In particular, rotenone and antimycin, two commonly used piscicides used within the range of boreal toads, are known to be toxic to boreal toad tadpoles (BTRT 2001, p. 12; Patla 1998). Adult amphibians may avoid water when it becomes toxic, and although this behavior may prevent direct mortality from poisoning, it may subject amphibians to other threats such as predation and dehydration (Hogrefe et al. 2005, p. 12). Poisoning may also result from application of other types of pesticides that are used for forest management and animal control, such as herbicides and insecticides (BTRT 2001). High levels of salinity due to road runoff may also affect boreal toad equilibrium (Dole et al. 1985). Stoddard et al. (2005) found that a high proportion of streams within ecoregions occupied by the eastern clade have high levels of salinity.
Recreation
Humans frequently congregate near water bodies for recreation activities, including camping, fishing, hiking, biking, and off-road vehicle use. These activities can cause direct mortality of eggs, tadpoles, and metamorphs due to trampling or vehicle impacts (Hogrefe et al. 2005, p. 15). Amphibians in or near recreational areas are also at risk of mortality as a result of handling by humans and killing by human pets (Reinkling et al. 1980). Additionally, recreation activities can degrade bank conditions, degrade water quality, and increase the abundance of ravens, jays, raccoons, skunks, and other potential amphibian predators that are attracted to human refuse (Hogrefe et al. 2005, p. 17). Human movement among water bodies may also facilitate the transfer of pathogens among boreal toad populations (Hogrefe et al. 2005, p. 15).
Upland habitats may also be degraded through recreation activities including skiing, hiking, and off-road vehicle use. Road, trail, and slope construction for these activities may fragment and degrade suitable upland habitats and dispersal corridors for boreal toads (Hogrefe et al. 2005, p. 15). These activities may also attract predators due to deposition of refuse and human waste (Hogrefe et al. 2005, p. 15).
Within the range of the Eastern population, recreation is widespread and is currently thought to be having negative impacts in particular areas occupied by boreal toads in Colorado and Utah. For example, reproduction is thought to be limited in a reintroduced population of boreal toads in Rocky Mountain National Park due to heavy fishing use that results in trampling of eggs and metamorphs (BTRT, pers. comm., March 2011). Similar impacts have been documented in Utah (UDWR 2005). As another example, in the Fishlake National Forest in Utah, off-road vehicle use destroyed boreal toad habitat along the north shore of Barney Lake (USDA Forest Service 2006a).
Residential and Commercial Development
In some parts of the boreal toad’s range, residential and commercial development has occurred in and near several historic habitats and may account for the extirpation of boreal toads from these areas (Thompson et al. 2004). In Utah, for example, several potential and historic
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habitats along the Wasatch Front have been developed as ski resorts or high-priced housing and are experiencing rapid rates of human population growth (Lee 2001). In Colorado, historic boreal toad habitat has been developed for ski resorts, and ski area expansions are proposed in areas of currently occupied boreal toad habitat (e.g. the Breckenridge Peak 6 proposed ski area expansion). But many boreal toad populations in the Southern Rockies, Utah, northeastern Nevada, and southern Idaho occur in remote, high elevation habitats that currently face little threat from commercial or residential development. Residential and commercial development currently impacts many areas within the range of the Eastern population (See Section XI, Map 16).
Roads
Roads fragment habitats and may prevent migration among different habitat types and subpopulations. Amphibians are particularly vulnerable to road kill mortalities during mass migrations to or from breeding habitats across roads (Koch & Peterson 1995). In some studies, road kill mortalities have caused substantial impacts on the population level of amphibians (Lehtinen et al. 1999).
Roads and associated fragmentation are common in and adjacent to boreal toad habitats within the range of the Eastern population (see Section XI, Map 17). For example, in Utah, roads pass through many historic and occupied boreal toad habitats, and several mortalities due to vehicle impacts have been observed (Fridell et al. 2000; Hogrefe et al. 2005, p. 17). Other detrimental factors associated with roads, including pollutants, erosion and stream sedimentation, exhaust emissions, vibrations, and noise, may also affect anuran densities either by causing direct mortality or interrupting behavior (Buchanan 1993). Roads can also alter patterns of water flow which sustain aquatic habitats upon which boreal toads depend (BTRT 2001).
In sum, habitats for boreal toads are subjected to a variety of threats. Any action that harms or destroys boreal toad habitat is likely contributing to the decline of boreal toads.
IV. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes
There is very little information on the extent to which boreal toads are collected or harvested for biological or commercial purposes (McGee and Keinath 2004, p. 37). Worldwide, the collection and harvest of amphibians for commercial use is extensive, and hundreds of millions of amphibians are collected and/or killed every year (Pough et al. 1998).
The potential threat to boreal toads from harvest and commerce may be significant since non-indigenous predators (e.g. bullfrogs) are sold in pet stores along with other exotic species that may prey on boreal toads and act as vectors for diseases such as chytrid fungus if released into the wild (Daszak et al. 1999).
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V. Disease or Predation
A. Disease
Boreal toads are susceptible to a variety of bacterial and fungal pathogens which have been documented within the boundaries of the Eastern population of boreal toads. But he primary pathogen of concern for boreal toad in the Southern Rocky Mountains is chytrid fungus (Hogrefe et al. 2005; McGee & Keinath 2005). Only one species of chytrid fungus, Batrachochytrium dendrobatidis, is known to be parasitic on amphibians (Fellers et al. 2001).
Chytrid is a microscopic, parasitic fungus that attacks the keratin and skin of amphibians and has caused 90-100 percent mortality rates in metamorphosed amphibians (McGee & Keinath 2004, p. 44). Populations of boreal toads infected with chytrid fungus have declined to near extinction within one year, and there are no documented cases of an infected population recovering following infection. Adult toads infected with chytrid exhibit symptoms such as lethargy and reluctance to flee, skin abnormalities, loss of righting reflex, and extended back legs (Fellers et al. 2001; National Wildlife Health Center 2001). Healthy tadpoles generally have oral discs with keratinized jaw sheaths and tooth rows that are heavily pigmented. In tadpoles infected with chytrid fungus, these structures are abnormally formed or lack pigment. This type of deformity may inhibit tadpole foraging ability (Fellers et al. 2001).
The exact mechanism that causes mortality in chytrid-infected individuals is not well understood (Sredl 2000). Potential mechanisms include disruption of water, oxygen, and ion exchange through the skin and secretion of a toxin by the fungus (Berger et al. 1998; Pessier et al. 1999). Carey (1993) hypothesized that some environmental factor or synergistic effects of more than one factor may stress boreal toads, causing suppression of the immune system or indirectly causing immunosuppression by effecting elevated secretion of adrenal cortical hormones. Boreal toads may be particularly susceptible to population declines from chytrid fungus because most infected toads die from the disease before reaching sexual maturity.
Preserved specimens of leopard frogs and at least one boreal toad, which were collected in Colorado in the 1970s, have tested positive for chytrid fungus indicating the pathogen has been present in at least some locations in the Southern Rocky Mountains since at least that time, and that the declines that occurred in the mid to late 1970s and early 1980s may have been caused by the chytrid fungus (Milius 2000).
Chytrid fungus has associated with declines of boreal toad throughout the Southern Rockies (National Wildlife Health Center 2001; Daszak et al. 2000). Chytrid fungus is widespread in Colorado (BTRT 2001-2006). In 2006-2007, 53 of 80 monitored sites with boreal toad populations were tested for chytrid fungus. Of these sites, 17 sites tested positive for chytrid fungus. In addition, chytrid fungus continues to appear in new locations in the state on a regular basis.
Chytrid fungus infection has been documented in one population of boreal toads in Utah, found along the East Fork Sevier River on the Paunsagunt Plateau (Thompson et al. 2004;
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UDWR 2005-2009). It is the suspected cause of several mortalities in Utah observed in recent years (Hogrefe et al. 2005, p. 13).
Amphibians are susceptible to infection from pathogens other than chytrid fungus. The bacterium Aeromonas hydrophila is present in many environments and can cause red-leg disease in amphibians (Hogrefe et al. 2005, p. 13). In addition, Blaustein et al. (1994a) identified the spread of a pathogenic fungus called Saprolegnia ferax that appears to be largely responsible for egg mortality in a boreal toad population in Oregon (Blaustein et al. 1994; Kiesecker and Blaustein 1997; Kiesecker et al. 2001). Saprolegnia is commonly carried by fish (Seymour 1970, Richards and Pickering 1978) and may be introduced to amphibian habitats via sport fish stocking (Kiesecker et al. 2001). Once introduced to a system, individual amphibians may transmit the pathogen to other populations as they migrate or disperse. Finally, limb malformations in toads have been linked directly to trematode infections by Ribeiroia ondatrae (Johnson et al. 2001; Johnson et al 2002), although the impacts of these infections on reproduction, and the magnitude of the infections across the breeding range, require further study. Preliminary analysis suggests that limb malformations may increase mortality in larval amphibians prior to and during metamorphosis.
B. Predation
In adult boreal toads, toxic skin secretions are effective repellents to some predators (Flier et al. 1980; Brodie and Formanowicz 1987). However, many animals are not deterred by this defense and boreal toads have many native predators, including common raven (Corvus corax) (Olson 1989, Corn 1993), gray jay (Perisoreus canadensis) (Beiswenger 1981), predaceous diving beetle larvae (Dytiscus sp.) (Livo 1998), western garter snake (Thamnophis elegans) (Arnold and Wassersug 1978), tiger salamander (Ambystoma tigrinum) (Hammerson 1982), and several other terrestrial vertebrates (Jones et al. 1999, Jones and Stiles 2000). Nonnative species such as raccoons (Procyon lotor) are also boreal toad predators (Jones et al. 1999).
Potential boreal toad predators are widespread throughout the range of the eastern clade and are suspected to be depressing toad populations in particular areas (UDWR 2009). For example, possible significant predation on boreal toads by birds also has been observed in Colorado and Idaho (Hammerson 1999). In addition, many fish that prey on toads have been transplanted into drainages where there were historically never present (Baxter and Stone 1995). Predation by introduced fishes is discussed further below, as invasive species is one of the “Other Natural or Anthropogenic Factors” affecting boreal toads.
Boreal toads may be especially susceptible to predation during breeding (Olson 1989, Corn 1993) because they are concentrated and relatively visible compared to other times of year. However, communal breeding, communal oviposition, and explosive breeding seasons may reduce the individual predation risk to adult boreal toads through dilution of predator effects (Hamilton 1971, Kagarise Sherman 1980).
To summarize, disease is the primary threat facing boreal toads in the Southern Rocky Mountains. The detection of chytrid fungus in Utah indicates that the disease may also be
28 impacting boreal toads elsewhere in the Eastern population. Impacts from predation may be severe in some locations and predation from introduced fishes in particular may be contributing to the decline of boreal toads.
VI. Inadequacy of Existing Regulatory Mechanisms
Most of the existing regulatory mechanisms for the boreal toad have been in place for years without any progress towards reversing the trend toward extinction. These regulatory mechanisms are discussed below.
The boreal toad is listed as a state endangered species in Colorado and New Mexico (Colorado Division of Wildlife 2010; New Mexico Dept. of Game and Fish 2010). See Colorado Rev. Stat. §§ 33-2-101 et seq.; New Mexico Stat. Ann. §§ 17-2-37 et seq. The endangered designation provides the basic mandate for the state agencies in Colorado and New Mexico to conserve the boreal toad and prohibits the collection, possession, or sale of this species. Consistent with this duty, a recovery plan for the boreal toad in Colorado was prepared in 1994 Colorado (Nesler and Goettle 1994), and the New Mexico Department of Fish and Game prepared a recovery plan for the toad within New Mexico in 2006 (New Mexico Department of Game and Fish 2006). The status of boreal toads in these states has not improved despite protection as an endangered species, likely in large part because these designations offer no protection for boreal toad habitat (McGee & Keinath 2004, p. 46).
In Wyoming, the boreal toad carries the designation of Native Species Status 1, which means that the species and its habitat is declining (McGee & Keinath 2004, p. 46). In Utah, decline prompted the Utah Division of Wildlife Resources to classify boreal toad as a state sensitive species (Utah Data Conservation Center 2010). See State of Utah Rule R657-48. Although Wyoming and Utah have recognized the decline of the boreal toad in these states through these designations, the designations carry no legal or regulatory weight. In Idaho, boreal toads are protected from collection as nongame species, along with all other native amphibians in the state. IDAPA 13.01.06.200. Boreal toads are without special status in Nevada (Nevada Natural Heritage Program 2010).
The U.S. Forest Service Region 2 (including Colorado and portions of Wyoming) and Region 3 (including New Mexico) classify the boreal toad as a sensitive species (USDA Forest Service 2009; USDA Forest Service 2007b). In addition, the boreal toad is on the Bureau of Land Management’s sensitive species lists in Wyoming, Colorado, Utah, and Idaho (BLM Wyoming 2010; BLM Idaho 2010; BLM Utah 2011; BLM Colorado 2009). But sensitive species designations afford little protection, requiring only that the impacts be considered but not preventing actions that would harm the boreal toad. Thus, the Forest Service or the BLM can conclude in a Biological Evaluation that individuals or populations will be harmed or destroyed by an action, but still carry out this action. The USDA Forest Service in Region 4 (including western Wyoming, southern Idaho, Nevada, and Utah) does not list the boreal toad as a sensitive species, and as such, impacts on boreal toads from activities in national forests within this region are not even considered (USDA Forest Service 2008a).
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The majority of boreal toad habitat in the Southern Rockies is on land managed by the U.S. Forest Service (USFS), so Petitioners reviewed all of the forest plans that cover the range of the Southern Rocky Mountain boreal toad population. Petitioners identified just two forest plans in the Southern Rockies that contain standards and guidelines specific to boreal toad: the White River Forest Plan in Colorado and the Medicine Bow Forest Plan in Wyoming.
The White River Forest Plan includes the following standards for boreal toad:
Allow no loss or reduction in habitat quality of occupied or known historic boreal toad or leopard frog habitat; Maintain adequate vegetation cover around occupied boreal toad or leopard frog breeding ponds when implementing management activities to minimize avian predation on newly metamorphosed frogs and toads; Use only chemical herbicides shown to have no effect on boreal toads or leopard frogs, or use other vegetation management techniques, within 300 feet of occupied or known historic boreal toad sites; and Do not use fish toxins with the potential to harm boreal toads or leopard frogs in occupied boreal toad and leopard frog habitats
(USDA Forest Service 2009b, p. 2-25).
The Medicine Bow Forest Plan contains the following standards:
Allow no loss or degradation of known or historic habitat for the boreal toad, wood frog, or northern leopard frog; and Forest Service employees working in boreal toad habitat will disinfect waders (nets and other items that come in contact with the water) with 10% bleach solution before moving between ponds or drainages to reduce the likelihood of chytrid fungus and other disease transmission.
(USDA Forest Service 2003, p. 1-44).
Although these standards are enforceable in these two forests, the White River and Medicine Bow national forests cover only a small proportion of the range of the Southern Rocky Mountains population. In addition, the standards do not adequately address all of the threats to the persistence of the boreal toad.
In 1994, a Boreal Toad Recovery Team for the Southern Rocky Mountains was formed of agency representatives from the FWS, Colorado Division of Wildlife, Wyoming Game and Fish Department, New Mexico Department of Game and Fish, National Park Service, U.S. Geological Survey, U.S. Environmental Protection Agency, U.S. Forest Service, and Bureau of Land Management, along with technical advisors from several universities and other interested parties. In addition to producing a recovery plan for the boreal toad in Colorado (Nesler and Goettle 1994), the Team prepared a conservation plan in 1998 (BTRT 1998) that was revised in 2001 (BTRT 2001). Similarly, the Utah Division of Wildlife Resources developed a
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conservation plan for boreal toads in 2005 (Hogrefe et al. 2005). Boreal toads in northeastern Nevada and southern Idaho do not appear to be covered by a conservation plan.
To evaluate the conservation plan and the implementing conservation agreements, FWS should apply its “Policy for Evaluating Conservation Efforts” (“PECE”). See 68 Fed. Reg. 15100 (March 28, 2003). The policy identifies two sets of criteria FWS must use in this evaluation. The first set of criteria relate to the certainty that the conservation effort will be implemented, and include among other things whether the “staffing, funding level, funding source, and other resources necessary to implement the effort are identified,” whether there is “a high level of certainty that the party [or parties] to the agreement or plan that will implement the conservation effort will obtain the necessary funding,” and whether “an implementation schedule (including completion dates) for the conservation effort is provided.” The second set of criteria developed by the U.S. Fish and Wildlife Service relate to the certainty that the conservation effort will be effective. As explained more fully below, using these criteria, any conservation program based solely on the implementation of voluntary measures – as in the conservation agreements for the boreal toad in the Southern Rocky Mountains and Utah – would be insufficient to address the threats faced by the boreal toad.
Uncertainty as to Implementation and Effectiveness of the Southern Rocky Mountains Conservation Plan
The Southern Rocky Mountains conservation plan provides guidance to all participating agencies in regard to management and conservation of the boreal toad and its habitat and provides an opportunity for each agency to sign a conservation agreement to define and confirm its commitment to boreal toad conservation. Several state and federal agencies plus the Colorado Natural Heritage Program have signed such agreements (Jackson 2008, p. 5).
Activities guided by the conservation plan include annual monitoring of known breeding populations; research of factors limiting toad survival; research of toad habitat, biology, and ecology; captive breeding and rearing techniques and protocols; experimental reintroductions of toads to vacant historic habitat; coordination with land management agencies, land use planners, and developers to protect the boreal toad and its habitats; and efforts to increase public education and awareness of the subspecies.
The Southern Rocky Mountains Conservation Plan is a voluntary, nonbinding agreement with no means of enforcement. This is stated in the conservation plan: “Federal, State, and private parties wishing to commit to participating in the implementation of parts of, or the entirety of this plan, can make that commitment through Conservation Agreements . . . .” (BTRT 2001, p.3). There is no penalty if signatories do not follow conservation plan, or even their specifically entered conservation agreements, nor can they be sued by the public or one of the other parties for noncompliance. As such, the conservation plan is not a regulatory mechanism, but instead a set of voluntary guidelines that may or not be followed. Another important factor that demonstrates uncertainty as to implementation is the fact that none of the conservation agreements include implementation schedules.
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Without mandatory and enforceable regulatory mechanisms, when the state or federal agencies are faced with tough management decisions, such as where conservation of the boreal toad conflicts with other aspects of the multiple use mandates of the agency (e.g. managing lands for timber yield or grazing allotments), the toads are likely to lose. Similarly, when they encounter tough budget decisions, such as where there is a choice between funding action for the boreal toad or another program, there will be little incentive for them to choose the toad.
Problems of budgeting priorities are compounded by the fact the conservation plan and the conservation agreements lack secure sources of funding. Appendix A of the conservation plan includes the conservation agreements entered by the participating state and federal agencies. All of the activities included in conservation agreements are “contingent on adequate funds being made available and allocated to the signatory agency.”
The U.S. FWS Region 6 states that it will provide funding through the Section 6 process to the Recovery Team or states involved in implementation, but no specifics are provided. In addition, funding under Section 6 is only available to assist in the development of programs for the conservation of endangered and threatened species, or to assist in monitoring the status of candidate species. Because the boreal toad is no longer a candidate species, FWS funding through Section 6 process is no longer available for implementation of the boreal toad conservation plan.
In the past, the Colorado Division of Wildlife (CDOW) has funded aspects of implementation of the recovery plan. But at the current time, funding for the Colorado Division of Wildlife is uncertain due to shortfalls in Colorado’s state budget. The State Senate recently passed Senate Bill 203 that reduces the amount of money that will be moved into the Native Species Conservation Trust Fund, which provides funding to implement conservation programs for nongame species in Colorado (see http://www.leg.state.co.us/clics/clics2011a/csl.nsf/BillFoldersSenate?OpenFrameSet). Thus, there will be less funding for nongame programs, including boreal toad recovery. The Colorado Division of wildlife also funds various programs to protect nongame species outside of the Species Conservation Trust Fund program. These programs are predominantly funded out of the Wildlife Cash Fund and Great Outdoors Colorado board grants. CDOW has used these funds in the past to fund boreal toad conservation activities and are planning to fund some boreal toad conservation activities out of those funds this year. But there is substantial uncertainty about the amount of funding that will available to spend on boreal toad conservation activities from these funds due to the potential for shifting CDOW priorities, anticipated shortfalls in the State of Colorado’s budget, and the potential for future cuts associated with ongoing efforts to balance the budget. Even if Colorado Division of Wildlife funding continues at current levels, it is not sufficient to fund all of the conservation activities that will be necessary to achieve the goals of the conservation plan.
In addition, the Federal land management agencies that manage boreal toad habitat and could fund aspects of the recovery plan are also facing budget shortfalls. Given that boreal toad is not a candidate species, it will be low on the list of priorities for limited federal funding.
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Under the “Policy for Evaluating Conservation Efforts,” the fact that staffing, funding level, funding source, and other resources necessary to implement the effort have not been specifically identified is an indication of uncertainty as to whether the activities will be implemented. To be sure, the conservation plan itself recognizes that “without a significant commitment of funds and time from all the involved agencies, recovery may be difficult, if not impossible, to achieve in the foreseeable future” (BTRT 2001, p. 4).
Moreover, the conservation agreements entered by the participating state and federal agencies include few specific actions and none commit to specific measures that would protect boreal toad habitat. Most of the commitments deal with research or surveying and monitoring activities. For example, the USFS, Wyoming Game and Fish Department, National Park Service, and BLM commit to assist with survey and monitoring of boreal toad populations on lands within their jurisdictions. The USFS Rocky Mountain Region commits to utilize their air quality experience to further research into toad declines, and the USGS Biological Resources Division commits to various research projects, including global warming and UV radiation impacts on boreal toads.
The remaining commitments largely reiterate preexisting statutory or regulatory requirements on the agencies. For example, the USFS Rocky Mountain Region commits to “exercise authority for the maintenance of biological diversity on national forests and for the protection and management of sensitive species (including the boreal toad) as provided in the Forest Service Manual.” At the time the USFS entered into this conservation agreement, they were operating under regulations implementing the National Forest Management Act that required them to ensure the viability of vertebrate species, but new proposed regulations have weakened this requirement. See 76 Fed. Reg. 8480.
Likewise, FWS Region 6 commits to reviewing and providing comments under the authority of Section 7 of the ESA for federal actions, the Fish and Wildlife Coordination Act for actions requiring Clean Water Act section 404 permits, and on water development projects regulated under the Federal Energy Commission. But because the boreal toad is not currently a candidate for listing under the ESA, the FWS would be unlikely to review and provide comments on federal actions that may negatively impact boreal toads. The Wyoming Game and Fish Department commits to enforcing the state law prohibiting the take of boreal toad. Yet the state does not consider habitat modification to be a “take” so this commitment will do little to address most threats to boreal toads within the state.
None of the conservation agreements include specific regulatory measures to protect the habitat of boreal toads from harmful land management activities. In the conservation agreement, USFS Rocky Mountain Region committed only to considering whether one or more Forest Plan amendments would be appropriate, and the USFS Carson National Forest committed to “consider” possible impacts of forest management decisions and plans on boreal toads and their habitat. Instead of making firm commitments to protect the toads, the USFS Carson National Forest merely offers the vague pledge to “take measures to avoid and/or mitigate such impacts whenever possible within the constraints of Forest Service policy and regulations.” As discussed above, Petitioners could find only two national forests with standards aimed at protecting boreal toads.
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Another example of a vague commitment in the conservation agreements is that of the National Park Service, Rocky Mountain National Park. It commits to “protect boreal toads and all suitable habitat in Rocky Mountain National Park from undue human disturbance by managing to protect and/or restore natural conditions and processes to the extent authorized by law.” Similarly, the BLM commits to “protect any boreal toad populations and suitable habitat which may be located on BLM lands from negative impacts which may be caused by other land use activities.” But neither agency commits to any of the specific conservation measures recommended in the conservation plan. And although these agencies that manage boreal toad habitat have taken some site-specific actions in particular locations aimed at better protecting boreal toad habitat, the lack of comprehensive regulatory protections has resulted in continued authorization of management activities that harm boreal toads and their habitat such as concentrated recreation, road-building, mining, grazing, or timber harvest.
Even if the all of the conservation actions described in the conservation plan were accomplished, the species would still likely not be recovered absent protection under the ESA. This is because the conservation plan is inadequate to address the serious threat posed by the deadly chytrid fungus.
As discussed above, chytrid fungus is the primary threat to the boreal toad and the disease continues to spread and cause population declines and losses despite significant research and effort into addressing the problem. There is still no effective strategy available to protect populations that are currently chytrid-free from becoming infected and declining, or to prevent populations currently infected with chytrid from continuing to decline. The conservation plan attempts to address the threat of chytrid fungus by: 1) translocating toads to suitable unoccupied habitats that are free of chytrid fungus to increase the number of chytrid free populations; and 2) conducting research on chytrid fungus, including research seeking strategies to facilitate increased resistance to chytrid.
To date, translocation efforts have been undertaken at four sites in Colorado. Of the four translocated populations (Red Mountain, Kanah Creek, Zimmerman Lake, Mysterious Creek), two are in sites where chytrid fungus has been detected (Red Mountain and Kanah Creek), one (Mysterious Creek) experienced loss of all sentinel tadpoles within two weeks of reintroduction (but is still chytrid free and may be a site for future translocation), and one (Zimmerman Lake) has been stocked every year since 2007 and is chytrid free, but still does not meet the viability criteria.
There are no additional translocation efforts planned in the near future in Colorado. This is likely due to limited funding and resources within the Colorado Division of Wildlife and the federal agencies that are signatories to the Conservation Plan, as well as difficulty in finding potential translocation sites with suitable habitat that are chytrid-free and without impending habitat threats.
In New Mexico, translocation took place at one site (Trout Lakes). Reproduction has occurred at this site but chytrid has been detected and the site receives heavy recreational pressure and does not yet meet the viability criteria. Translocation at an additional site (Lagunita
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Lakes) is planned in the future if sufficient funding is available. It appears that there are no current or proposed reintroduction sites in Wyoming.
Because of the limited success of existing translocation efforts and lack of suitable sites for future translocations, it is evident that the current emphasis on translocation in the conservation plans is unlikely to address the threats faced by boreal toads. In addition, although research on chytrid fungus (including research seeking strategies to facilitate increased resistance to chytrid) is essential, these research efforts have not yet yielded solutions to the chytrid fungus problem, and substantial additional time and research funding is necessary. A federal listing could increase the amount of funding available and hasten the pace of important research.
The inadequacy of the conservation plan for the Southern Rocky Mountains is most clearly demonstrated by the fact that, except perhaps in a few localities, there has been no discernable impact on population trends in the region that can be directly attributable to these management actions (McGee & Keinath 2004, p. 46). The Colorado conservation plan has accomplished many of the actions that it describes, but, as of 2011, the plan has not come close to meeting its criteria for delisting the toad in Colorado. In 1999, there were six viable boreal toad populations in Colorado. When the plan was written in 2001, there was one viable population. This is still the case at the current time, despite the fact that the recovery plan has now been in place for more than eight years.
Though a number of the activities of the Southern Rockies conservation plan have been undertaken and the recovery team continues to do valuable work, the plan does not include regulatory mechanisms in place to ensure the conservation of the Southern Rocky Mountain population of the boreal toad. Because boreal toads have already been decimated by chytrid fungus and other threats, recovery in the region is likely unattainable without the additional resources and protections that would be available if the species was listed under the ESA.
Uncertainty as to the Implementation and Effectiveness of the Utah Conservation Plan
The Utah Boreal Toad Conservation Plan was developed to define current boreal toad distributions, determine critical ecology and life history information, identify the nature and magnitude of threats, and expedite the implementation of conservation actions for boreal toad (Hogrefe et al. 2005).
As with the Southern Rocky Mountains plan, implementation of conservation measures in the Utah plan are purely voluntary on the part of the land management agencies. The Utah plan acknowledges that the “cooperation of federal land management agencies, state agencies, and private landowners will be critical to the protection of boreal toad habitats” (Hogrefe et al. 2005, p. 31). But no agencies have committed to implementing any of these habitat management guidelines. With merely voluntary measures in the plan and no firm commitments to implement them by the relevant agencies, it is uncertain whether the plan will be implemented.
The conservation plan outlines habitat guidelines for land managers that could be adopted into management plans (Hogrefe et al. 2005, p. 31-33). But to our knowledge, no federal agency has incorporated these guidelines into their management plans, or systematically voluntarily
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implemented these guidelines on lands that they manage. The majority of boreal toad habitat in Utah is on U.S. Forest Service land and Petitioners reviewed forest plans to check for any conservation measures aimed at protection of boreal toads. The Ashley, Dixie, Fish Lake, Manti-La Sal, and Wasatch Cache forest plans contain no conservation measures specific to the boreal toad. The Uintah National Forest has the following guideline: “Protect known occupied boreal toad habitat from disturbance (e.g. trampling) during the active breeding season (generally four to five weeks following snowmelt).” But this conservation measure is provided as a voluntary guideline, not an enforceable standard, and is therefore not binding and does not constitute an adequate regulatory mechanism. In addition, the Uintah National Forest Plan covers only a small proportion of the range of the Eastern population, and this guideline does not address the full suite of threats that boreal toads face.
Uncertainty over the funding of the Utah plan also exists. Local and federal natural resource agencies have volunteered funding and personnel to the conservation of the boreal toad in Utah (Hogrefe et al. 2005, p. 1). Yet the plan does not detail these sources of funding or explain whether they will be renewed. In the past, boreal toad monitoring and conservation activities have been funded through Utah’s Endangered Species Mitigation Fund Grants. But because of budget shortfalls, this year the Endangered Species Mitigation Fund money paid the salaries of state nongame biologists, rather than to specific nongame projects, such as boreal toad monitoring. Petitioners are unaware of any secure sources of funding that will ensure that research projects and other actions in the Utah plan will be implemented in the future. The federal land management agencies face similar budget shortages.
Another problem is that the recommendations in the plan are without any schedule for implementation. For example, the conservation plan outlines several areas that deserve research, including habitat use and availability, population size, movements and more. But no specifics are provided as to when these actions should be completed. And a number of the conservation actions outlined in the conservation plan have not been completed in the six years since the plan was published. For example, the plan provides that threats to habitats should be identified during population monitoring and habitat responses to conservation measures and threats should be evaluated (Hogrefe et al. 2005, p. 31). But the 2009 monitoring report includes little in the way of identifying habitat threats or recording how habitat has responded to the past threats outlined in the conservation plan.
In addition, many of the habitat protection measures are vague and lack any specific direction on what they would entail. For example, the plan includes a measure to “Eliminate or reduce impacts of pesticides and contaminants” (Hogrefe et al. 2005, p. 32), but does not explain how this should be accomplished. No pesticide uses are prohibited and no pesticide use buffer strips are recommended. Similarly, it includes a measure to “Encourage local, state, and federal land use planning that minimizes impacts [from commercial and residential development] to boreal toad populations and habitat” (p. 32) but such a measure is unlikely to be implemented without any details on how to accomplish it.
The conservation plan identified major specific threats to boreal toad populations in nearly every region historically occupied by boreal toads (Hogrefe et al. 2005, p. 20-27). But to our knowledge, with a few minor exceptions, none of these threats have been addressed by Utah
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Division of Wildlife Resources or the federal agencies that manage boreal toad habitat in each of these regions. For example, the conservation plan states that boreal toad populations in West Box Elder County and the Bear River Range are being impacted by livestock grazing on public lands, which has severely degraded riparian areas that are known boreal toad breeding habitat, but does not recommend specific measures to address this documented threat, and the general grazing guidelines have not been adopted or systematically implemented by the federal land management agencies that manage this habitat in West Box Elder County or the Bear River Range.
Finally, even if the conservation measures were implemented, it is uncertain whether they would be effective at recovering the boreal toad. The inadequacy of the conservation plan for Utah is most clearly demonstrated by the fact that, although the plan has accomplished some of the actions it describes, the plan has not yet come close to achieving its management objective despite being in place since 2005. The goal of the plan is to maintain or restore multiple, viable breeding populations in nine of the 14 mountain ranges or geologic areas in Utah where boreal toads historically occurred. As of 2009, only one population in Utah met the plan’s definition of viability. One additional population in another of the 14 mountain ranges/geologic regions met the criteria for viability in previous years but not in 2009, and the genetically unique Paunsangunt Plateau population “remains critically low and may be in jeopardy of extirpation.” And even the remaining “viable” population is small and at-risk due to isolation, and could suffer declines in the future from threats like chytrid fungus and habitat destruction. The conservation measures in the conservation plan do not adequately address any of these issues.
Though a number of the activities of the conservation plan have been undertaken and the Utah Division of Wildife Resources continues to do valuable work, the plan does not put adequate regulatory mechanisms in place to conserve boreal toads in Utah. Because boreal toads have already been decimated by a variety of threats, it is possible that the recovery in the region is unattainable without the additional resources and protections that would be available if the species was listed under the ESA, especially given that documented threats to most populations have not been addressed and that chytrid fungus has been detected in Utah.
For all these reasons, the inadequacy of existing regulatory mechanisms is a threat to the boreal toad now and in the foreseeable future.
VII. Other Natural and Anthropogenic Factors
Factors such as climate change, increased ultraviolet radiation, invasive species, and isolation may be contributing to the decline of the Eastern population of the boreal toad. Each of these is discussed below.
Climate Change
Several researchers have examined the likely impacts of climate change on amphibians. Amphibians may be especially susceptible to climate change because they are ectotherms, which means that their body temperature varies with their surroundings (Donnelly & Crump 1998).
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Changes in ambient temperature may influence amphibian behaviors, including those related to reproduction (Blaustein et al. 2001, p. 1808). Potentially, changes in ambient temperature on a global scale could disrupt timing of breeding, periods of hibernation, and ability to find food (Blaustein et al. 2001, p. 1808). Furthermore, global warming could potentially affect amphibians at the population level and could contribute to widely reported population declines (e.g. Blaustein & Wake 1995; Stebbins & Cohen; Ovaska 1977). Global warming could also have a number of indirect impacts on amphibians. For example, one potential consequence of global warming is the increased spread of infectious disease (Cunningham et al. 1996; Epstein 1997). To be sure, in parts of the Southern Rockies, chytrid fungus may be limited to lower elevations where climactic conditions facilitate optimal growth of the fungus. Warming temperatures may facilitate the spread of chytrid fungus into previously unaffected or little- affected areas at higher elevations in the Southern Rocky Mountains (Muths et al. 2008).
In the case of boreal toads, the primary threats from climate change are droughts and early or late season freezing temperatures (McGee & Keinath 2004, p. 41). These changes may cause breeding pools to dry up before larvae metamorphose into terrestrial life stages or may cause death to toads either before they enter hibernacula or after they leave hibernacula to move to breeding sites. In addition, Bartelt and others (2010) conclude based on their modeling study of boreal toads in southeastern Idaho that climate warming will increase the physiological cost of landscapes thereby limiting the activity for toads in different habitats.
The effects of climate change on boreal toads may have already been observed. Blaustein et al. (2001, p. 1806) found a non-significant trend for boreal toads to breed increasingly early, which was associated with increased temperature at a site in Oregon. Corn (2003, p. 624) explains that earlier breeding observed by Blaustein and others (2001) may have resulted from reduced precipitation, which has been associated with increased mortality of boreal toads.
Ultraviolet Radiation
Anthropogenic degradation of atmospheric ozone (Stolarski et al. 1992) may be causing an increase in levels of solar ultraviolet-B (UV-B; 290-315 nm). There is some evidence for recent UV-B increases in relatively undisturbed temperate latitudes (Blumthaler et al. 1997) and progressive increases at lower latitudes are anticipated (Worrest and Grant 1989, Zurer 1993). Amphibians may be particularly sensitive to changes in levels of UV radiation because their skin is not protected by hair or feathers and their eggs lack protective outer shells (Blaustein et al. 1994b, Corn 1998).
Among amphibians, boreal toads may be especially susceptible to increased UV-B radiation because they deposit their eggs in shallow water (Corn 1998). Worrest and Kimeldorf (1976) observed that enhanced UV-B radiation caused developmental abnormalities and mortality of boreal toad tadpoles as they approached metamorphosis. Boreal toad tadpoles exposed daily to high levels of UV-B radiation developed anomalous, concave curvatures of the spine, and abnormally thick and pigmented corneas at early stages of development. The radiation damage to the dorsal surface of the tadpoles was severe and the survival rate was reduced. Although this study demonstrates potential impacts of high levels of UV-B radiation, Corn
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(1998) cautions that the ecological relevance of the experiment is uncertain, because tadpoles were continuously exposed to UV-B radiation levels that were much higher than those observed in natural systems.
Other work suggests that UV radiation may decrease hatching success in natural systems. Blaustein et al. (1994b) found that boreal toad and Cascades frog in Oregon showed significantly lower photolyase levels compared to Pacific treefrog (Hyla regilla). Photolyase is an enzyme that repairs damage due to UV radiation exposure. In field experiments, hatching success of embryos exposed to UV radiation was significantly greater in Pacific treefrog than in boreal toad or Cascades frog. Moreover, boreal toad hatching success increased by 50 percent in habitats shielded from UV-B radiation. Kiesecker and Blaustein (1995) reported similar increases in hatching success of toad embryos shielded from radiation at the same sites in the following year. Corn and Muths (2002) proposed that temperature stress is as plausible a hypothesis as increased UV-B to explain episodes of high mortality observed in Oregon (Kiesecker et al. 2001). In addition, Kiesecker et al. (2001) observed catastrophic embryo mortality from S. ferax infection in shallow water that was protected from UV-B but not in water protected from UV-B.
Not all studies, however, have demonstrated detrimental impacts from UV-B radiation (Grant and Licht 1995; Blaustein et al. 1996). UV-B exposure did not appear to influence boreal toad hatching success in Colorado (Corn 1998), suggesting that UV-B radiation may not be contributing to observed population declines in the Southern Rocky Mountains. Additional experiments on boreal toad eggs from Colorado, Utah, Montana, and Washington showed no differences in hatching success with varying amounts of UV-B exposure (BTRT 2001). Effects of UV-B radiation have not been determined in Utah (Hogrefe et al. 2005). However, in Utah, habitat elevations are considerably lower and UV-B radiation levels are probably less than in Colorado.
Invasive Species
Nonindigenous species can potentially threaten boreal toads directly through predation, and indirectly as competitors for resources, vectors for pathogens, and as the target of management actions that may have ancillary affects on toads (e.g., use of piscicides, insecticides, or herbicides to control exotic species) (McGee & Keinath 2004, p. 38; BLM 2005, p. 3-25).
Invasive species are widespread throughout the range of the Eastern population. Stoddard et. al. (2005) found that a high proportion of the streams in areas occupied by the Eastern population are occupied by nonnative vertebrate species. For example, nonnative amphibians are present in 80% of the stream length in the Southern Rocky Mountain ecoregion in Colorado and the Wasatch and Uintah Mountain ecoregion in Utah (Stoddard et al. 2005).
Introduced salmonids at higher elevations are likely to present a significant threat to boreal toads that occupy high (> 800 meters) mountain lakes and streams because 95 percent of these lakes in the western United States were naturally fishless prior to stocking (Bahls 1992). In New Mexico, numerous streams and suitable boreal toad habitat continue to be stocked with exotic trout (USDA Forest Service 2002). All life stages of amphibians are subject to predation by introduced fishes (McGee & Keinath 2004, p. 38). Indirect effects of predation include:
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1. Adult avoidance of egg laying sites where predators are present (Resetarits and Wilbur 1989; Hopey and Petranka 1994); 2. Decreased larval foraging and growth rates as a result of staying in refuges to avoid predators (Figiel and Semlitsch 1990; Skelly 1992; Kiesecker and Blaustein 1998; Tyler et al. 1998); and 3. Decreased adult foraging, growth rates, and overwinter survival as a result of avoiding areas with fishes (Bradford 1983).
Bullfrogs (Rana catesbeiana) are a noninindigenous species that have been implicated as a cause of amphibian declines throughout the western United States (McGee & Keinath 2004, p. 39). All life history stages of amphibians may be vulnerable to predation from adult bullfrogs and eggs and larvae may be preyed upon by bullfrog tadpoles (McGee & Keinath 2004, p. 39). The cumulative impacts that bullfrogs have on native amphibian populations often result in reduced levels of species diversity (Lonsinger and Askew 2010).
Introduced species can spread pathogens to boreal toads. Bullfrogs can carry chytrid fungus without mortality, serving as a reservoir for the disease and vector for the transmission of the pathogen to boreal toads (Muths and Hero 2010; Schloegel et al. 2010). Blaustein et al. (1994) observed that the water fungus Saprolegnia, a common pathogen of fish species reared and released from fish hatcheries, has been associated with amphibian declines. This suggests that releasing hatchery raised fish into the wild may increase the risk of infecting amphibians with pathogens from fish. Additionally, pathogens introduced by nonindigenous species are suspected to act synergistically with other natural and anthropogenic caused threats. Kiesecker and Blaustein (1995) observed that the combination of UV radiation and Saprolegnia fungus increased occurrences of mortality in amphibian embryos.
There is relatively little information on the impact exotic weeds have on amphibians. However, there is some evidence that the presence of exotic aquatic vegetation enhances the survival of nonindigenous bullfrogs (Kupferberg 1997).
Moreover, management of weed and insect pests can be a significant threat to amphibians. Cultural control of invasive plant species through grazing practices can result in trampling of all life stages, as well as increased sediment and nutrient loads in waterways (USDA Forest Service 2007a). Mechanical or manual control can also harm boreal toads through incidental trampling or by reducing their cover from predation and UV radiation, and herbicides can be toxic to the species or its prey (USDA Forest Service 2007a).
Isolation
Many remaining breeding populations of boreal toad in the Eastern population are small and isolated (Hogrefe 2005, p. 15). For example, in Colorado, all but one of the monitored chytrid-free populations are at risk due to small population size and isolation.
Small, isolated populations are more susceptible to extirpations due to stochastic events, human impacts, and environmental factors (Soulé 1987; Begone et al. 1990). Lack of gene flow
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may cause loss of genetic variability due to random genetic drift (Wright 1931) and inbreeding depression may occur (Franklin 1980). Once these populations are extirpated, their isolation precludes genetic interchange and recolonization of habitat (Carey et al. 2005, p. 236).
In sum, several other natural or anthropogenic factors may be threatening boreal toads in the Eastern population.
VIII. CRITICAL HABITAT
Section 4(a)(3) of the Endangered Species Act and implementing regulations require that, to the maximum extent prudent and determinable, FWS designate critical habitat at the time the species is determined to be endangered or threatened. 16 U.S.C. § 1533(a)(3)(A)(i); 50 C.F.R. § 424.12; see also id. at § 1533(b)(6)(C). The Endangered Species Act defines the term “critical habitat” to mean:
i. the specific areas within the geographical area occupied by the species, at the time it is listed . . . , on which are found those physical or biological features (I) essential to the conservation of the species and (II) which may require special management considerations or protection; and
ii. specific areas outside of the geographical area occupied by the species at the time it is listed . . . , upon a determination by the Secretary that such areas are essential for the conservation of the species.
Id. at § 1532(5)(A).
Petitioner expects that FWS will comply with this unambiguous mandate and designate critical habitat concurrently with the listing of a distinct population segment of the boreal toad. All areas within the DPS that are occupied by boreal toads should be designated, along with additional areas that could provide connectivity between existing populations. In short, all habitat utilized for breeding, shelter, movement, and foraging meet the definition of critical habitat and must therefore be designated as such.
IX. CONCLUSION
Petitioners have assessed the best scientific information available regarding the past, present, and future threats faced by boreal toad and have determined that the Eastern population of boreal toads is in danger of extinction throughout all of its range (Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho). Specifically, the Eastern population of boreal toad is threatened by the following factors: present or threatened destruction, curtailment, or modification of habitat or range; disease; predation; inadequacy of existing regulatory mechanisms; climate change; ultraviolet radiation; and invasive species. Based on this information, boreal toads in the Southern Rocky Mountains, Utah, northeastern Nevada, and southern Idaho must be listed as a distinct population segment under the Endangered Species
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Act. In the alternative, boreal toads in the Southern Rocky Mountains should be listed as a distinct population segment.
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XI. MAPS
MAP 1: Rough boundaries of the Eastern Distinct Population Segment. The boundaries include the portion of the gross range of Anaxyrus boreas mapped by the IUCN, within the rough boundaries of the clade identified by Switzer et al. 2009 and Goebel et al. 2009 (digitized from paper maps in Switzer et al. 2009 and Goebel et al. 2009).
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MAP 2: Rough boundaries of the eastern clade, and locations of genetic samples, from Goebel et al. 2009 and Switzer et al. 2009 (digitized from paper maps in Goebel et al. 2009 and Switzer et al. 2009).
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MAP 3: Boundaries of the Southern Rocky Mountains Distinct Population Segment. Boundaries include the portion of the gross range of A. boreas in the Southern Rocky Mountains.
:
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MAP 4: Proportion of the gross range of Anaxyrus boreas that would be lost if the Eastern population was lost.
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MAP 5: Proportion of the gross range of Anaxyrus boreas that would be lost if the Southern Rocky Mountains population was lost.
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MAP 6: Forest cover and thus boreal toad habitat is generally less contiguous and more patchy and isolated in the area occupied by the Eastern population and the Southern Rocky Mountains population, when compared with most of the rest of the range of Anaxyrus boreas.
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MAP 7: The Southern Rockies DPS occupies the Southern Rockies Ecoregion, which is an unusual ecological setting when compared with ecological settings occupied by Anaxyrus boreas throughout the remainder of: 1) the Eastern population, and 2) the range of the species.
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MAP 8: Boreal toads in central Utah occupy the Wasatch and Uintah Mountains ecoregion, which is an unusual ecological setting when compared with ecological settings occupied by Anaxyrus boreas throughout the remainder of: 1) the Eastern population, and 2) the range of the species.
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MAP 9: Boreal toads on the Paunsagunt Plateau in southern Utah occupy an ecotone at the southern range margin, which is an unusual ecological setting when compared with ecological settings occupied by Anaxyrus boreas throughout the remainder of: 1) the Eastern population, and 2) the range of the species.
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MAP 10: Boreal toads in the Eastern population in northeast Nevada and southeastern Idaho occupy a unusual ecological setting in a transition zone between the Middle Rockies, Northern and Central Basin and Range, and Wasatch and Uintah Mountains ecoregions, where boreal toad habitat goes from being relatively continuous to being naturally patchy and isolated.
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MAP 11: Areas in southern ID, northeastern NV, and northwestern WY where small amounts of gene flow across the boundaries of the eastern DPS are possible.
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MAP 12: In Nevada, the boundary of the Eastern distinct population segment should align with the western margin of the Bonneville Basin.
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MAP 13: Although there may be limited gene flow with populations to the north of the Eastern population in Idaho, the Snake River Plain likely forms a barrier that limits movement. It is unlikely that boreal toads are able to regularly successfully disperse across the majority of the Snake River Plain. Similarly, a large dissected lava plateau covered in sagebrush steppe vegetation likely forms a barrier that limits gene flow between toads in the Eastern population in southeastern Idaho and northwestern Utah from those in the southwest corner of Idaho. There are no reliable records of boreal toad occurrence in this dissected lava plateau. In addition the areas where gene flow might be possible between the Eastern population and Idaho in the Snake River Plain and the dissected lava plateau, have high density suburban and exurban development and human-caused fragmentation which is an additional barrier to gene flow See Map 16).
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MAP 14: Livestock grazing allotments in watersheds with boreal toad occurrences, and thus areas where boreal toad populations may be threatened due to impacts of livestock grazing.
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MAP 15: Locations of active hard rock mining claims in watersheds with boreal toad occurrences, and thus watersheds where boreal toads may be threatened by mining.
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Map 16: Exurban and urban areas and areas with a high degree of human-caused fragmentation in watersheds with boreal toad occurrences, and thus areas where boreal toad populations may be threatened with residential and commercial development and associated fragmentation.
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Map 17: Major roads and areas with a high level of human caused fragmentation in watersheds with boreal toad occurrences, and thus areas where boreal toad populations may be threatened due to impacts associated with roads. Note that this map only displays major highways.
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