Amphibian decline and extinction: what we know and what we need to learn

For over 350 million yr, thousands of amphibian species have lived on Earth. Since the 1980s, amphibians have been disappearing at an alarming rate, in many cases quite suddenly. What is causing these declines and extinctions? In the modern era (post 1500) there are 6 leading causes of biodiversity loss in general, and all of these acting alone or together are responsible for modern amphibian declines: commercial use; introduced/exotic species that compete with, prey on, and parasitize native frogs and salamanders; land use change; contaminants; climate change; and infectious disease. The first 3 causes are historical in the sense that they have been operating for hundreds of years, although the rate of change due to each accelerated greatly after about the mid-20th century. Contaminants, climate change, and emerging infectious diseases are modern causes suspected of being responsible for the so-called 'enigmatic decline' of amphibians in protected areas. Introduced/exotic pathogens, land use change, and infectious disease are the 3 causes with a clear role in amphibian decline as well as extinction; thus far, the other 3 causes are only implicated in decline and not extinction. The present work is a review of the 6 causes with a focus on pathogens and suggested areas where new research is needed. Batrachochytrium dendrobatidis (Bd) is a chytrid fungus that is an emerging infectious disease causing amphibian population decline and species extinction. Historically, pathogens have not been seen as a major cause of extinction, but Bd is an exception, which is why it is such an interesting, important pathogen to understand. The late 20th and early 21st century global biodiversity loss is characterized as a sixth extinction event. Amphibians are a striking example of these losses as they disappear at a rate that greatly exceeds historical levels. Consequently, modern amphibian decline and extinction is a lens through which we can view the larger story of biodiversity loss and its consequences.     

Evaluating multiple causes of amphibian declines of Ecuador using geographical quantitative analyses

Amphibians are declining at alarming rates worldwide; however, the causes of these declines remain somewhat elusive. Here we evaluated three major threats implicated in declines of populations and disappearance of Ecuadorian amphibians: chytridiomicosis, climate change, and habitat loss. We assessed spatial patterns of these key threats to Ecuadorian amphibians using a multi‐species database of endemic frogs along with information on the pathogen's distribution and environmental requirements, species sensitivity to climate change (indirectly based on species geographical distribution and ecological properties) and habitat loss. Our results show that amphibians display a non‐random pattern of extinction risk, both geographically and taxonomically. Further, climate change, chytridiomicosis, and their synergetic effects, are likely currently exerting the greatest impact on amphibians in Ecuador, while habitat loss does not seem to be causing precipitous declines. The most threatened species under the IUCN extinction risk categories are exactly those that appear to be the most affected by these threats. By examining multiple potential causes of amphibian threat level in a spatially explicit framework our study provides new insights about what combination of factors are most important in amphibian declines in a tropical diversity hotspot. Further, our approach and conclusions are useful for studying declines in other regions of the world.     

Climate change and amphibian declines: is there a link?

Abstract. Global climates have been changing, sometimes rapidly and dramatically, throughout the evolutionary history of amphibians. Therefore, existing amphibian species have been derived from those that have survived major climatic disturbances. Although recent global climate change has resulted in warming in many regions, temperatures in some areas to date have not changed measurably, or have even cooled. Declines of some amphibian populations have been correlated with climate events, but demonstrations of direct causal relationships need further research. Data are available indicating some indirect effect of climate change on the initiation of breeding activities of some amphibians that occur earlier than in previous springs, but the costs and benefits of these changes are just beginning to be investigated. Climate may also play an indirect role in facilitating epidemics of infectious disease. Regardless of the role that climate changes may have played in past and current amphibian declines, future shifts in climate, should they prove as dramatic as predicted, will certainly pose challenges for surviving amphibian populations and for successful recovery efforts of species that have suffered declines.     

Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation

The pathogenic chytrid fungus Batrachochytrium dendrobatidis (Bd) can cause precipitous population declines in its amphibian hosts. Responses of individuals to infection vary greatly with the capacity of their immune system to respond to the pathogen. We used a combination of comparative and experimental approaches to identify major histocompatibility complex class II (MHC-II) alleles encoding molecules that foster the survival of Bd-infected amphibians. We found that Bd-resistant amphibians across four continents share common amino acids in three binding pockets of the MHC-II antigen-binding groove. Moreover, strong signals of selection acting on these specific sites were evident among all species co-existing with the pathogen. In the laboratory, we experimentally inoculated Australian tree frogs with Bd to test how each binding pocket conformation influences disease resistance. Only the conformation of MHC-II pocket 9 of surviving subjects matched those of Bd-resistant species. This MHC-II conformation thus may determine amphibian resistance to Bd, although other MHC-II binding pockets also may contribute to resistance. Rescuing amphibian biodiversity will depend on our understanding of amphibian immune defence mechanisms against Bd. The identification of adaptive genetic markers for Bd resistance represents an important step forward towards that goal.     

Amphibian defenses against ultraviolet-B radiation

As part of an overall decline in biodiversity, amphibian populations throughout the world are disappearing. There are a number of potential causes for these declines, including those related to environmental changes such as increasing ultraviolet-B (UV-B) radiation due to stratospheric ozone depletion. UV-B radiation can kill amphibian embryos or can cause sublethal effects that can harm amphibians in later life stages. However, amphibians have defenses against UV-B damage that can limit damage or repair it after exposure to UV-B radiation. These include behavioral, physiological, and molecular defenses. These defenses differ interspecifically, with some species more able to cope with exposure to UV-B than others. Unfortunately, the defense mechanisms of many species may not be effective against increasing persistent levels of UV-B radiation that have only been present for the past several decades due to human-induced environmental damage. Moreover, we predict that persistent UV-B-induced mortality and sublethal damage in species without adequate defenses could lead to changes in community structure. In this article we review the effects of UV-B radiation on amphibians and the defenses they use to avoid solar radiation and make some predictions regarding community structure in light of interspecific differences in UV-B tolerance.     

An examination of amphibian sensitivity to environmental contaminants: are amphibians poor canaries?

Nearly two decades ago, the global biodiversity crisis was catapulted to the front pages of newspapers with the recognition of worldwide amphibian declines. Amphibians earned their appellation, 'canaries in a coal mine', because of apparent high sensitivity to human-mediated environmental change. The most frequently cited causes for high susceptibility include permeable skin, a dual aquatic-terrestrial life cycle and a relatively rudimentary immune system. While some researchers have questioned the basis for the canary assertion, there has been no systematic evaluation of amphibian sensitivity to environmental challenges relative to other taxa. Here, we apply a database representing thousands of toxicity tests to compare the responses of amphibians relative to that of other taxonomic groups. The use of standardized methods combined with large numbers of identical challenges enables a particularly powerful test of relative effect size. Overall, we found that amphibians only exhibit moderate relative responses to water-borne toxins. Our findings imply that, as far as chemical contaminants are concerned, amphibians are not particularly sensitive and might more aptly be described as 'miners in a coal mine'. To the extent that amphibian declines have been mediated by chemical contaminants, our findings suggest that population losses and extinctions may have already occurred in a variety of taxa much more sensitive than amphibians.
Ecology Letters (2010) 13: 60–67     

A general assessment of the conservation status and decline trends of Mexican amphibians

We present a review on the conservation status and population trends of the 372 amphibian species currently recognized for Mexico. We based our analyses on the information gathered by the International Union for the Conservation of Nature-the Global Amphibian Assessment (IUCN-GAA) as well as on available literature about imminent or potential threats to these organisms in Mexico. This country has the fifth largest amphibian fauna in the world and almost 58% of the species that inhabit this country are considered as threatened. We highlight the proportion of species per order, family, and genus that are currently under severe risk in Mexico. In addition, we prepared a detailed list of the main factors that are threatening amphibians in this country. Evidence is provided that the six main mechanisms that are globally leading amphibians to extinction (alien species, over-exploitation, land use change, global changes, pollution, and infectious diseases) are indeed currently operating in Mexico. We discuss the relative importance of each of these causes. We also highlight the paucity of quantitative studies that support the current conservation status of Mexican amphibian species.     

Are snake populations in widespread decline?

Long-term studies have revealed population declines in fishes, amphibians, reptiles, birds and mammals. In birds, and particularly amphibians, these declines are a global phenomenon whose causes are often unclear. Among reptiles, snakes are top predators and therefore a decline in their numbers may have serious consequences for the functioning of many ecosystems. Our results show that, of 17 snake populations (eight species) from the UK, France, Italy, Nigeria and Australia, 11 have declined sharply over the same relatively short period of time with five remaining stable and one showing signs of a marginal increase. Although the causes of these declines are currently unknown, we suspect that they are multi-faceted (such as habitat quality deterioration, prey availability), and with a common cause, e.g. global climate change, at their root.     

Amphibians as models for studying environmental change

The use of amphibians as models in ecological research has a rich history. From an early foundation in studies of amphibian natural history sprang generations of scientists who used amphibians as models to address fundamental questions in population and community ecology. More recently, in the wake of an environment that human disturbances rapidly altered, ecologists have adopted amphibians as models for studying applied ecological issues such as habitat loss, pollution, disease, and global climate change. Some of the characteristics of amphibians that make them useful models for studying these environmental problems are highlighted, including their trophic importance, environmental sensitivity, research tractability, and impending extinction. The article provides specific examples from the recent literature to illustrate how studies on amphibians have been instrumental in guiding scientific thought on a broad scale. Included are examples of how amphibian research has transformed scientific disciplines, generated new theories about global health, called into question widely accepted scientific paradigms, and raised awareness in the general public that our daily actions may have widespread repercussions. In addition, studies on amphibian declines have provided insight into the complexity in which multiple independent factors may interact with one another to produce catastrophic and sometimes unpredictable effects. Because of the complexity of these problems, amphibian ecologists have been among the strongest advocates for interdisciplinary research. Future studies of amphibians will be important not only for their conservation but also for the conservation of other species, critical habitats, and entire ecosystems.     

Multiple zoosporic parasites pose a significant threat to amphibian populations

There is substantial evidence for the dominant role of Batrachochytrium dendrobatidis in amphibian population dynamics. However, a wide range of other pathogens could also be important in precipitating amphibian population declines, particularly in the face of climate change or other stressors. Here we discuss some examples of zoosporic parasites in the Chytridiomycota, Mesomycetozoa, Perkinsozoa and Oomycota, all of which infect amphibians in freshwater habitats. The pathosystem model provides an excellent basis for understanding host–parasite interactions. Chemotactic zoopores and several families of proteases facilitate infection. Introduction of non-native host may accelerate the dispersal of these parasites. Unlike B. dendrobatidis some of the other zoosporic parasites grow well at or slightly above 25 °C, and their growth rates are likely to increase with global warming. The interactions of parasites with each other and the combined effect of simultaneous infection with multiple species in amphibian populations remain to be carefully studied.     

Global stressors and the global decline of amphibians: tipping the stress immunocompetency axis

There is a widespread consensus that the earth is experiencing a mass extinction event and at the forefront are amphibians, the most threatened of all vertebrate taxa. A recent assessment found that nearly one-third (32%, 1,856 species) of the world’s amphibian species are threatened. Amphibians have existed on the earth for over 300 million years, yet in just the last two decades there have been an alarming number of extinctions, nearly 168 species are believed to have gone extinct and at least 2,469 (43%) more have populations that are declining. Infectious diseases have been recognized as one major cause of worldwide amphibian population declines. This could be the result of the appearance of novel pathogens, or it could be that exposure to environmental stressors is increasing the susceptibility of amphibians to opportunistic pathogens. Here I review the potential effects of stressors on disease susceptibility in amphibians and relate this to disease emergence in human and other wildlife populations. I will present a series of case studies that illustrate the role of stress in disease outbreaks that have resulted in amphibian declines. First, I will examine how elevated sea-surface temperatures in the tropical Pacific since the mid-1970s have affected climate over much of the world and could be setting the stage for pathogen-mediated amphibian declines in many regions. Finally, I will discuss how the apparently rapid increase in the prevalence of amphibian limb deformities is linked to the synergistic effects of trematode infection and exposure to chemical contaminants.     

Complexity in conservation: lessons from the global decline of amphibian populations

As part of an overall "biodiversity crisis" many amphibian populations are in decline throughout the world. Numerous causes have been invoked to explain these declines. These include habitat destruction, climate change, increasing levels of ultraviolet radiation, environmental contamination, disease, and the introduction of non-native species. In this paper, we argue that amphibian population declines are caused by different abiotic and biotic factors acting together in a context-dependent fashion. Moreover, different species and different populations of the same species may react in different ways to the same environmental insult. Thus, the causes of amphibian population declines will vary spatially and temporally. Although some generalizations (e.g. those concerning environmental stress and disease outbreaks) can be made about amphibian population declines, we suggest that these generalizations take into account the context-dependent dynamics of ecological systems.     

Linking global warming to amphibian declines through its effects on female body condition and survivorship

There is general consensus that climate change has contributed to the observed decline, and extinction, of many amphibian species throughout the world. However, the mechanisms of its effects remain unclear. A laboratory study in 1980–1981 in which temperate zone amphibians that were prevented from hibernating had decreased growth rates, matured at a smaller size and had increased mortality compared with those that hibernated suggested one possible mechanism. I used data from a field study of common toads (Bufo bufo) in the UK, between 1983 and 2005, to determine whether this also occurs in the field. The results demonstrated two pathways by which global warming may cause amphibian declines. First, there was a clear relationship between a decline in the body condition of female common toads and the occurrence of warmer than average years since 1983. This was paralleled by a decline in their annual survival rates with the relationship between these two declines being highly correlated. Second, there was a significant relationship between the occurrence of mild winters and a reduction in female body size, resulting in fewer eggs being laid annually. Climate warming can, therefore, act on wild temperate zone amphibians by deleteriously affecting their physiology, during and after hibernation, causing increased female mortality rates and decreased fecundity in survivors.     

Differentiating Migration and Dispersal Processes for Pond-Breeding Amphibians

Abstract Understanding the movement of animals is critical to many aspects of conservation such as spread of emerging disease, proliferation of invasive species, changes in land-use patterns, and responses to global climate change. Movement processes are especially important for amphibian management and conservation as species declines and extinctions worldwide become ever more apparent. To better integrate behavioral and ecological data on amphibian movements with our use of spatially explicit demographic models and guide effective conservation solutions, I present 1) a synopsis of the literature regarding behavior, ecology, and evolution of movement in pond-breeding amphibians possessing biphasic life cycles to distinguish between migration and dispersal processes, 2) a working hypothesis of juvenile-based dispersal, and 3) a discussion of conservation issues that follow from distinguishing the spatial and temporal movements of amphibians at different scales. I define amphibian migration as intrapopulational, round-trip movements toward and away from aquatic breeding sites. Population-level management, in general, can be focused on spatial scales of <1.0 km with attention focused on adult population and juveniles that remain near the natal wetland. I define amphibian dispersal as interpopulational, unidirectional movements from natal sites to other breeding sites. Metapopulation- or landscape-level management can be focused on movements among populations at spatial scales >1.0–10.0 km and on importance of terrestrial connectivity. The ultimate goal of conservation for amphibians should be long-term regional persistence by addressing management issues at both local and metapopulation scales.     

An identification of invariants in life history traits of amphibians and reptiles

While many morphological, physiological, and ecological characteristics of organisms scale with body size, some do not change under size transformation. They are called invariant. A recent study recommended five criteria for identifying invariant traits. These are based on that a trait exhibits a unimodal central tendency and varies over a limited range with body mass (type I), or that it does not vary systematically with body mass (type II). We methodologically improved these criteria and then applied them to life history traits of amphibians, Anura, Caudata (eleven traits), and reptiles (eight traits). The numbers of invariant traits identified by criteria differed across amphibian orders and between amphibians and reptiles. Reproductive output (maximum number of reproductive events per year), incubation time, length of larval period, and metamorphosis size were type I and II invariant across amphibians. In both amphibian orders, reproductive output and metamorphosis size were type I and II invariant. In Anura, incubation time and length of larval period and in Caudata, incubation time were further type II invariant. In reptiles, however, only number of clutches per year was invariant (type II). All these differences could reflect that in reptiles body size and in amphibians, Anura, and Caudata metamorphosis (neotenic species go not through it) and the trend toward independence of egg and larval development from water additionally constrained life history evolution. We further demonstrate that all invariance criteria worked for amphibian and reptilian life history traits, although we corroborated some known and identified new limitations to their application.     

Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use

Probiotic therapy through bioaugmentation is a feasible disease mitigation strategy based on growing evidence that microbes contribute to host defences of plants and animals. Amphibians are currently threatened by the rapid global spread of the pathogen, Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis. Bioaugmentation of locally occurring protective bacteria on amphibians has mitigated this disease effectively in laboratory trials and one recent field trial. Areas still naïve to Bd provide an opportunity for conservationists to proactively implement probiotic strategies to prevent further amphibian declines. In areas where Bd is endemic, bioaugmentation can facilitate repatriation of susceptible amphibians currently maintained in assurance colonies. Here, we synthesise the current research in amphibian microbial ecology and bioaugmentation to identify characteristics of effective probiotics in relation to their interactions with Bd, their host, other resident microbes and the environment. To target at‐risk species and amphibian communities, we develop sampling strategies and filtering protocols that result in probiotics that inhibit Bd under ecologically relevant conditions and persist on susceptible amphibians. This filtering tool can be used proactively to guide amphibian disease mitigation and can be extended to other taxa threatened by emerging infectious diseases.     

A comparison of understanding of the amphibian crisis by zoo visitors across three countries

Despite the global declines in the rate of amphibians, evaluation of public understanding of the crisis has not yet been carried out. We surveyed visitors (n = 1,293) at 15 zoos in Brazil, New Zealand, and the United Kingdom, using a certainty‐based assessment method to compare visitor knowledge of the global amphibian crisis. We further analyzed zoo educational material about amphibians to explore its potential to raise awareness through amphibian‐focused environmental education. Visitors in the three countries had relatively little understanding of amphibians and the global amphibian crisis. When the degree of confidence in answering the questions (high, medium, and low) is accounted for, correct answers varied between 28% and 39%. This compared to scores of between 58% and 73% when the degree of confidence in responding was not accounted for. However, specific areas of knowledge (e.g., biology, conservation, biogeography, and conceptual ideas) varied significantly across the countries. Visitors had a weaker grasp of biogeographical and conservation issues than general amphibian biology. Zoo visitors in Brazil knew less about amphibian conservation than those in New Zealand or the United Kingdom. There was less amphibian‐focused content in educational materials in zoos in Brazil than there was in the United Kingdom. Improving information about the global amphibian crisis may increase support for future conservation actions. Outreach education is one of the most important approaches in any strategic planning for conservation of species. Amphibian‐focused environmental education at institutions such as zoos and aquaria can be a crucial intervention to support amphibian conservation worldwide.     

Measuring the meltdown: drivers of global amphibian extinction and decline

Habitat loss, climate change, over-exploitation, disease and other factors have been hypothesised in the global decline of amphibian biodiversity. However, the relative importance of and synergies among different drivers are still poorly understood. We present the largest global analysis of roughly 45% of known amphibians (2,583 species) to quantify the influences of life history, climate, human density and habitat loss on declines and extinction risk. Multi-model Bayesian inference reveals that large amphibian species with small geographic range and pronounced seasonality in temperature and precipitation are most likely to be Red-Listed by IUCN. Elevated habitat loss and human densities are also correlated with high threat risk. Range size, habitat loss and more extreme seasonality in precipitation contributed to decline risk in the 2,454 species that declined between 1980 and 2004, compared to species that were stable (n = 1,545) or had increased (n = 28). These empirical results show that amphibian species with restricted ranges should be urgently targeted for conservation.     

Batrachology of Japan and adjacent regions - a systematic review

As is the case with most other organisms, studies of amphibians started with systematics as the basis for many other biological fields, but systematics itself has endured a slower progress than other fields of biology have enjoyed for a long time. Nevertheless, philosophical and methodological 'revolutions' in the past 30 years, combined with more recent progress in biochemical and molecular techniques, have been forcing current systematics into a great change. Stejneger's (1907) monumental book, the first thorough review of amphibians from Japan and adjacent regions, was published nearly a century ago, and since then, the increase in number of areas that have been closely surveyed, together with the application of new theories and methods, have greatly enlarged our knowledge of the amphibian fauna in this region. For example, extensive experiments by the Hiroshima School using artificial hybridization techniques greatly contributed to our understandings of relationships among some groups of amphibians that had been taxonomically confusing. In addition to this, new species discovered by more detailed field surveys in a wider area and cryptic species revealed by analyses of isozymes and acoustic properties have made for a great increment in the number of taxa in this region. Further, analyses of DNA sequences now enable us to infer the affinities of taxa with few phylogenetically informative phenotypic properties, and the resultant phylogenetic hypotheses further contribute to our understandings of biogeography and many other issues on amphibian evolution. From these advances, it has been clarified that the amphibian species diversity is far greater than was previously expected, which in turn means a high endemism within particular regions. It is expected that future studies will also reveal exact systematic relationships of wide-ranging species, both those occurring within this region and those extending outside of it. For that purpose, international and interdisciplinary studies are indispensable. But what is also necessary is to conserve amphibian populations so that they will not disappear before their true relationships are realized. Knowledge of systematics among young amphibian biologists is also a matter of high priority.     

Density‐dependent and density‐independent drivers of population change in Barton Springs salamanders

Understanding population change is essential for conservation of imperiled species, such as amphibians. Worldwide amphibian declines have provided an impetus for investigating their population dynamics, which can involve both extrinsic (density‐independent) and intrinsic (density‐dependent) drivers acting differentially across multiple life stages or age classes. In this study, we examined the population dynamics of the endangered Barton Springs Salamander (Eurycea sosorum) using data from a long‐term monitoring program. We were interested in understanding both the potential environmental drivers (density‐independent factors) and demographic factors (interactions among size classes, negative density dependence) to better inform conservation and management activities. We used data from three different monitoring regimes and multivariate autoregressive state‐space models to quantify environmental effects (seasonality, discharge, algae, and sediment cover), intraspecific interactions among three size classes, and intra‐class density dependence. Results from our primary data set revealed similar patterns among sites and size classes and were corroborated by our out‐of‐sample data. Cross‐correlation analysis showed juvenile abundance was most strongly correlated with a 9‐month lag in aquifer discharge, which we suspect is related to inputs of organic carbon into the aquifer. However, sedimentation limited juvenile abundance at the surface, emphasizing the importance of continued sediment management. Recruitment from juveniles to the sub‐adult size class was evident, but negative density‐dependent feedback ultimately regulated each size class. Negative density dependence may be an encouraging sign for the conservation of E. sosorum because populations that can reach carrying capacity are less likely to go extinct compared to unregulated populations far below their carrying capacity. However, periodic population declines coupled with apparent migration into the aquifer complicate assessments of species status. Although both density‐dependent and density‐independent drivers of population change are not always apparent in time series of animal populations, both have important implications for conservation and management of E. sosorum.