Herpetologists often complain that, despite amphibians' being one of the most threatened vertebrate classes, there is a dearth of funding and capacity to tackle the global crisis afflicting them. We compared the average funding per species listed under the US Endangered Species Act (ESA) to quantify funding favoritism across vertebrate classes in the United States and compared ESA listings with NatureServe evaluations of endangerment in order to examine listing bias. We found that, on average, listed US amphibians receive one-quarter of the ESA funding that other vertebrate classes do. This inequality is compounded by listing bias, with 82% of the amphibians found to be at risk by NatureServe remaining unlisted under the ESA. We recommend that federal, state, and private conservation groups take reactive andproactive measures to build capacity to sustain this important class of vertebrates for future generations.
The widespread loss of amphibians is a defining characteristic of the sixth great extinction (Wake and Vredenburg 2008). More than 40% of the known amphibians are in serious decline, with at least 122 species having become extinct since 1980 (Stuart et al. 2004, Hoffmann et al. 2010). The dire status of the taxon is likely under-estimated relative to more well-known vertebrate classes, because for 24% of the world's 6260 amphibians there are insufficient data to determine their population status (Hoffmann et al. 2010).
Many amphibians living in the United States are as threatened as their more publicized tropical counterparts (Lannoo 2005, IUCN 2009). At least 36 of the 300 recognized species in the United States are listed as critically imperiled or presumed extinct (NatureServe 2011). Several amphibian species in the United States survive only because of intensive, ex situ breeding programs. The Wyoming Toad (Bufo baxteri Porter) was extirpated in the wild in 1994 and now persists only in captive populations (Odum and Corn 2005). Similar fates are shared by at least six other US amphibians now managed in ex situ programs (Muths et al. 2001, Fellers et al. 2007, Chelgren et al. 2008, Richter et al. 2009, Beauclerc et al. 2010, Gaston et al. 2010, Lannoo 2012). There is broad, international, scientific consensus on the breadth, depth, and potential causes of the amphibian crisis, as well as extensive press coverage (Stuart et al. 2004, Wake and Vredenburg 2008, Collins and Crump 2009, Hoffmann et al. 2010). However, our capacity to mitigate threats, including disease, habitat loss, invasive species, overharvesting, climate change, and pollution, remains woefully inadequate (Mendelson et al. 2006). This has prompted complaints from frustrated conservationists that amphibians are a neglected vertebrate class and that the existing mechanisms to support species preservation are weighted in favor of other taxa (Stuart et al. 2004, Lannoo 2012). Although it is difficult to objectively test a hypothesis of biased taxon funding, annual reports by the US Fish and Wildlife Service (USFWS) to Congress on federal and state expenditures to preserve threatened and endangered species make it possible to evaluate the amounts of conservation funding to US species allocated under the Endangered Species Act (ESA). We evaluated listing bias by comparing the discrepancies in endangerment assessments of US species between the ESA (a legally recognized definition) and NatureServe (which is not legally recognized but indicates the potential for a formal listing; see the supplemental material, available online at http://dx.doi.org/10.1525/bio.2012.62.2.13). NatureServe is an independent organization working closely with the International Union for Conservation of Nature (IUCN) to make expert assessments of endangerment.
We compiled reports related to ESA-related expenditures over the fiscal years 2004–2007 prepared by the USFWS for Congress (USFWS 2004, 2006, 2007). The spending totals (summed over all four years) included disbursements by all federal and state agencies, not only by the USFWS. Outlays in the reports to Congress included the broad categories of federal or state expenditures, and these were each subdivided into land acquisition or management actions. Following the principle that land acquisition is a specialized conservation action (Salafsky et al. 2008), we simply lumped all expenditures by year.
The USFWS reports expenditures by the lowest taxonomic unit, including subspecies and distinctive population segment level. To achieve standard taxonomic resolution for comparison among species, we aggregated the subspecies and distinctive-population segments to the species level. We recorded for each ESA-listed species the NatureServe rounded global conservation status (critically imperiled, imperiled, vulnerable, apparently secure, secure) (NatureServe 2011). Because of small sample sizes for the presumed extinct and possibly extinct status groups, these samples were merged and reported as a single category (presumed extinct). The independent group NatureServe has collaborated closely with the IUCN in its Global Amphibian Assessment, using a consistent, proven endangerment-assessment methodology (Master 1991). For each species, we recorded both the USFWS priority as either endangered or threatened. Unlike NatureServe, the ESA does not have a rounded global status for species-level comparisons, so where multiple subspecies or populations were encountered and aggregated, we recorded the conservation status for the species as the status of the least-threatened subspecies or population.
All of the data were analyzed in SPSS (IBM, Armonk, New York) and tested for normality using a Kolmogorov—Smirnov test and for homogeneity of variance using a Levene's test. The data were log10 transformed in order to normalize the data and to meet the analysis assumptions of normal distribution and homogeneity of variance. A one-way ANOVA (analysis of variance) was used to test the null hypotheses that there were no differences in funding allocations related to vertebrate class, USFWS priority, or NatureServe priority.
Magnitude of disparities
The average ESA-listed amphibian received only 25% of the funding from 2004 through 2007 allocated to the average mammal, bird, or reptile, and around 10% of that allocated to the average listed fish (figure 1). This apparent funding bias was not statistically significant (F(4, 310) = 1.209, p = .31), but we argue that a real funding bias exists when the figures are adjusted for listing bias (figure 1). Amphibians were the most underlisted taxon; NatureServe listed 122 amphibians as at risk, but only 21 species are listed as threatened or endangered under the ESA—a disparity of 82% (figure 1). A comparison with other vertebrate classes also indicated a major disparity for fish (with 70% of apparently threatened and endangered fish unlisted). The NatureServe—ESA discrepancies were modest for birds, reptiles, and mammals, at 25%, 40%, and 22%, respectively (figure 1).
Furthermore, funding allocations did not match the ESA assessments of extinction risk; the average threatened species (across all taxa) identified by the ESA received $5.9 million annually compared with only $1.3 million per year for their endangered counterparts (F(1, 313) = 4.923, p = .03). This was confirmed by the NatureServe threat assessments: ESA-listed species classified in NatureServe's seriously imperiled category received an average of 77% less funding than those characterized in the less-threatened vulnerable category (figure 2; F(6, 308) = 15.140, p < .001).
The ESA should protect amphibians too
Despite being valuable research models (Burggren and Warburton 2007) and potential sources of medicines (Chivian and Bernstein 2008) and food (Gratwicke et al. 2010), as well as providing ecosystem services (Davic and Welsh 2004), amphibians are the most underlisted and underfunded vertebrate group in the United States, as was shown by the results above. The ESA specifically indicates that commercial or other nonbiodiversity value systems should not be considered in the designation process (Rohlf 1991, Brown and Shogren 1998). However, social, economic, and political trade-offs often influence funding and may explain the bias favoring nonamphibian vertebrate taxa (Restani and Marzluff 2002). Important swaying factors known to influence resource allocation are species charisma (Rohlf 1991, Czech et al. 1998) and the economic incentives from commercial or game species (Dawson and Shogren 2001).
The rate at which new species are becoming threatened throughout the world has outstripped our ability to respond (Hoffmann et al. 2010). ESA funding cannot be apportioned to protect unlisted species, so clearing the widely recognized listing backlog is a high priority (USGAO 2002). Even so, our analyses and those of others (e.g., Restani and Marzluff 2001) have shown that a formal recognition of endangered status is a poor predictor of financial support. Currently, only 20% of the federal and state funding required to meet ESA directives is available, and the average amount of support per species has declined since the late 1970s (Scott et al. 2006). Almost three-quarters of USFWS field offices receive insufficient funds to complete ESA-related work (USGAO 2002). The critical lack of financial support to do the job is further confounded by the actual funding priorities' failing to reflect global conservation priorities. For example, 50% of ESA-related expenditures are apportioned to more than 50 species considered by NatureServe to be globally safe. Salmonids are a case in point, having benefited from funding through their controversial status as evolutionary significant units or distinctive-population segments (Pennock and Dimmick 1997, Cronin 2006). This has resulted in the Chinook salmon's (listed as secure by NatureServe) receipt of $714 million in ESA funding from 2004 through 2007, while commercial fisheries simultaneously harvested 84,000 pounds of this species (worth $194 million; NOAA 2010). Oddly, none of the whitefishes (subfamily Coregoninae), recognized by NatureServe as some of the most-endangered US salmonids, are listed by the ESA. Therefore, they are ineligible for ESA-related benefits. Amphibians are affected similarly. The tiger salamander is listed by NatureServe as globally secure; however, the ESA-listed Sonoran subspecies Ambystoma tigrinum stebbinsi received $331,000 from 2004 to 2007. By contrast, at least 100 other distinctly recognized amphibian species have received no funding, despite their being identified by experts as high priorities. The ESA could begin to address these issues by creating the equivalent of a global status category that considers the status of the species as a whole and that can be followed by subspecific identifications and comparisons in order to maintain perspective. We recognize that subspecific designations can be a prelude to complete species recognition. Nonetheless, our evaluation here has exposed the fact that globally secure species are consuming 50% of ESA funding.
It is conceivable, but unlikely, that amphibians may simply be less costly to conserve than are other vertebrates, which would explain the funding bias. This is plausible, given that many amphibians have small ranges (Ricketts et al. 2005). However, as a class of vertebrates, amphibians vary tremendously in life-history strategies and distribution, and they face a diverse range of complex threats, which makes generalization impossible. USFWS species recovery plans must now estimate recovery costs, but to date, this process has been too inconsistent to allow for meaningful comparisons (Tear et al. 1995). There are also few quantitative data on the relationship between the absolute amount of funding distributed and the effectiveness of threat mitigation. Therefore, it is reasonable to presume that fairly distributed amounts of funding are essential to building collective conservation capacity. Although it is now the highest priority for herpetologists (Lannoo 2012), there has been little financial support for enhancing amphibian conservation competency.
Reactive and proactive solutions
Amphibians in the United States require immediate attention and their fair share of the limited amount of conservation dollars. We recognize two complementary approaches: identifying and assisting those species already in or approaching decline and preventing reductions in species numbers and populations before they become eligible for listing (under the ESA) or recognition (under NatureServe). A first step is recognizing that amphibians must benefit from the ESA mandate and related funding, especially given the rapidly increasing threats to species in the United States (Wake and Vredenburg 2008, Collins and Crump 2009, Hoffmann et al. 2010). On a broad scale, lawmakers must create legislative funding mechanisms that can grow at a rate commensurate with increasing threats in order to ensure that the ESA is implemented as was originally intended. This will take time, but emergency measures should be considered immediately in order to respond at a national level to the devastating consequences of mass mortalities caused by an ongoing Batrachochytrium dendrobatidis epidemic. This fungal pathogen has already caused the extinction of at least three US species (Burrowes et al. 2004) and has pushed several others to the brink of extinction (Odum and Corn 2005, Pilliod et al. 2010, Vredenburg et al. 2010). The effects of this disease have been even more dramatic on naive populations of amphibians elsewhere, where up to 50% of the species and 80% of the individuals at mountainous tropical sites have disappeared (Lips et al. 2006, 2008). Although it does not appear to be causing extinctions at this scale in the United States (Longcore et al. 2007, Rothermel et al. 2008), the influence of this fungus on many species remains unclear, and a proactive response plan designed to avert extinctions is needed. Other emerging diseases, including the amphibian ranaviruses (Gray et al. 2009), must be monitored for population-level effects, and we must be prepared to implement management prescriptions for these disease threats. Federal agencies have demonstrated an ability to respond to other emergency situations—for example, the insidious white nose syndrome, a disease that has caused the deaths of more than a million insect-devouring bats in Connecticut, Massachusetts, Vermont, New Jersey, Pennsylvania, Virginia, West Virginia, North Carolina, and Indiana (Blehert et al. 2009, USFWS 2011). The government responded by creating and providing the resources to implement a national management plan by the USFWS (2011). A similar coordinated effort should be initiated for critically endangered amphibians through a multiagency task force, including the hiring of at least one full-time staff member dedicated to conservation actions that mitigate amphibian extinction. There already exists a nascent community of external partners for such a task force, including a nongovernmental-organization community (i.e., the IUCN Amphibian Survival Alliance and Amphibian Ark, Partners in Amphibian and Reptile Conservation, Save The Frogs) with the needed expertise and ready-to-implement conservation plans (Mendelson et al. 2006).
The ESA is a valuable tool for conservation but should be deployed more effectively in order to provide the necessary resources to save US amphibians. Besides the exploration of how existing legal and legislative mechanisms can build capacity in order to address the amphibian crisis, help will be needed from many stakeholders, especially nonfederal funders. Private foundations in particular have the flexibility and resources to implement capacity-building actions for amphibians. Within this crisis lies a significant opportunity to make measurable, global biodiversity impacts in a completely uncrowded field. Foundations also can take advantage of the incredible amount of scientific information from both NatureServe and the IUCN that has already led to the identification of species targets, many of which are not being supported by the ESA. Such partnerships could serve the dual function of steering some amphibian species away from the precipice while mobilizing resources and actions to prevent more ESA listings.
The traditional reactive model of initiating action only after the endangerment of a species will ultimately—and almost assuredly—be more costly in dollars and overall biodiversity than a proactive approach. Under the current model, the conservation community emphasizes the need for certainty in population numbers. However, in reality, the status of a species is generally in doubt until it can no longer be found, at which point it is too late to act (Wolfe 2005). For example, it took more than 30 years of a grassroots campaign to list the dusky gopher frog (Lithobates sevosus) under the ESA. This excruciatingly slow process no doubt helped contribute to its now dire status: It now includes only one remnant, naturally occurring population (Lannoo 2012). To help avoid this circumstance, we need to rely more on adaptive resource management, a proactive tool for coping with uncertainty that requires a commitment to both monitoring and management actions under clearly defined objectives (Williams 2002).
The Amphibian Research and Monitoring Initiative (ARMI) of the US Geological Survey has been working toward this goal since it was established in 2000. ARMI researchers monitor national parks, wildlife refuges, and other protected lands to assess species and population status and then use these objectively collected data to develop and advance conservation recommendations (Muths and Dreitz 2008). Likewise, there also is a national grassroots community of academic, state, and federal biologists operating under the Partners in Amphibian and Reptile Conservation banner that facilitates communication among public and private stakeholders to advance the conservation of these taxa.
These are examples of organizations and wildlife professionals that need adequate resources to understand little-studied amphibians, to objectively and continuously assess status and threats, and then to implement mitigation and management actions to prevent declines and extinctions (Lyons 2008). Our present analysis clearly indicates that amphibians are both underlisted and underfunded through the ESA. However, this federal act in coordination with fair amounts of funding could still prevent the extinction of significant numbers of amphibians. We are especially encouraged because of the existence of networks of professional specialists who have already identified the highest priorities and solutions for beginning to stabilize amphibian species and populations (Gascon et al. 2007). What are needed now are financial resources from a fair apportionment of the federal ESA obligation that, in turn, are leveraged with complementary support from the private sector.
The authors are grateful to Christopher Estes, Claude Gascon, Mike Lannoo, Karen Lips, Jim Nichols, Joe Mendelson, George Rabb, John Sauer, and anonymous reviewers for insightful comments and recommendations. Amphibian research at the Smithsonian Conservation Biology Institute is supported by Frank and Susan Mars.