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.     

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.     

Infectious disease and amphibian population declines

Abstract. A series of recent papers have implicated pathogens and parasites in amphibian population declines. Here, we review evidence on the link between infectious disease and amphibian population declines. We conclude that available data provide the clearest link for the fungal disease amphibian chytridiomycosis, although other pathogens are also implicated. We suggest additional experimental and observational data that need to be collected to provide further support that these other pathogens are associated with declines. We suggest that, in common with many emerging infectious diseases (EIDs) of humans, domestic animals and other wildlife species, emergence of chytridiomycosis may be driven by anthropogenic introduction (pathogen pollution). Finally, we review a number of recent advances in the host–parasite ecology of chytridiomycosis that help explain its emergence and impact.     

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.     

Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses

Chytridiomycosis is an emerging infectious disease of amphibians caused by a chytrid fungus, Batrachochytrium dendrobatidis. This panzootic does not equally affect all amphibian species within an assemblage; some populations decline, others persist. Little is known about the factors that affect disease resistance. Differences in behavior, life history, biogeography, or immune function may impact survival. We found that an innate immune defense, antimicrobial skin peptides, varied significantly among species within a rainforest stream amphibian assemblage that has not been exposed to B. dendrobatidis. If exposed, all amphibian species at this central Panamanian site are at risk of population declines. In vitro pathogen growth inhibition by peptides from Panamanian species compared with species with known resistance (Rana pipiens and Xenopus laevis) or susceptibility (Bufo boreas) suggests that of the nine species examined, two species (Centrolene prosoblepon and Phyllomedusa lemur) may demonstrate strong resistance, and the other species will have a higher risk of disease-associated population declines. We found little variation among geographically distinct B. dendrobatidis isolates in sensitivity to an amphibian skin peptide mixture. This supports the hypothesis that B. dendrobatidis is a generalist pathogen and that species possessing an innate immunologic defense at the time of disease emergence are more likely to survive.     

Amphibian declines: future directions

Abstract. The amphibian decline problem is complex, and there is no easy solution. I highlight four major areas of future research that should increase our ability to detect declines, elucidate their underlying mechanisms, and advance our capacity to manage and conserve amphibian populations. First, a statistically sensitive monitoring approach is necessary to determine the distribution and abundance of amphibian populations, to assess whether they are declining, and to quantify the extent of declines. Most amphibian populations characteristically fluctuate, detection probabilities may be low for many species and populations tend to decline in numbers between years more often than they increase. These traits make establishing monitoring programmes difficult and distinguishing declines from natural fluctuations challenging. It is thus necessary to determine the best monitoring techniques based on their statistical power and to use appropriate statistical methods for detecting population trends. Secondly, although amphibian population studies occur most commonly at single or few breeding sites, research should occur often at the landscape level, and conservation efforts should focus on suitable habitat (whether or not it is occupied) and dispersal capabilities of species. Metapopulation dynamics are probably important for many species, but we must be cautious how we define metapopulations. That is, the term ‘metapopulation’ is currently used to define a wide range of demographic situations in amphibian populations, each with different management implications. Thirdly, recent advances in molecular genetic techniques make it possible to infer demographic events such as effects of recent fragmentation, bottlenecks or hybridization. Molecular techniques can be used in conjunction with census surveys to bolster knowledge about demographic processes such as declines. Alternatively, in the absence of long‐term census data, molecular data can be used to infer population trends. New genomic approaches may make estimating adaptive genetic variation more feasible. Fourthly, multi‐factorial studies are needed to disentangle the complexity of the several putative causes that probably interact to cause amphibian declines. Recent studies demonstrate the value of a multi‐factorial approach, and more work is needed to elucidate the synergistic effects of multiple environmental factors affecting amphibian populations simultaneously worldwide.     

Ultraviolet radiation, toxic chemicals and amphibian population declines

Abstract. As part of an overall ‘biodiversity crisis’, many amphibian populations are in decline throughout the world. Numerous factors have contributed to these declines, including habitat destruction, pathogens, increasing ultraviolet (UV) radiation, introduced non‐native species and contaminants. In this paper we review the contribution of increasing UV radiation and environmental contamination to the global decline of amphibian populations. Both UV radiation and environmental contaminants can affect amphibians at all life stages. Exposure to UV radiation and to certain contaminants can kill amphibians and induce sublethal affects in embryos, larvae and adults. Moreover, UV radiation and contaminants may interact with one another synergistically. Synergistic interactions of UV radiation with contaminants can enhance the detrimental effects of the contaminant and UV radiation.     

The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines

Amphibian species have experienced population declines and extinctions worldwide that are unprecedented in recent history. Many of these recent declines have been linked to a pathogenic skin fungus, Batrachochytrium dendrobatidis, or to iridoviruses of the genus Ranavirus. One of the first lines of defense against pathogens that enter by way of the skin are antimicrobial peptides synthesized and stored in dermal granular glands and secreted into the mucus following alarm or injury. Here, I review what is known about the capacity of amphibian antimicrobial peptides from diverse amphibians to inhibit B. dendrobatidis or ranavirus infections. When multiple species were compared for the effectiveness of their in vitro antimicrobial peptides defenses against B. dendrobatidis, non-declining species of rainforest amphibians had more effective antimicrobial peptides than species in the same habitat that had recently experienced population declines. Further, there was a significant correlation between the effectiveness of the antimicrobial peptides and resistance of the species to experimental infection. These studies support the hypothesis that antimicrobial peptides are an important component of innate defenses against B. dendrobatidis. Some amphibian antimicrobial peptides inhibit ranavirus infections and infection of human T lymphocytes by the human immunodeficiency virus (HIV). An effective antimicrobial peptide defense against skin pathogens appears to depend on a diverse array of genes expressing antimicrobial peptides. The production of antimicrobial peptides may be regulated by signals from the pathogens. However, this defense must also accommodate potentially beneficial microbes on the skin that compete or inhibit growth of the pathogens. How this delicate balancing act is accomplished is an important area of future research.     

Rainforest frogs of the Australian Wet Tropics: guild classification and the ecological similarity of declining species.

Rainforest frogs are classified into nine ecological guilds based on features of reproduction, habitat use, temporal activity, microhabitat and body size. The largest ecological differences are between the microhylid frogs and the rest of the frog species. Within the non-microhylids, there are two primary groups consisting of (i) regionally endemic rainforest specialists, and (ii) a more ecologically diverse group of species that are less specialized in their habitat requirements. Most of the regionally endemic rainforest specialists, which includes species in three ecological guilds, have declined or gone missing in recent years. Multivariate analyses of the ecological characteristics of these species show that it is not a single characteristic that isolates those species that have declined from those which have not. The guilds that have undergone significant population declines in the Wet Tropics are all characterized by the combination of low fecundity, a high degree of habitat specialization and reproduction in flowing streams. These results have important implications for the determination of the causal factors in the unexplained global decline of many amphibian species.     

Host size influences the effects of four isolates of an amphibian chytrid fungus

Understanding factors that influence host–pathogen interactions is key to predicting outbreaks in natural systems experiencing environmental change. Many amphibian population declines have been attributed to an amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd). While this fungus is widespread, not all Bd‐positive populations have been associated with declines, which could be attributed to differences in pathogen virulence or host susceptibility. In a laboratory experiment, we examined the effects of Bd isolate origin, two from areas with Bd‐associated amphibian population declines (El Copé, Panama, and California, USA) and two from areas without Bd‐related population declines (Ohio and Maine, USA), on the terrestrial growth and survival of American toad (Anaxyrus americanus) metamorphs reared in larval environments with low or high intraspecific density. We predicted that (1) Bd isolates from areas experiencing declines would have greater negative effects than Bd isolates from areas without declines, and (2) across all isolates, growth and survival of smaller toads from high‐density larval conditions would be reduced by Bd exposure compared to larger toads from low‐density larval conditions. Our results showed that terrestrial survival was reduced for smaller toads exposed to Bd with variation in the response to different isolates, suggesting that smaller size increased susceptibility to Bd. Toads exposed to Bd gained less mass, which varied by isolate. Bd isolates from areas with population declines, however, did not have more negative effects than isolates from areas without recorded declines. Most strikingly, our study supports that host condition, measured by size, can be indicative of the negative effects of Bd exposure. Further, Bd isolates’ impact may vary in ways not predictable from place of origin or occurrence of disease‐related population declines. This research suggests that amphibian populations outside of areas experiencing Bd‐associated declines could be impacted by this pathogen and that the size of individuals could influence the magnitude of Bd's impact.     

Analysis of three amphibian populations with quarter-century long time-series.

Amphibians are in decline in many parts of the world. Long tme-series of amphibian populations are necessary to distinguish declines from the often strong fluctuations observed in natural populations. Time-series may also help to understand the causes of these declines. We analysed 23-28-year long time-series of the frog Rana temporaria. Only one of the three studied populations showed a negative trend which was probably caused by the introduction of fish. Two populations appeared to be density regulated. Rainfall had no obvious effect on the population fluctuations. Whereas long-term studies of amphibian populations are valuable to document population declines, most are too short to reveal those factors that govern population dynamics or cause amphibian populations to decline.     

Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii

Recent outbreaks of new diseases in many ecosystems are caused by novel pathogens, impaired host immunity, or changing environmental conditions. Identifying the source of emergent pathogens is critical for mitigating the impacts of diseases, and understanding the cause of their recent appearances. One ecosystem suffering outbreaks of disease in the past decades is coral reefs, where pathogens such as the fungus Aspergillus sydowii have caused catastrophic population declines in their hosts. Aspergillosis is one of the best-characterized coral diseases, yet the origin of this typically terrestrial fungus in marine systems remains unknown. We examined the genetic structure of a global sample of A. sydowii, including isolates from diseased corals, diseased humans, and environmental sources. Twelve microsatellite markers reveal a pattern of global panmixia among the fungal isolates. A single origin of the pathogen into marine systems seems unlikely given the lack of isolation by distance and lack of evidence for a recent bottleneck. A neighbour-joining phylogeny shows that sea fan isolates are interspersed with environmental isolates, suggesting there have been multiple introductions from land into the ocean. Overall, our results underscore that A. sydowii is a true opportunist, with a diversity of nonrelated isolates able to cause disease in corals. This study highlights the challenge in distinguishing between the role of environment in allowing opportunistic pathogens to increase and actual introductions of new pathogenic microorganisms for coral diseases.     

Individualistic Population Responses of Five Frog Species in Two Changing Tropical Environments over Time

Roughly 40% of amphibian species are in decline with habitat loss, disease, and climate change being the most cited threats. Heterogeneity of extrinsic (e.g. climate) and intrinsic (e.g. local adaptations) factors across a species’ range should influence population response to climate change and other threats. Here we examine relative detectability changes for five direct-developing leaf litter frogs between 42-year sampling periods at one Lowland Tropical Forest site (51 m.a.s.l.) and one Premontane Wet Forest site (1100 m.a.s.l.) in southwest Costa Rica. We identify individualistic changes in relative detectability among populations between sampling periods at different elevations. Both common and rare species showed site-specific declines, and no species exhibited significant declines at both sites. Detection changes are correlated with changes in temperature, dry season rainfall, and leaf litter depth since1969. Our study species share Least Concern conservation status, life history traits, and close phylogenetic relationship, yet their populations changed individualistically both within and among species. These results counter current views of the uniformity or predictability of amphibian decline response and suggest additional complexity for conservation decisions.     

There Is No Evidence for a Temporal Link between Pathogen Arrival and Frog Extinctions in North-Eastern Australia

Pathogen spread can cause population declines and even species extinctions. Nonetheless, in the absence of tailored monitoring schemes, documenting pathogen spread can be difficult. In the case of worldwide amphibian declines the best present understanding is that the chytrid fungus Batrachochytrium dendrobatidis (Bd) has recently spread, causing amphibian declines and extinction in the process. However, good evidence demonstrating pathogen arrival followed by amphibian decline is rare, and analysis of putative evidence is often inadequate. Here we attempt to examine the relationship between Bd arrival and amphibian decline across north-eastern Australia, using sites where a wave-like pattern of amphibian decline was first noticed and at which intensive research has since been conducted. We develop an analytical framework that allows rigorous estimation of pathogen arrival date, which can then be used to test for a correlation between the time of pathogen arrival and amphibian decline across sites. Our results show that, with the current dataset, the earliest possible arrival date of Bd in north-eastern Australia is completely unresolved; Bd could have arrived immediately before sampling commenced or may have arrived thousands of years earlier, the present data simply cannot say. The currently available data are thus insufficient to assess the link between timing of pathogen arrival and population decline in this part of the world. This data insufficiency is surprising given that there have been decades of research on chytridiomycosis in Australia and that there is a general belief that the link between Bd arrival and population decline is well resolved in this region. The lack of data on Bd arrival currently acts as a major impediment to determining the role of environmental factors in driving the global amphibian declines, and should be a major focus of future research.     

Mortality Rates Differ Among Amphibian Populations Exposed to Three Strains of a Lethal Ranavirus

Infectious diseases are a growing threat to biodiversity, in many cases because of synergistic effects with habitat loss, environmental contamination, and climate change. Emergence of pathogens as new threats to host populations can also arise when novel combinations of hosts and pathogens are unintentionally brought together, for example, via commercial trade or wildlife relocations and reintroductions. Chytrid fungus (Batrachochytrium dendrobatidis) and amphibian ranaviruses (family Iridoviridae) are pathogens implicated in global amphibian declines. The emergence of disease associated with these pathogens appears to be at least partly related to recent translocations over large geographic distances. We experimentally examined the outcomes of novel combinations of host populations and pathogen strains using the amphibian ranavirus Ambystoma tigrinum virus (ATV) and barred tiger salamanders (Ambystoma mavortium, formerly considered part of the Ambystoma tigrinum complex). One salamander population was highly resistant to lethal infections by all ATV strains, including its own strain, and mortality rates differed among ATV strains according to salamander population. Mortality rates in novel pairings of salamander population and ATV strain were not predictable based on knowledge of mortality rates when salamander populations were exposed to their own ATV strain. The underlying cause(s) for the differences in mortality rates are unknown, but local selection pressures on salamanders, viruses, or both, across the range of this widespread host–pathogen system are a plausible hypothesis. Our study highlights the need to minimize translocations of amphibian ranaviruses, even among conspecifc host populations, and the importance of considering intraspecific variation in endeavors to manage wildlife diseases.     

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.     

Amphibian chytrid fungus Batrachochytrium dendrobatidis in Cusuco National Park, Honduras

Amphibian population declines in Honduras have long been attributed to habitat degradation and pollution, but an increasing number of declines are now being observed from within the boundaries of national parks in pristine montane environments. The amphibian chytrid fungus Batrachochytrium dendrobatidis has been implicated in these declines and was recently documented in Honduras from samples collected in Pico Bonito National Park in 2003. This report now confirms Cusuco National Park, a protected cloud forest reserve with reported amphibian declines, to be the second known site of infection for Honduras. B. dendrobatidis infection was detected in 5 amphibian species: Craugastor rostralis, Duellmanohyla soralia, Lithobates maculata, Plectrohyla dasypus, and Ptychohyla hypomykter. D. soralia, P. dasypus, and P. hypomykter are listed as critically endangered in the IUCN Red List of Threatened Species and have severely fragmented or restricted distributions. Further investigations are necessary to determine whether observed infection levels indicate an active B. dendrobatidis epizootic with the potential to cause further population declines and extinction.     

Genetic characterization of chytrids isolated from larval amphibians collected in central and east Texas

Chytridiomycosis, an emerging infectious disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), has caused amphibian population declines worldwide. Bd was first described in the 1990s and there are still geographic gaps in the genetic analysis of this globally distributed pathogen. Relatively few genetic studies have focused on regions where Bd exhibits low virulence, potentially creating a bias in our current knowledge of the pathogen's genetic diversity. Disease-associated declines have not been recorded in Texas (USA), yet Bd has been detected on amphibians in the state. These strains have not been isolated and characterized genetically; therefore, we isolated, cultured, and genotyped Bd from central Texas and compared isolates to a panel of previously genotyped strains distributed across the Western Hemisphere. We also isolated other chytrids from east Texas not known to infect amphibians. To identify larval amphibian hosts, we sequenced part of the COI gene. Among 37 Bd isolates from Texas, we detected 19 unique multi-locus genotypes, but found no genetic structure associated with host species, Texas localities, or across North America. Isolates from central Texas exhibit high diversity and genetically cluster with BdGPL isolates from the western U.S. that have caused amphibian population declines. This study genetically characterizes isolates of Bd from the south central U.S. and adds to the global knowledge of Bd genotypes.     

The Link Between Rapid Enigmatic Amphibian Decline and the Globally Emerging Chytrid Fungus

Amphibians are globally declining and approximately one-third of all species are threatened with extinction. Some of the most severe declines have occurred suddenly and for unknown reasons in apparently pristine habitats. It has been hypothesized that these “rapid enigmatic declines” are the result of a panzootic of the disease chytridiomycosis caused by globally emerging amphibian chytrid fungus. In a Species Distribution Model, we identified the potential distribution of this pathogen. Areas and species from which rapid enigmatic decline are known significantly overlap with those of highest environmental suitability to the chytrid fungus. We confirm the plausibility of a link between rapid enigmatic decline in worldwide amphibian species and epizootic chytridiomycosis.