Bufo nelsoni Stejneger, 1893
Editor's note: Following Frost (2000a), we have covered Amargosa toads (Bufo nelsoni) as Bufo boreas nelsoni in the boreal toad (B. boreas) species account (Muths and Nanjappa, this volume). However, most workers familiar with these animals agree that they deserve species status. The arguments for this position (further arguments can be found on the discussion board of AmphibiaWeb ) and what is known about the conservation status of Amargosa toads are presented as follows.
2Hobart M. Smith
3Robert W. Murphy
4David J. Morafka
Taxa in the B. boreas group have had varied histories, being considered species and subspecies at different times. For example, Stejneger (1893) considered B. halophilus a species, but it is now commonly treated as a subspecies of B. boreas. Bufo exsul (black toads) has been particularly volatile, switching rank several times; they were described as a species (Myers, 1942a), treated as a subspecies of B. boreas (Tihen, 1962; Schmidt, 1953), and again as a species (Schuierer, 1962, 1963; Feder, 1977; Stebbins, 1985). Some nominal taxa such as B. boreas columbiensis, B. nestor, and B. pictus are no longer considered by current authorities. Similar taxonomic instability is seen in other North American bufonids, such as the Bufo americanus group (Blair, 1941; Frost, 2000a).
Nomenclatural History of B. nelsoni. Bufo nelsoni was described as a subspecies of Bufo boreas (Stejneger, 1893). Camp (1917b) stated that the two samples described by Stejneger as nelsoni represented B. halophilus; subsequently, Stejneger did not include nelsoni as a subspecies or species in later checklists (Stejneger and Barbour, 1917, 1923, 1933, 1939). Despite this history of rejection, many species lists, accounts, and field guides included nelsoni and treated it as a subspecies of B. boreas (Grinnell and Camp, 1917; Slevin, 1928; Linsdale, 1940; Myers, 1942a; Stejneger and Barbour, 1943; Pickwell, 1948; Wright and Wright, 1949; Stebbins, 1951, 1954a, 1972; Schmidt, 1953; Conant, 1956; Cochran, 1961; Banta, 1965; Collins et al., 1978, 1982; Collins, 1990, 1997; Stebbins and Cohen, 1995; Frost, 2000a,b; Center for North American Herpetology, 2002). A species list by Frank and Ramus (1995) treated nelsoni as a subspecies of B. halophilus, perhaps based on Camp (1917b).
Savage (1960b) was the first to refer to nelsoni as a species, and this stands as a proper nomenclatural change according to the rules of the International Code of Zoological Nomenclature (hereinafter the “Code,” International Commission on Zoological Nomenclature [ICZN], 1999). After Savage (1960b), many guides and papers treated nelsoni as a species (Savage and Schuierer, 1961; Karlstrom, 1962; Schuierer, 1963; Altig, 1970; Blair, 1972a; Bury et al., 1980; Maxson et al., 1981; Stebbins, 1985; Altig and Johnson, 1986; Altig and Dodd, 1987; Graybeal, 1993; Goebel, 1996a; Altig et al., 1998; Powell et al., 1998; Burroughs, 1999; Duellman and Sweet, 1999) as did many unpublished documents and dissertations (Feder, 1977; Altig, 1981; Maciolek, 1983a,b; Hoff, 1994, 1996; Clemmer, 1995; Goebel, 1996a; Heinrich, 1996; Stein, 1996, 1999; Stein et al., 2000; Sjoberg, 2000, 2001). Bufo nelsoni was listed as a full species on the Integrated Taxonomic Information System (2002) database compiled by the Smithsonian Institution with the highest credibility rating by their Taxonomic Working Group. Bufo nelsoni was consistently treated as a species within the Federal listing process (Federal Register, 1977, 1982, 1985, 1989, 1991, 1994, 1995, 1996) and in a petition to list Bufo nelsoni as an Endangered Species (Biodiversity Legal Foundation, 1994). Conservation programs treated Bufo nelsoni as a species (Burroughs, 1999; Nevada Division of Wildlife, 2000; Bureau of Land Management, 2002; Nature Conservancy, 2002). Thus, since 1960 nelsoni has been treated both as a species and a subspecies, although there has been considerable consensus by authors of original research and conservation measures in treating B. nelsoni as a species.
Frost (2000a,b) and Collins (Collins et al., 1978, 1982; Collins, 1990, 1997) provided critically important lists and commentaries on the scientific and standard English names for amphibians. These have been invaluable and influential to the scientific community (e.g., Muths and Nanjappa, this volume). But the variable treatment of nelsoni as a subspecies by some and a species by others has led to some unfortunate consequences. For example, species accounts on AmphibiaWeb (2002) provided no mention of nelsoni at all. Bufo nelsoni was not included as a subspecies of B. boreas (Garcia, 2002), perhaps because she believed it was a species. However, nelsoni was not given an independent species account because AmphibiaWeb provided accounts only for species recognized by the American Museum of Natural History (Frost, 2000b).
Similarly, by initially following Crother et al. (2000; but see Crother et al., 2003), Bufo nelsoni was not given a separate treatment in this volume (Muths and Nanjappa, this volume), which we now try to provide. First we review why nelsoni may not have been treated as a species. We then discuss morphological and genetic evidence and implications from the biogeographical history of the Great Basin. We conclude that B. nelsoni is a species and review conservation measures.
Is Bufo nelsoni a subspecies? Justification and publication. Both Frost (2000a,b) and Collins (Collins et al., 1978, 1982; Collins, 1990, 1997) treated nelsoni as a subspecies of B. boreas within their influential species lists. While neither provided a reason, it was probably due to a lack of any published, taxonomically sound justification for treating nelsoni as a species.
Frost (2000b) recognized Savage (1960b) as the first to treat nelsoni as a species, and that stands nomenclaturally. However, Savage did not provide any justification for that change. While justification is not required by the Code, acceptance by others generally requires some justification. Perhaps none of the many authors in the published literature cited above supplied taxonomically sound evidence for elevation, but certainly Feder (1977) did. She clearly stated that B. nelsoni was a species and provided allozymic data sufficient for taxonomic justification. Unfortunately, Feder’s work was not published in a format that is commonly accepted. Again, the rules of the Code do not apply to non-nomenclatural matters, such as publication issues discussed here. But the taxonomic literature generally follows guidance by the Code on a variety of matters, and the Code does not consider Master’s and Ph.D. dissertations as acceptable publications (Article 8). Thus, nelsoni may have been treated as a subspecies because Feder’s data were poorly distributed (due to lack of publication), not because her conclusions were discredited.
If unpublished sources are available, exceptions that do not involve new scientific names have been incorporated into the taxonomic literature, especially when they provide credit to authors (e.g., Myers, 1931). Feder’s dissertation is available on microfilm from both the University of California at Berkeley and the University of Montana. On these grounds, we regard Feder (1977) as a legitimate part of the citable (not necessarily published) literature on B. nelsoni. In fact, her dissertation has been cited in the published literature (Graybeal, 1993). Below, we provide some details from Feder (1977). We encourage readers interested in further documentation to examine her dissertation in its entirety.
Recently, Frost (2002) treated nelsoni as a species and included a reference to Feder’s (1977) work. Similarly, Collins and Taggart (2002) will treat nelsoni as a species. However, we provide a more thorough account of nelsoni here.
Morphological evidence. Taxonomic instability among North American bufonids, including B. nelsoni, may be due to limited morphological change and a lack of understanding of the evolutionary history of diagnosable morphological characters (Wright and Wright, 1949; Baldauf, 1959; Karlstrom, 1962; Tihen, 1962; Martin, 1972; Winokur and Hillyard, 1992). Many bufonid species groups have been identified based on morphological similarity, but the relationships within and among those groups have been difficult to determine (Tihen, 1962; W.F. Blair, 1964b, 1972a).
The original species account for nelsoni (Stejneger, 1893) did not give many diagnostic characters: "Diagnosis – Similar to B. boreas. Skin between warts smooth; snout protracted, pointed in profile; webs of hind legs very large; soles rather smooth; limbs shorter, elbows and knees not meeting when adpressed to the sides of the body; inner metacarpal tubercle usually very large." Both Linsdale (1940) and Wright and Wright (1949) noted the toad had small feet and reduced webbing, which was just the reverse of Stejneger’s (1893) account and may have been Stejneger’s original intention.
Stejneger concluded nelsoni was a subspecies: "This seems to be the southern form of Bufo boreas, distinguished from the latter as above. Extreme examples of both forms are very different and would readily pass for distinct species, but specimens occur in which one or the other of the characters are less developed, making it expedient to use a trinomial appellation." Linsdale (1940) concluded nelsoni was a valid subspecies of B. boreas based on its narrow wedge-shaped head, protracted snout, short limbs, and reduced webbing of the hind feet. Myers (1942a) distinguished B. exsul from nelsoni largely on the dark color of the former. Morphological characters of nelsoni are discussed by Wright and Wright (1949) and Karlstrom (1962), but both suggested that more comprehensive analyses were needed. Morphological analyses of tadpoles by Altig (1970), Altig and Johnson (1986), and Altig et al. (1998) treated nelsoni as a species based on allopatry, not on unique morphological characters.
Confusion about morphological characters may have led to specimen misidentification. Bufo nelsoni was reported from Pahranagat Valley, Lincoln County, Nevada and Hot Creek Valley, Nye County, Nevada (Linsdale, 1940), the north slope of Bullfrog Hills, Nye County, Nevada (Maciolek, 1983b), and Resting Springs, Morans, and Lone Pine, Owens Valley, California (Wright and Wright, 1949). Schuierer (1963) and Maciolek (1983b) concluded these sightings were not B. nelsoni, which is believed to occur only in Oasis Valley, Nye County, Nevada (Savage, 1960; Schuierer, 1963, Nevada Division of Wildlife, 2000). Bufo nelsoni may be a cryptic species better identified by collection site rather than specific morphological characters. It has been > 100 yr since the original description appeared, yet an understanding of the evolution of the North American bufonid groups based on morphology eludes us.
Genetic evidence. Feder (1977) analyzed allozymes in all taxa of the B. boreas group and found that nelsoni was distinct from all other members of the boreas group. Feder (1977, p. 37) concluded: "The designation of the two desert isolates as subspecies of B. boreas must now be reconsidered in light of this new genetic evidence. Specific status best describes the position of B. exsul and B. nelsoni within the Boreas group." Her conclusion was based on analyses of 360 metamorphosed individuals (302 from the B. boreas group, including 13 nelsoni and 58 outgroup individuals). Genetic distances were calculated from allele frequencies of 21 loci, 11 of which were variable within the B. boreas group. All samples of nelsoni had a unique allele for PGM, and nelsoni had unique allele frequencies at other loci. One allele at the ME locus (ME88) was fixed in both B. exsul and nelsoni but was found in low frequencies in populations of B. boreas nearest B. exsul and nelsoni. Phenetic dendrograms based on UPGMA and distance-Wagner cluster analyses both identified B. nelsoni as a unique lineage similar to B. exsul.
Goebel's (1996a, 2003) mitochondrial DNA analysis examined 194 samples from the B. boreas group including two from nelsoni. Phylogenetic analyses of restriction site data (378 base pairs) and control region sequences (834 base pairs) identified nelsoni as a unique lineage closely related to both B. exsul and some specimens of B. b. halophilus (B. b. halophilus was considered paraphyletic, closely related to both B. b. boreas and B. nelsoni).
Eric Simandle is analyzing microsatellite data from Great Basin boreal toads including Bufo nelsoni (E. Simandle, personal communication). More data from Simandle and others should give new perspectives on the evolution of B. nelsoni and the B. boreas group.
Implications from Biogeography: Isolated populations in the B. boreas group. Bufo nelsoni and Bufo exsul may be two of many species that persist in small, isolated populations surrounding the Great Basin. Myers (1942a) and Karlstrom (1962) hypothesized that B. boreas was widespread in the Pliocene, covering much of the coastal, Sierra, and Great Basin regions, and speciation in the group resulted from isolation in the Pleistocene. Climatic and geologic fluctuations in the Great Basin region during the Pleistocene resulted in repeated wet and dry cycles with an increasing trend toward dryness that resulted in increased fragmentation of drainages (Mifflin and Wheat, 1979; Axelrod and Raven, 1985; Stokes, 1986; Hovingh, 1997). Present distributions of northern leopard frogs (Rana pipiens), Oregon spotted frogs (R. pretiosa), western toads (Bufo boreas), Woodhouse's toads (B. woodhousii), red-spotted toads (B. punctatus), and tiger salamanders (Ambystoma tigrinum) are all consistent with fragmentation of populations in the Pliocene and Pleistocene within the Great Basin region (Green et al., 1996; Hovingh, 1997). Immunological data (Maxson et al., 1981) suggest that lineages in the B. boreas group separated in the Pleistocene. Schuierer (1963) suggested that toads in the lower Owens Valley were distinct and should receive subspecific status based on morphological variation. The pattern of mtDNA evolution is consistent with fragmentation of the B. boreas group in and surrounding the Great Basin as well. Isolated and genetically differentiated populations include boreal toads in Kane County, Utah (Goebel, 2003), and in Haiwee Springs, California (described below). Frost (2002) felt that geographic variation within B. boreas was poorly studied and might mask a number of cryptic species.
Murphy and Morafka (unpublished data) investigated an isolated population of “B. boreas” from Haiwee Springs (about 1,500 m elevation) in the Coso Range, China Lake Naval Weapons Center Station, Inyo County, California, using 834 base pairs of homologous control region nucleotides. The sequences from this population in the Mojave Desert were compared to those obtained from a number of B. b. halophilus from coastal areas of California and to nelsoni. Toads from Haiwee Springs clustered with nelsoni; only a single base pair separated the two. However, the population from Haiwee Springs also differed from B. b. halophilus by only one base pair. These small differences allowed genetic identification of toads from the Mojave Desert, and this population is certainly a distinct population segment (DPS) deserving of additional protection. Importantly, if nelsoni retains recognition as a species, then the Mojave Desert population may also merit species status (i.e. description as a new species). We do not regard it at the present time as representative of B. nelsoni. Numerous other springs in the Coso Range provide potential habitats for toads. Additional sampling could reveal further variation and evidence for either gene flow or isolation. The disjunct mesic riparian and montane habitats of the northwestern Mojave Desert are rich in vertebrate, arthropod, and vascular plant endemics, some of which are very locally restricted and isolated from one another.
Specific Status of Bufo nelsoni. We recognize Bufo nelsoni as a species. Bufo nelsoni was diagnosed by allozymic data (Feder, 1977). Therefore, the first justification of species rank for Bufo nelsoni should be credited to Feder (1977), validating Savage’s (1960b) strictly nomenclatural elevation. Mitochondrial DNA data by Goebel (1996a, 2003) and Murphy and Morafka (above) are consistent with species status for B. nelsoni. Bufo nelsoni is allopatric to all other members of the B. boreas group (Nevada Division of Wildlife, 2000), and both Altig et al. (1998) and Powell et al. (1998) recognize nelsoni as a species based on allopatry. We have not identified any morphological characters that distinguish B. nelsoni; it may be a cryptic species. The Taxonomic Working Group for the Integrated Taxonomic Information System database (IT IS, 2002) makes judgments on species status; they independently concluded that nelsoni was a species, although criteria were not provided. Recently, Frost (2002) treated nelsoni as a species, also. Since 1960, most authors of original data on B. nelsoni and the B. boreas group concur.
Conservation. Amargosa toads are endemic to Oasis Valley in Nye County, Nevada. Their historical range may be limited to a 16-km stretch of the Amargosa River and nearby spring systems between Springdale and Beatty. They are isolated; there are no known or probable connections between them and other members of the Bufo boreas species group (Nevada Division of Wildlife, 2000). Early anecdotal population counts were highly variable. Linsdale (1940) saw “many small young toads” in 1931; Wright and Wright (1949) found 5 and 4 on consecutive days in 1942; Savage (1960) found 5, “a few,” “thousands,” and 40, during March, May, June, and November 1958. More recent opportunistic counts varied between 20 adults (Altig and Dodd, 1987) and larger numbers (e.g., 98 adults, Altig, 1981; 49 adults, Maciolek, 1983a; 15 breeding pairs, Hoff, 1994; 40 adults, Heinrich, 1996).
Population estimates based on mark-recapture data (Stein, 1996, 1999; Sjoberg, 2000, 2001; Stein et al., 2000) led to higher numbers. A population size of 536 adults was estimated in 1997 (Stein, 1999). More accurate measures based on animals tagged with passive internal transponders (PIT tags) were made in 1998–2001. Between 13 and 15 localities were surveyed three times each year and 2,895 adults were tagged by 2001. Data for 1999 were thoroughly analyzed and the population size was estimated at 4,697 ± 715 adults at surveyed localities (Stein, 1999; Stein et al., 2000). A potential population of 25,000 toads throughout Oasis Valley was estimated based on the number of toads at surveyed sites and potential habitat in the Valley as estimated from satellite imagery (Stein et al., 2000; Sjoberg, 2002; J. Sjoberg, personal communication). Preliminary analyses from surveys in 2000 (1,415 adults captured, 875 new captures) and 2001 (1,185 adults captured, 667 new captures) suggest similar population sizes and that the population may be stable in the short term (Sjoberg, 2000, 2001; J. Sjoberg, personal communication). Stein (2000) concluded that there was no evidence of a long-term population decline of Amargosa toads in the Oasis Valley, but fluctuating populations might account for variability in past population estimates. Perhaps the greatest concern is the limited distribution of a species that numbers 25,000 at best (and may be much smaller) and the potential susceptibility of its riparian habitat in a desert environment.
Federal designations for the Amargosa toad varied similarly. Bufo nelsoni was a candidate species (Category 2) for listing under the Endangered Species Act as early as 1977 (Federal Register, 1977). They were elevated to a Category 1 candidate (Federal Register, 1982), but reduced to Category 2 (Federal Register, 1985). In 1994, the U.S. Fish and Wildlife Service was petitioned to emergency list Bufo nelsoni as Endangered (Biodiversity Legal Foundation, 1994; petition date 19 September 1994). Bufo nelsoni was again elevated to a Category 1 species (Federal Register, 1994 [15 November]) and in a 90-d finding the U.S. Fish and Wildlife Service found that the petition action might be warranted (Federal Register, 1995c). However, after finding that toads were more abundant and widespread than stated in the petition (Heinrich, 1996) and habitat was being managed by the Bureau of Land Management, The Nature Conservancy, and private land owners (Stein, 1999), the U.S. Fish and Wildlife Service recommended removal of the Amargosa toad from Category 1 (U.S.F.W.S., 1995) and determined listing was not warranted (Federal Register, 1996a). Amargosa toads are currently classified as a Species of Concern (a new category similar to Category 2, Federal Register, 1996b), which does not provide any federal protection to the species or its habitat.
Amargosa toads were classified as a Protected amphibian by the State of Nevada in 1998, which does provide some protection. The Nevada Natural Heritage Program gave Amargosa toads a designation of highest global and state concern (G1S1, Clemmer, 1995). An Amargosa Toad Working Group was formed in 1994 and meets biannually to implement and provide oversight for conservation actions (Burroughs, 1999; Nevada Division of Wildlife, 2000). Threats to these toads include direct kill and habitat disturbance by wild burros, livestock, and off-road vehicles; predation and competition by nonnative aquatic species; and alteration of riparian plant communities by invasion of tamarisk (Tamarix sp.; Burroughs, 1999; Nevada Division of Wildlife, 2000). Habitats have been affected by lowered water tables due to increased groundwater use for municipal, agricultural, and industrial purposes. Habitats also have been changed or eliminated by human activities including the alteration of springs or direct diversion of water for agricultural use and urban development. The Amargosa river channel and its riparian corridor were altered for flood control and vehicular traffic. The river channel is assumed to have served as the primary route for toad movements between populations and disruption may have resulted in fragmentation of toad habitats.
A formal multiparty conservation agreement was completed (Nevada Division of Wildlife, 2000), and a long-term species management plan is being developed (J. Sjoberg, personal communication). Some conservation measures have been implemented. Protective fencing was provided for several localities (Nevada Division of Wildlife, 2000; Burroughs, 2001), including Indian Springs in 1993 and Crystal Springs in 1995. The Bureau of Land Management (BLM) removed 900 feral burros in 1995 and 1996 (Nevada Division of Wildlife, 2000; Bureau of Land Management, 2002). The BLM and cooperators also initiated a program to remove invasive and non-native tamarisk trees (Nevada Division of Wildlife, 2000; Burroughs, 2001; Bureau of Land Management, 2002). Measures were initiated to control nonnative crayfish (Procambarus sp.), bullfrogs (Rana catesbeiana), and black bullheads (Ameiurus melas, Nevada Division of Wildlife, 2000; Burroughs, 2001), which may prey on or compete with B. nelsoni (Hoff, 1994; Nevada Division of Wildlife, 2000). Local volunteer landowners are creating and maintaining Amargosa toad habitat and participating in long-term planning for conservation and habitat protection (Burroughs, 1999). Beginning in 1998, surveys were conducted at least three times annually to identify population size, habitat use, movement and distribution of individuals, and life history parameters (Nevada Division of Wildlife, 2000; Sjoberg, 2000, 2001; Stein et al., 2000; Burroughs, 2001). Much of the potential and historical range of Amargosa toads is now protected either formally (land acquisitions and agreements) or by informal agreements with landowners (J. Sjoberg, personal communication). The Nature Conservancy purchased over 263 ha of land in the Oasis Valley (Rogers, 1999; Nature Conservancy, 2002). Habitat has been restored or modified at several sites to control vegetation and manage water in riparian habitats (Burroughs, 2001). A nature trail and educational visitor center is planned near Beatty (Burroughs, 2001). Databases for B. nelsoni and all sensitive species in the Oasis Valley are being collected and managed by the Nevada National Heritage Program (G. Clemmer, personal communication). A Web site (Simandle, 2002) has been developed from which information on B. nelsoni can be obtained.
Information on the ecology and life history of Amargosa toads is fragmentary, but aspects of habitat and habitat preference, life history and population biology parameters, behavior, and causes of mortality including cannibalism and captive rearing have been described (Wright and Wright, 1949; Savage, 1960b; Savage and Schuierer, 1961; Altig, 1981; Maciolek, 1983a; Hoff, 1994, 1996; Clemmer, 1995; Heinrich, 1996; Stein et al. 2000) and are reviewed elsewhere (Nevada Division of Wildlife, 2000). Researchers at the University of Nevada, Reno, are currently investigating metapopulation structure and its implications for conservation and habitat restoration in Amargosa toads and quantifying characteristics of oviposition sites and habitats of adult toads (Burroughs, 2001; D. Jones and E. Simandle, personal communication). Recently, Jones et al. (2003) report predation on Amargosa toads by introduced American bullfrogs (Rana catesbeiana).
Acknowledgments. Thanks to Steve Corn, Darrel Frost, David Wake, Eric Simandle, Glenn Clemmer, and Jon Sjoberg who all provided comments that contributed to this paper. Thanks to Glenn Clemmer (Nevada Natural Heritage Program) for providing many unpublished reports and correct citations from the Federal Register. Thanks to Jon Sjoberg (Nevada Division of Wildlife), who provided unpublished reports from 2000 and 2001. Research on toad genetics of the population from Haiwee Springs was supported by a contract issued to California State University, Dominguez Hills by the Directorate of Public Works, National Training Center, Fort Irwin, California, to D.J.M., and by the Natural Sciences and Engineering Research Council of Canada grant A3148 to R.W.M.
Department of Environmental, Population, and Organismic Biology
Campus Box 334
University of Colorado
Boulder, Colorado 80309-0334
University of Colorado Museum
Campus Box 214
University of Colorado
Boulder, Colorado 80309-0334
2Hobart M. Smith
Department of Environmental, Population, and Organismic Biology
Campus Box 334
University of Colorado
Boulder, Colorado 80309-0334
3Robert W. Murphy
Centre for Biodiversity and Conservation Biology
Royal Ontario Museum
100 Queen's Park
Toronto, Ontario, Canada M5S 2C6
4David J. Morafka
Department of Biology
California State University, Dominguez Hills
1000 East Victoria Street
Carson, California 90747-0005
Literature references for Amphibian Declines: The Conservation Status of United States Species, edited by Michael Lannoo, are here.
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