An interaction between climate change and infectious disease drove widespread amphibian declines

Climate change might drive species declines by altering species interactions, such as host–parasite interactions. However, few studies have combined experiments, field data, and historical climate records to provide evidence that an interaction between climate change and disease caused any host declines. A recently proposed hypothesis, the thermal mismatch hypothesis, could identify host species that are vulnerable to disease under climate change because it predicts that cool‐ and warm‐adapted hosts should be vulnerable to disease at unusually warm and cool temperatures, respectively. Here, we conduct experiments on Atelopus zeteki, a critically endangered, captively bred frog that prefers relatively cool temperatures, and show that frogs have high pathogen loads and high mortality rates only when exposed to a combination of the pathogenic chytrid fungus (Batrachochytrium dendrobatidis) and high temperatures, as predicted by the thermal mismatch hypothesis. Further, we tested various hypotheses to explain recent declines experienced by species in the amphibian genus Atelopus that are thought to be associated with B. dendrobatidis and reveal that these declines are best explained by the thermal mismatch hypothesis. As in our experiments, only the combination of rapid increases in temperature and infectious disease could account for the patterns of declines, especially in species adapted to relatively cool environments. After combining experiments on declining hosts with spatiotemporal patterns in the field, our findings are consistent with the hypothesis that widespread species declines, including possible extinctions, have been driven by an interaction between increasing temperatures and infectious disease. Moreover, our findings suggest that hosts adapted to relatively cool conditions will be most vulnerable to the combination of increases in mean temperature and emerging infectious diseases.     

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.     

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.     

Ecophysiology meets conservation: understanding the role of disease in amphibian population declines

Infectious diseases are intimately associated with the dynamics of biodiversity. However, the role that infectious disease plays within ecological communities is complex. The complex effects of infectious disease at the scale of communities and ecosystems are driven by the interaction between host and pathogen. Whether or not a given host-pathogen interaction results in progression from infection to disease is largely dependent on the physiological characteristics of the host within the context of the external environment. Here, we highlight the importance of understanding the outcome of infection and disease in the context of host ecophysiology using amphibians as a model system. Amphibians are ideal for such a discussion because many of their populations are experiencing declines and extinctions, with disease as an important factor implicated in many declines and extinctions. Exposure to pathogens and the host's responses to infection can be influenced by many factors related to physiology such as host life history, immunology, endocrinology, resource acquisition, behaviour and changing climates. In our review, we discuss the relationship between disease and biodiversity. We highlight the dynamics of three amphibian host-pathogen systems that induce different effects on hosts and life stages and illustrate the complexity of amphibian-host-parasite systems. We then review links between environmental stress, endocrine-immune interactions, disease and climate change.     

Global amphibian declines: sorting the hypotheses

Abstract. Reports of malformed amphibians and global amphibian declines have led to public concern, particularly because amphibians are thought to be indicator species of overall environmental health. The topic also draws scientific attention because there is no obvious, simple answer to the question of what is causing amphibian declines? Complex interactions of several anthropogenic factors are probably at work, and understanding amphibian declines may thus serve as a model for understanding species declines in general. While we have fewer answers than we would like, there are six leading hypotheses that we sort into two classes. For class I hypotheses, alien species, over‐exploitation and land use change, we have a good understanding of the ecological mechanisms underlying declines; these causes have affected amphibian populations negatively for more than a century. However, the question remains as to whether the magnitude of these negative effects increased in the 1980s, as scientists began to notice a global decline of amphibians. Further, remedies for these problems are not simple. For class II hypotheses, global change (including UV radiation and global climate change), contaminants and emerging infectious diseases we have a poor, but improving understanding of how each might cause declines. Class II factors involve complex and subtle mechanistic underpinnings, with probable interactions among multiple ecological and evolutionary variables. They may also interact with class I hypotheses. Suspected mechanisms associated with class II hypotheses are relatively recent, dating from at least the middle of the 20th century. Did these causes act independently or in concert with pre‐existing negative forces of class I hypotheses to increase the rate of amphibian declines to a level that drew global attention? We need more studies that connect the suspected mechanisms underlying both classes of hypotheses with quantitative changes in amphibian population sizes and species numbers. An important step forward in this task is clarifying the hypotheses and conditions under which the various causes operate alone or together.     

Global amphibian declines: a perspective from the Caribbean

Recent concern over the possibility of a global decline in amphibians prompted this assessment of the West Indian species. At the species level, the West Indian amphibian fauna (156 species, all frogs and toads) has not undergone a general decline, and no species is known to be extinct. However, one Puerto Rican species (Eleutherodactylus karlschmidti) has not been seen in over ten years despite considerable search effort. Seven other species, including the Puerto Rican livebearing frog (E. jasperi), have not been seen recently, although their present status cannot be determined until additional effort is made to locate them. Two stream-associated species on Hispaniola (E. semipalmatus and Hyla vasta) appear to have declined in recont years, probably due to the alteration of riparian habitats by deforestation. Other vertebrate groups in the West Indies, such as mammals, have been more affected by human-caused environmental degradation than have amphibians. Large-scale extinctions of frogs and other forest-dwelling species are not expected to occur until forest cover reaches very low levels. Haiti is on the brink of such extinctions with less than 1% of its forest cover remaining. Two recommendations are made to help curtail the expected loss of biodiversity: (i) import charcoal to replace that produced by burning native trees (used as cooking fuel), as an immediate measure, and (ii) control human population growth, as a long-term solution.     

Consistent trophic amplification of marine biomass declines under climate change

The impact of climate change on the marine food web is highly uncertain. Nonetheless, there is growing consensus that global marine primary production will decline in response to future climate change, largely due to increased stratification reducing the supply of nutrients to the upper ocean. Evidence to date suggests a potential amplification of this response throughout the trophic food web, with more dramatic responses at higher trophic levels. Here we show that trophic amplification of marine biomass declines is a consistent feature of the Coupled Model Intercomparison Project Phase 5 (CMIP5) Earth System Models, across different scenarios of future climate change. Under the business‐as‐usual Representative Concentration Pathway 8.5 (RCP8.5) global mean phytoplankton biomass is projected to decline by 6.1% ± 2.5% over the twenty‐first century, while zooplankton biomass declines by 13.6% ± 3.0%. All models project greater relative declines in zooplankton than phytoplankton, with annual zooplankton biomass anomalies 2.24 ± 1.03 times those of phytoplankton. The low latitude oceans drive the projected trophic amplification of biomass declines, with models exhibiting variable trophic interactions in the mid‐to‐high latitudes and similar relative changes in phytoplankton and zooplankton biomass. Under the assumption that zooplankton biomass is prey limited, an analytical explanation of the trophic amplification that occurs in the low latitudes can be derived from generic plankton differential equations. Using an ocean biogeochemical model, we show that the inclusion of variable C:N:P phytoplankton stoichiometry can substantially increase the trophic amplification of biomass declines in low latitude regions. This additional trophic amplification is driven by enhanced nutrient limitation decreasing phytoplankton N and P content relative to C, hence reducing zooplankton growth efficiency. Given that most current Earth System Models assume that phytoplankton C:N:P stoichiometry is constant, such models are likely to underestimate the extent of negative trophic amplification under projected climate change.     

Predicted insect diversity declines under climate change in an already impoverished region

Being ectotherms, insects are predicted to suffer more severely from climate change than warm-blooded animals. We forecast possible changes in diversity and composition of butterflies, grasshoppers and dragonflies in Belgium under increasingly severe climate change scenarios for the year 2100. Two species distribution modelling techniques (Generalised Linear Models and Generalised Additive Models), were combined via a conservative version of the ensemble forecasting strategy to predict present-day and future species distributions, considering the species as potentially present only if both modelling techniques made such a prediction. All models applied were fair to good, according to the AUC (area under the curve of the receiver operating characteristic plot), sensitivity and specificity model performance measures based on model evaluation data. Butterfly and grasshopper diversity were predicted to decrease significantly in all scenarios and species-rich locations were predicted to move towards higher altitudes. Dragonfly diversity was predicted to decrease significantly in all scenarios, but dragonfly-rich locations were predicted to move upwards only in the less severe scenarios. The largest turnover rates were predicted to occur at higher altitudes for butterflies and grasshoppers, but at intermediate altitudes for dragonflies. Our results highlight the challenge of building conservation strategies under climate change, because the changes in the sites important for different groups will not overlap, increasing the area needed for protection. We advocate that possible conservation and policy measures to mitigate the potentially strong impacts of climate change on insect diversity in Belgium should be much more pro-active and flexible than is the case presently.     

Water loss and temperature interact to compound amphibian vulnerability to climate change

Ectotherm thermal physiology is frequently used to predict species responses to changing climates, but for amphibians, water loss may be of equal or greater importance. Using physical models, we estimated the frequency of exceeding the thermal optimum (T_opt) or critical evaporative water loss (EWL_crit) limits, with and without shade‐ or water‐seeking behaviours. Under current climatic conditions (2002–2012), we predict that harmful thermal (>T_opt) and hydric (>EWL_crit) conditions limit the activity of amphibians during ~70% of snow‐free days in sunny habitats. By the 2080s, we estimate that sunny and dry habitats will exceed one or both of these physiological limits during 95% of snow‐free days. Counterintuitively, we find that while wet environments eliminate the risk of critical EWL, they do not reduce the risk of exceeding T_opt (+2% higher). Similarly, while shaded dry environments lower the risk of exceeding T_opt, critical EWL limits are still exceeded during 63% of snow‐free days. Thus, no single environment that we evaluated can simultaneously reduce both physiological risks. When we forecast both temperature and EWL into the 2080s, both physiological thresholds are exceeded in all habitats during 48% of snow‐free days, suggesting that there may be limited opportunity for behaviour to ameliorate climate change. We conclude that temperature and water loss act synergistically, compounding the ecophysiological risk posed by climate change, as the combined effects are more severe than those predicted individually. Our results suggest that predictions of physiological risk posed by climate change that do not account for water loss in amphibians may be severely underestimated and that there may be limited scope for facultative behaviours to mediate rapidly changing environments.     

Future potential distribution of the emerging amphibian chytrid fungus under anthropogenic climate change

Anthropogenic climate change poses a major threat to global biodiversity with a potential to alter biological interactions at all spatial scales. Amphibians are the most threatened vertebrates and have been subject to increasing conservation attention over the past decade. A particular concern is the pandemic emergence of the parasitic chytrid fungus Batrachochytrium dendrobatidis, which has been identified as the cause of extremely rapid large-scale declines and species extinctions. Experimental and observational studies have demonstrated that the host-pathogen system is strongly influenced by climatic parameters and thereby potentially affected by climate change. Herein we project a species distribution model of the pathogen onto future climatic scenarios generated by the IPCC to examine their potential implications on the pandemic. Results suggest that predicted anthropogenic climate change may reduce the geographic range of B. dendrobatidis and its potential influence on amphibian biodiversity.     

Conservation effectiveness of protected areas for Hong Kong butterflies declines under climate change

Protected areas are important in conserving the rapid decline of biodiversity in the Anthropocene. Yet uncertainty persists whether protected areas will continue to meet conservation goals if climate change causes community or ecosystem shifts. Previous research has proven equivocal with some studies finding protected areas fail conservation objectives and others finding objectives are largely met. The effectiveness of protected area systems within tropical Asia and for insects are particularly under-studied. Using species distribution modeling of 68 butterfly species (15,346 locality records), we carried out an evaluation of the effectiveness of protected areas in Hong Kong, one of the most well-covered (40% land area) protected area systems in the Asian tropics, and projected how the ability to protect biodiversity would change under different climate change scenarios and different conservation target schemes. Under climate change, 15–37% of the modeled species in 2000 were projected to become extirpated by 2050. Under all conservation target schemes, the proportion of species unprotected increased or leveled, by up to as much as 7%. If buffer grids were considered as unprotected, the increase in these gap species was much greater, by up to as much as 22%. These results together indicate that under climate change, the effectiveness of protected areas for butterflies in Hong Kong is likely to decrease despite the territory’s relatively high proportion of protected area coverage. We also highlight here the importance of the fortification of partly protected areas in mediating biodiversity loss under the impacts of global change.     

Questioning the use of an amphibian colour morph as an indicator of climate change

The effects of recent climate changes on earth ecosystems are likely among the most important ecological concerns in human history. Good bioindicators are essential to properly assess the magnitude of these changes. In the last decades, studies have suggested that the morph proportion of the eastern red‐backed salamander (Plethodon cinereus), one of the most widely distributed and abundant vertebrate species in forests of eastern North America, could be used as a proxy for monitoring climate changes. Based on new discoveries in the northern areas of the species' range and on one of the largest compilation ever made for a vertebrate in North America (236 109 observations compiled from 1880 to 2013 in 1148 localities), we demonstrate however that climatic and geographic variables do not influence the colour morph proportions in P. cinereus populations. Consequently, we show that the use of colour morph proportions of this species do not perform as an indicator of climate change. Our findings indicate that bioindicator paradigms can be significantly challenged by new ecological research and more representative databases.     

Riding the wave: structural and energetic principles of helical membrane proteins

Genome sequencing efforts have revealed that perhaps as many as 20-40% of open reading frames in complex organisms may encode proteins containing at least one helical transmembrane segment. Contrasting with this approaching tidal wave of helical membrane proteins is the fact that our understanding of the sequence-structure-function relationships for membrane proteins lags far behind that of soluble proteins. This looming reality emphasizes the tremendous biochemical and structural work that remains to be done on helical membrane proteins in order to elucidate the structural and energetic principles that specify and stabilize their folds, which define their functions. These facts are not lost on the pharmaceutical industry, where successful therapeutics and major discovery efforts are targeting membrane proteins.     

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.