the wave: Reconciling the roles of disease and climate change in am- phibian declines. PLoS Biology 6:e72 (original) (raw)
Related papers
Biological Conservation, 2017
The impacts of pathogen emergence in naïve hosts can be catastrophic, and pathogen spread now ranks as a major threat to biodiversity. However, pathogen impacts can persist for decades after epidemics and produce variable host outcomes. Chytridiomycosis in amphibians (caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd) is an exemplar, with impacts ranging from rapid population crashes and extinctions, to population declines and subsequent recoveries. Here, we investigate long-term impacts associated with chytridiomycosis in Australia. We conducted a continent-wide assessment of the disease, reviewing data collected since the arrival of Bd in about 1978, to assess and characterize mechanisms driving past, present and future impacts. We found chytridiomycosis to be implicated in the extinction or decline of 43 of Australia's 238 amphibian species. Population trajectories of declined species are highly variable; six species are experiencing ongoing declines, eight species are apparently stable and 11 species are recovering. Our results highlight that while some species are expanding, Bd continues to threaten species long after its emergence. Australian case-studies and synthesis of the global chytridiomycosis literature suggests that amphibian reservoir hosts are associated with continued declines in endemically infected populations, while population stability is promoted by environmental conditions that restrict Bd impact, and maintenance of high recruitment capacity that can offset mortality. Host genetic adaptation or decreased pathogen virulence may facilitate species recovery, but neither has been empirically demonstrated. Understanding processes that influence Bd-host dynamics and population persistence is crucial for assessing species extinction risk and identifying strategies to conserve disease-threatened species.
2017
Emerging infectious diseases are increasingly recognized as key threats to wildlife. Batrachochytrium dendrobatidis (Bd), the causative agent of chytridiomycosis, has been implicated in mass mortalities, population declines, and local and global extinctions of many species of amphibians around the world. As such, it is currently the largest infectious disease threat to biodiversity. Understanding the distribution and spatial dynamics of Bd is crucial to predicting spread to new geographic areas, revealing the history of infection, and developing appropriate management strategies. One of the most striking features of Bd is the variability in outcome of infection that has been observed within a species, among populations. By identifying and comparing differences in variables that co-vary between populations exhibiting different infection characteristics, we can start to disentangle the mechanisms allowing for parasite persistence and proliferation. However, infection dynamics operate across nested levels of biological organization: within-host processes underlie among-host processes within a population. As such, this thesis works within the classical themes of spatial epidemiology to consider: 1) the distribution of Bd and the evidence for spatial heterogeneity in both the prevalence and intensity of infection, and 2) the role of individual-and population-level traits in defining infection outcome. The research presented, identifies that Bd functions endemically within Rana pipiens populations in Ontario. Outbreaks of chytridiomycosis are not observed, but infection dynamics show significant interannual fluctuations related to stable geographic factors and local climatic nuances experienced at particular host life history stages. However, v Rana pipiens also display variation in resistance to the pathogen, mediated by thermoregulation, dispersal behaviour, and phenotypic properties. Comparisons between host populations show variation in skin-associated bacterial communities, which may mediate susceptibility to chytridiomycosis. These bacterial communities are found to vary across latitude and between sites experiencing different levels of anthropogenic disturbance. Additionally, individual level traits, such as amphibian body temperature and body size are reported to influence bacterial community. Hence, this research highlights the importance of considering context-dependent individual-and populationlevel environmental heterogeneity, when attempting to predict the infection risk of Bd.
Batrachochytrium salamandrivorans and the Risk of a Second Amphibian Pandemic
EcoHealth, 2017
Amphibians are experiencing devastating population declines globally. A major driver is chytridiomycosis, an emerging infectious disease caused by the fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Bd was described in 1999 and has been linked with declines since the 1970s, while Bsal is a more recently discovered pathogen that was described in 2013. It is hypothesized that Bsal originated in Asia and spread via international trade to Europe, where it has been linked to salamander die-offs. Trade in live amphibians thus represents a significant threat to global biodiversity in amphibians. We review the current state of knowledge regarding Bsal and describe the risk of Bsal spread. We discuss regional responses to Bsal and barriers that impede a rapid, coordinated global effort. The discovery of a second deadly emerging chytrid fungal pathogen in amphibians poses an opportunity for scientists, conservationists, and governments to imp...
Conservation Biology, 2010
Chytridiomycosis is an emerging disease of amphibians caused by the chytrid fungus Batrachochytrium dendrobatidis (hereafter Bd) (Fisher et al. 2009). Chytridiomycosis is thought to be contributing significantly to global amphibian declines (Berger et al. 1998; Stuart et al. 2004; Skerratt et al. 2007). In the Neotropics the disease has spread in a wave-like fashion (Lips et al. 2008), and arrival at previously pathogen-free sites in this region results in mass mortalities and extinctions (Lips et al. 2008). Little is known, however, about the effects of Bd after population declines have occurred. In some places, Bd persists where it has invaded (Retallick et al. 2004). Thus, amphibians may evolve resistance to this novel pathogen such that the negative effects of Bd are attenuated over time. Murray et al. (2009) address this very important question. They used a multistate mark-recapture model to estimate survival of Bd-infected and Bd-free frogs (Litoria pearsoniana) in Queensland, where Bd has been present for 30 years. The use ofmark-recapturemethods is a clear improvement over earlier studies in which survival was estimated but did not account for imperfect detectability of animals in field studies (Faustino et al. 2004; Schmidt 2004). Murray et al. found that Bd causes a substantial reduction in survival. This matters because a reduction in adult survival can lead to amphibian population declines (Schmidt et al. 2005) and because it implies that Bd remains a dangerous pathogen, such that amphibian populations are unlikely to recover from population declines caused by Bd for many decades, if ever. Here, I point out that the apparent monthly survival estimates ofMurray et al.
Conservation Biology, 2009
Estimating disease-associated mortality and transmission processes is difficult in free-ranging wildlife but important for understanding disease impacts and dynamics and for informing management decisions. In a capture-mark-recapture study, we used a PCR-based diagnostic test in combination with multistate models to provide the first estimates of disease-associated mortality and detection, infection, and recovery rates for frogs endemically infected with the chytrid fungus Batrachochytrium dendrobatidis (Bd), which causes the pandemic amphibian disease chytridiomycosis. We found that endemic chytridiomycosis was associated with a substantial reduction (approximately 38%) in apparent monthly survival of the threatened rainforest treefrog Litoria pearsoniana despite a long period of coexistence (approximately 30 years); detection rate was not influenced by disease status; improved recovery and reduced infection rates correlated with decreased prevalence, which occurred when temperatures increased; and incorporating changes in individuals' infection status through time with multistate models increased effect size and support (98.6% vs. 71% of total support) for the presence of disease-associated mortality when compared with a Cormack-Jolly-Seber model in which infection status was restricted to the time of first capture. Our results indicate that amphibian populations can face significant ongoing pressure from chytridiomycosis long after epidemics associated with initial Bd invasions subside, an important consideration for the long-term conservation of many amphibian species worldwide. Our findings also improve confidence in estimates of disease prevalence in wild amphibians and provide a general framework for estimating parameters in epidemiological models for chytridiomycosis, an important step toward better understanding and management of this disease.
Ecology and Evolution, 2019
Numerous species of amphibians declined in Central America during the 1980s and 1990s. These declines mostly affected highland stream amphibians and have been primarily linked to chytridiomycosis, a deadly disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd). Since then, the majority of field studies on Bd in the Tropics have been conducted in midland and highland environments (>800 m) mainly because the environmental conditions of mountain ranges match the range of ideal abiotic conditions for Bd in the laboratory. This unbalanced sampling has led researchers to largely overlook host–pathogen dynamics in lowlands, where other amphibian species declined during the same period. We conducted a survey testing for Bd in 47 species (n = 348) in four lowland sites in Costa Rica to identify local host– pathogen dynamics and to describe the abiotic environment of these sites. We de‐ tected Bd in three sampling sites and 70% of the surveyed species. We found evidence that lowland study sites exhibit enzootic dynamics with low infection inten‐ sity and moderate to high prevalence (55% overall prevalence). Additionally, we found evidence that every study site represents an independent climatic zone, where local climatic differences may explain variations in Bd disease dynamics. We recommend more detection surveys across lowlands and other sites that have been historically considered unsuitable for Bd occurrence. These data can be used to identify sites for potential disease outbreaks and amphibian rediscoveries.
Evaluating the links between climate, disease spread, and amphibian declines
Proceedings of the National Academy of Sciences, 2008
Human alteration of the environment has arguably propelled the Earth into its sixth mass extinction event and amphibians, the most threatened of all vertebrate taxa, are at the forefront. Many of the worldwide amphibian declines have been caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd), and two contrasting hypotheses have been proposed to explain these declines. Positive correlations between global warming and Bd-related declines sparked the chytrid-thermal-optimum hypothesis, which proposes that global warming increased cloud cover in warm years that drove the convergence of daytime and nighttime temperatures toward the thermal optimum for Bd growth. In contrast, the spatiotemporal-spread hypothesis states that Bd-related declines are caused by the introduction and spread of Bd, independent of climate change. We provide a rigorous test of these hypotheses by evaluating ( i ) whether cloud cover, temperature convergence, and predicted temperature-dependent Bd growt...
Examining the Evidence for Chytridiomycosis in Threatened Amphibian Species
PloS one, 2011
Extinction risks are increasing for amphibians due to rising threats and minimal conservation efforts. Nearly one quarter of all threatened/extinct amphibians in the IUCN Red List is purportedly at risk from the disease chytridiomycosis. However, a closer look at the data reveals that Batrachochytrium dendrobatidis (the causal agent) has been identified and confirmed to cause clinical disease in only 14% of these species. Primary literature surveys confirm these findings; ruling out major discrepancies between Red List assessments and real-time science. Despite widespread interest in chytridiomycosis, little progress has been made between assessment years to acquire evidence for the role of chytridiomycosis in species-specific amphibian declines. Instead, assessment teams invoke the precautionary principle when listing chytridiomycosis as a threat. Precaution is valuable when dealing with the world's most threatened taxa, however scientific research is needed to distinguish between real and predicted threats in order to better prioritize conservation efforts. Fast paced, cost effective, in situ research to confirm or rule out chytridiomycosis in species currently hypothesized to be threatened by the disease would be a step in the right direction. Ultimately, determining the manner in which amphibian conservation resources are utilized is a conversation for the greater conservation community that we hope to stimulate here.