Application of Genetic Bottleneck Testing to the Investigation of Amphibian Declines: a Case Study with Natterjack Toads

Abstract: Declines of amphibians are causing widespread concern and in some cases have been explained by factors such as climate change and the spread of microbial pathogens. A problem remains, however, in the unequivocal demonstration of decline in situations where populations may be undergoing natural fluctuations in abundance. We describe the application of a genetic test for bottlenecks ( Cornuet & Luikart 1996 ) that should distinguish between natural oscillations and true population declines. British natterjack toads (   Bufo calamita  ) provide examples of populations that have not declined in recent decades, populations that have declined, and populations in which trends are unclear. Microsatellite allele frequency data from these populations were tested for heterozygote excess and shifts in allele frequency distributions, and inferences from these computations about bottlenecks (i.e., persistently smaller population sizes than the recent means) were compared with demographic information. The genetic test correctly identified bottlenecks and should therefore prove useful in demonstrating whether amphibian declines have occurred where long-term demographic time series are not available.     

Inconclusiveness of Chytridiomycosis as the Agent in Widespread Frog Declines

Abstract:  Although there is considerable evidence to support the hypothesis that the chytrid fungus Batrachochytrium dendrobatidis is the primary agent responsible for widespread declines in amphibian populations, particularly rainforest frog populations in Australia and Central America, I argue the case has not yet been made conclusively. Few specimens were collected at the time of population declines, so it may never be possible to conclusively determine their cause. It remains unclear whether the pathogen is novel where declines have occurred. Although it is not necessary that the infection be novel for it to be implicated in declines, if a preexisting pathogen has only recently caused extinctions, cofactors must be important. Whether the pattern of outbreaks represents a "wave" of extinctions is unclear, but if it does, the rate of spread in Australia is implausibly high for a waterborne pathogen, given the most likely estimates of epidemiological parameters. Although B. dendrobatidis is an amphibian pathogen according to Koch's postulates, the postulates are neither necessary nor sufficient criteria to identify a pathogen. The following key pieces of information are necessary to better understand the impact of this fungus on frog communities: better knowledge of the means and rate of transmission under field conditions, prevalence of infection among frog populations, as distinct from morbid individuals, and the effect of the fungus on frogs in the wild. It is crucial to determine whether there are strains of the fungus with differing pathogenicity to particular frog species and whether host-pathogen coevolution has occurred or is occurring. Recently developed diagnostic tools bring into reach the possibility of addressing these questions and thus developing appropriate strategies to manage frog communities that may be affected by this fungus.     

Thermal Physiology,Disease, and Amphibian Declines on the Eastern Slopes of the Andes

Rising temperatures, a widespread consequence of climate change, have been implicated in enigmatic amphibian declines from habitats with little apparent human impact. The pathogenic fungus Batrachochytrium dendrobatidis (Bd), now widespread in Neotropical mountains, may act in synergy with climate change causing collapse in thermally stressed hosts. We measured the thermal tolerance of frogs along a wide elevational gradient in the Tropical Andes, where frog populations have collapsed. We used the difference between critical thermal maximum and the temperature a frog experiences in nature as a measure of tolerance to high temperatures. Temperature tolerance increased as elevation increased, suggesting that frogs at higher elevations may be less sensitive to rising temperatures. We tested the alternative pathogen optimal growth hypothesis that prevalence of the pathogen should decrease as temperatures fall outside the optimal range of pathogen growth. Our infection‐prevalence data supported the pathogen optimal growth hypothesis because we found that prevalence of Bd increased when host temperatures matched its optimal growth range. These findings suggest that rising temperatures may not be the driver of amphibian declines in the eastern slopes of the Andes. Zoonotic outbreaks of Bd are the most parsimonious hypothesis to explain the collapse of montane amphibian faunas; but our results also reveal that lowland tropical amphibians, despite being shielded from Bd by higher temperatures, are vulnerable to climate‐warming stress. Fisiología Termal, Enfermedades y Disminuciones de Anfibios en las Laderas Orientales de los Andes     

Amphibian Declines: Judging Stability, Persistence, and Susceptibility of Populations to Local and Global Extinctions

Extinctions are normal biological phenomena. Both mass extinctions in geological time and local extinctions in ecological time are well documented, but rates of extinction have increased in recent years—especially in vertebrates, including amphibians—as illustrated by recent reports of their population declines and range reductions. We suggest that long-term population data are necessary for rigorously evaluating the significance of the amphibian declines. Due to the physiological constraints, relatively low mobility, and site fidelity of amphibians, we suggest that many amphibian populations may be unable to recolonize areas after local extinction.     

Species Review of Amphibian Extinction Risks in Madagascar: Conclusions from the Global Amphibian Assessment

Abstract:  We assessed the extinction risks of Malagasy amphibians by evaluating their distribution, occurrence in protected areas, population trends, habitat quality, and prevalence in commercial trade. We estimated and mapped the distribution of each of the 220 described Malagasy species and applied, for the first time, the IUCN Red List categories and criteria to all species described at the time of the assessment. Nine species were categorized as critically endangered, 21 as endangered, and 25 as vulnerable. The most threatened species occur on the High Plateau and/or have been subjected to overcollection for the pet trade, but restricted extent of occurrence and ongoing habitat destruction were identified as the most important factors influencing extinction threats. The two areas with the majority of threatened species were the northern Tsaratanana-Marojejy-Masoala highlands and the southeastern Anosy Mountains. The current system of protected areas includes 82% of the threatened amphibian species. Of the critically endangered species, 6 did not occur in any protected area. For conservation of these species we recommend the creation of a reserve for the species of the Mantella aurantiaca group, the inclusion of two Scaphiophryne species in the Convention on the International Trade in Endangered Species Appendix II, and the suspension of commercial collecting for Mantella cowani . Field surveys during the last 15 years reveal no pervasive extinction of Malagasy amphibians resulting from disease or other agents, as has been reported in some other areas of the world.     

Effects of Landscape Composition and Wetland Fragmentation on Frog and Toad Abundance and Species Richness in Iowa and Wisconsin, U.S.A.

Abstract: Management of amphibian populations to reverse recent declines will require defining high-quality habitat for individual species or groups of species, followed by efforts to retain or restore these habitats on the landscape. We examined landscape-level habitat relationships for frogs and toads by measuring associations between relative abundance and species richness based on survey data derived from anuran calls and features of land-cover maps for Iowa and Wisconsin. The most consistent result across all anuran guilds was a negative association with the presence of urban land. Upland and wetland forests and emergent wetlands tended to be positively associated with anurans. Landscape metrics that represent edges and patch diversity also had generally positive associations, indicating that anurans benefit from a complex of habitats that include wetlands. In Iowa the most significant associations with relative abundance were the length of the edge between wetland and forest ( positive) and the presence of urban land (negative). In Wisconsin the two most significant associations with relative abundance were forest area and agricultural area ( both positive). Anurans had positive associations with agriculture in Wisconsin but not in Iowa. Remnant forest patches in agricultural landscapes may be providing refuges for some anuran species. Differences in anuran associations with deep water and permanent wetlands between the two states suggest opportunities for management action. Large-scale maps can contribute to predictive models of amphibian habitat use, but water quality and vegetation information collected from individual wetlands will likely be needed to strengthen those predictions. Landscape habitat analyses provide a framework for future experimental and intensive research on specific factors affecting the health of anurans.     

Integrating the Metapopulation and Habitat Paradigms for Understanding Broad-Scale Declines of Species

Abstract:  Caughley (1994) argued that researchers working on threatened populations tended to follow the "small population paradigm" or the "declining population paradigm," and that greater integration of these paradigms was needed. Here I suggest that two related paradigms exist at the broader spatial scale, namely the metapopulation paradigm and habitat paradigm, and that these two paradigms also need to be integrated if we are to provide sound management advice. This integration is not trivial, and I outline five problems that need to be addressed: (1) habitat variables may not measure habitat quality, so site-specific data on vital rates are needed to resolve the effects of habitat quality and metapopulation dynamics; (2) measurements of vital rates may be confounded by movements; (3) vital rates may be density dependent; (4) vital rates may be affected by genotype; and (5) vital rates cannot be measured in unoccupied patches. I reviewed papers published in Conservation Biology from 1994 to 2003 and found 41 studies that analyzed data from 10 or more sites to understand the factors limiting species' distributions. Five of the analyses presented were purely within the metapopulation paradigm, 14 were purely within the habitat paradigm, 17 involved elements of both paradigms, and 7 were theoretically ambiguous (2 papers presented 2 distinct analyses and were counted twice). This suggests that many researchers appreciate the need to integrate the paradigms. Only one study, however, used data on vital rates to resolve the effects of habitat quality and metapopulation dynamics (problem 1), and this study did not address problems 2–5. I conclude that more intensive research incorporating site-specific data on vital rates and movement is needed to complement the numerous analyses of distributional data being produced.     

Spatial Scale and Determination of Species Status of the Green Frog

Although the importance of spatial scale in determining species status (abundance and distribution) is widely recognized, most ecological investigations have been conducted at local scales. Our goal was to investigate the importance of spatial scale in assessing the status of the green frog ( Rana clamitans melanota) in the center of its range in eastern North America. Using repeated surveys at 160 ponds from 1992 to 1994, we investigated patterns of occupancy, abundance, and turnover at local, sub-regional, regional, and geographic scales to determine the status of the green frog in southwestern Ontario, Canada. Patterns of pond occupancy were stable at the geographic scale. Occupancy was stable in two regions and decreased in one. At the sub-regional scale, occupancy was stable in six sub-regions, increased in one, and decreased in two. Patterns of adult abundance were stable at the geographic scale. At the regional scale trends in adult abundance were increasing, decreasing, or stable in each of three regions. At the sub-regional scale abundance was stable in three, increasing in one, decreasing in two, and no trend occurred in three sub-regions. At the local scale abundance was stable at 20% of ponds, increased at 17.8%, decreased at 14.4%, and no trend existed at 47.8%. Colonization and extinction rates ranged from 0 to 0.20 and 0 to 0.35 ponds/pond occupied/year, respectively, and differed among regions. Local extinctions took place at 25% of ponds during the study, but no sub-regional or regional scale extinctions occurred. Small populations (<10 adults/pond) were prone to local extinction. Determination of the status of the green frog is scale dependent. Although green frog populations are dynamic, it is common and stable at the geographic scale, but its status varies among regions or sub-regions. Although processes that negatively affect a species may operate at the local scale, a large-scale perspective is necessary to determine status.