Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity.

Chytridiomycosis is an emerging fungal disease that has been implicated in the global decline of amphibian populations. Identifying climatic and geographic factors associated with its presence may be useful in control and prevention measures. Factors such as high altitude, cool temperature, and wet climate have been associated with chytridiomycosis outbreaks. Although some of these factors have been studied in a laboratory setting, there have been few studies in a natural setting. In this investigation, the relationship between altitude, average summer maximum temperature, or the amount of rainfall and the presence or absence of chytridiomycosis are statistically tested using data from 56 study sites in Australia. Currently, in Australia, 48 native species of wild amphibians have been found infected with chytridiomycosis. The 56 sites in the present study, extending along approximately 50% of the coastline of Australia, have been identified as either a chytrid site, where > or = 1 species are infected with chytridiomycosis, or a no-decline site, where none of the species present at the site are experiencing a decline or are known to be infected. The odds-ratio test and two-proportions test applied to this data indicate that the presence of chytridiomycosis in Australia is significantly related to temperature. In particular, the presence of chytridiomycosis is more likely at sites where the average summer maximum temperature is < 30 degrees C. The results of the analyses do not indicate a significant relationship between the presence of chytridiomycosis and altitude or rainfall.

Amphibians are among the most endangered vertebrate groups. One of the main reasons for their biodiversity loss is the relatively recent global spread of chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), which has contributed to the decline or extinction of at least 200 amphibian species. With relevant knowledge accumulating, it has become evident that the effects of chytridiomycosis can differ among geographic regions not only on the interspecific level but also within species. Ultimately, temporal and spatial variation in the outcome of chytridiomycosis is driven by the evolutionary arms race between the parasite and its hosts. Proximately, this variation may arise due to variation in host susceptibility, differences in the pathogenicity of different lineages of Bd, variation in prevailing environmental conditions, or interactions between these factors. Here, we summarize the evidence for each one of these possibilities and draw attention to the fact that studies considering several of these factors simultaneously are scarce, and those taking all into account are lacking entirely. Consequently, the overall interpretation of the differences in the outcomes of existent studies and experiments has remained difficult. We conclude that future research should focus on the interactive effects of co-evolutionary history, host susceptibility, Bd virulence, and relevant environmental factors on disease outcomes. These studies will help in deepening our understanding of disease dynamics, in predicting future hotspots of chytridiomycosis outbreaks, and in focusing conservation efforts to where they are most needed.

Reviewed by: Sparing Nature: The Conflict between Human Population Growth and Earth's Biodiversity J. Roberts, Ph.D. Sparing Nature: The Conflict between Human Population Growth and Earth's Biodiversity Author: Jeffrey K. McKee Publisher: Rutgers University Press, ISBN: 0813531411 (hard cover) Pages: 210 In Sparing Nature, Jeffrey K. McKee, an anthropologist at Ohio State University in the United States, makes a compelling argument in support of his proposition that there is a longstanding relationship between human population growth and the loss of plant and animal biodiversity worldwide. Reading through the pages, one can detect the ideas of Thomas Malthus, Charles Darwin, Kingsly Davis, Paul Ehrlich, Barry Commoner, Garrett Hardin and E.O. Wilson, among other notables. Clearly McKee's thinking has been importantly shaped by these scholars. All of these scholars discussed, in one form or another, problems associated with population growth. And one, E.O. Wilson, has repeatedly addressed the biodiversity problem. McKee's work differs in that it is entirely devoted to the subject of population growth and the loss of biodiversity. Using wit combined with scientific rigor, McKee takes the reader on a six million year journey, beginning with our prehuman ancestors and ending at the present day. What he shows the reader on this journey is often disturbing. But it is a "good read." It is clearly the work of an erudite, concerned and thoughtful scientist. McKee presents three propositions that are the foundation of his book. Proposition one states that "there is a very close relationship between biodiversity loss and human population growth." Proposition two states that "the most important conservation measure we can take is to slow or halt the growth of the human population." Proposition three states that "conserving biodiversity is vital to the health of our planet, and conseqently is vital to us." These propositions are based on a set of beliefs that shape the author's thinking. McKee firmly believes that a major biodiversity crisis is at hand; that humans are largely responsible for the current biodiversity crisis; that this crisis is not sustainable and is life threatening, not only to the flora and fauna of the planet, but to the human species as well; that each species plays a part in maintaining the world's ecosystems and each is important in its own right; that all life-forms compete for space and other limited resources and that human beings are out-competing other organisms for limited space and resources; and that, if rapid corrective action is not taken to radically reduce the number of human beings on the planet, extinction rates of species will accelerate in the future. McKee presents his argument within the span of nine chapters (a preface, notes, and index complete his 210 page book). Chapter I begins with an introduction to basic ecological concepts. The main propositions of the book are presented. Chapter II provides an overview of how evolution works. The fossil record is used to draw a link between population growth and the loss of biodiversity. Problems with measuring species biodiversity and species loss [End Page 87] are discussed. The claim is made that population growth, and associated expansion of humans into all ecosystems, is leading to the destruction of ecosystem biodiversity, species biodiversity and genetic biodiversity. Finally, McKee introduces Darwin's so-called "Wedge" model to illustrate how one species can push into the abyss of extinction other species. In Chapter III McKee details the evolution of pre-humans in Africa. Using the fossil record, McKee skillfully and meticulously shows that between 6 million to 1.8 million years ago our prehuman ancestors had little impact on biodiversity. It was not until the arrival of Homo erectus about 1.8 million years ago that the loss of biodiversity became problematic. As our ancient ancestors migrated out of Africa to distant lands, the rate of biodiversity loss accelerated even further. As McKee carefully documents in Chapter IV, the pattern of population growth and biodiversity loss took a major turn for the worse with the advent of agriculture some 10,000 years ago in what is now the Middle East. Chapter V introduces the reader to basic demographic concepts and principles. Using quantitative data...

Most of the Earth's biodiversity resides in the tropics. However, a comprehensive understanding of which factors control range limits of tropical species is still lacking. Climate is often thought to be the predominant range‐determining mechanism at large spatial scales. Alternatively, species’ ranges may be controlled by soil or other environmental factors, or by non‐environmental factors such as biotic interactions, dispersal barriers, intrinsic population dynamics, or time‐limited expansion from place of origin or past refugia. How species ranges are controlled is of key importance for predicting their responses to future global change. Here, we use a novel implementation of species distribution modelling (SDM) to assess the degree to which African continental‐scale species distributions in a keystone tropical group, the palms (Arecaceae), are controlled by climate, non‐climatic environmental factors, or non‐environmental spatial constraints. A comprehensive data set on African palm species occurrences was assembled and analysed using the SDM algorithm Maxent in combination with climatic and non‐climatic environmental predictors (habitat, human impact), as well as spatial eigenvector mapping (spatial filters). The best performing models always included spatial filters, suggesting that palm species distributions are always to some extent limited by non‐environmental constraints. Models which included climate provided significantly better predictions than models that included only non‐climatic environmental predictors, the latter having no discernible effect beyond the climatic control. Hence, at the continental scale, climate constitutes the only strong environmental control of palm species distributions in Africa. With regard to the most important climatic predictors of African palm distributions, water‐related factors were most important for 25 of the 29 species analysed. The strong response of palm distributions to climate in combination with the importance of non‐environmental spatial constraints suggests that African palms will be sensitive to future climate changes, but that their ability to track suitable climatic conditions will be spatially constrained.

The emergence of a novel infectious disease, chytridiomycosis, is now widely recognized as a major cause of amphibian declines and biodiversity loss across local and global scales. Amphibian mortalities caused by the pathogenic chytrid fungus, Batrachochytrium dendrobatidis (Bd) were first recorded in Iberia, Europe over a decade ago. In August 2009, hundreds of post‐metamorphic common midwife toads (Alytes obstetricans) were found dead in the water and margins of a pond in the Serra da Estrela Natural Park, north‐central Portugal. Histological and genetic analyses confirmed their infection with Bd. Given the likelihood of a new outbreak of chytridiomycosis, we evaluated the possible impacts of this disease on populations of A. obstetricans within the Park by conducting field surveys during 2010 and 2011. We compared the present distribution and abundance of A. obstetricans with historical records, and quantified the present prevalence and intensity of infection by Bd. Results showed that (1) A. obstetricans disappeared from 67% of the 1 × 1 km squares where it was recorded in the past, (2) breeding is currently limited to 16% of the confirmed breeding sites in the past, and that (3) larvae are now less abundant, as well as are highly infected by Bd in the remaining sites. These effects were most pronounced at altitudes above 1200 m. Our findings suggest that an outbreak of chytridiomycosis is responsible for the rapid decline of A. obstetricans in Serra da Estrela, and we believe that urgent conservation measures are needed to prevent local extinction of the species.

Chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal), has had an unprecedented impact on amphibian biodiversity. Although Bd is globally widespread, Bsal is currently spreading, increasing the probability that these pathogens will co-occur in individual amphibians. Interactions among coinfecting parasites can have significant outcomes on disease dynamics and impact and, therefore, may have important consequences for amphibian conservation. We analyzed the patterns of Bd-Bsal coinfections in two species of free-ranging urodeles during an outbreak of chytridiomycosis in Spain. Our goals were to assess 1) the probability of co-occurrence of both chytrid species and 2) the correlation of pathogen loads in coinfected hosts. We detected coinfections in 81.58% of Triturus marmoratus (n=38) and in 18.75% of Ichthyosaura alpestris (n=16). Histopathologic lesions of chytridiomycosis were observed only in T. marmoratus. Our results demonstrate a positive relationship between Bd and Bsal loads in T. marmoratus, whereas the co-occurrence analysis showed a random association among pathogens in both urodele species. Overall, we show that Bd-Bsal coinfections intensify pathogen load in T. marmoratus and could, therefore, increase disease severity and have important consequences for the conservation of some amphibian species.

Amphibian chytridiomycosis caused by Batrachochytrium dendrobatidis is reported in Uruguayan native amphibians for the first time. Histological evidence of infection was observed in tadpoles of Hypsiboas pulchellus, Odontophrynus maisuma, Physalaemus henselii, and Scinax squalirostris. The effects of chytridiomycosis on these species are still unknown. However, the disease is of potential concern for the conservation of the apparently declining species P. henselii and also for O. maisuma, given its restricted distribution in habitats which are being increasingly disturbed.

Introduction

Species that are tolerant of broad environmental gradients may be less vulnerable to epizootic outbreaks of disease. Chytridriomycosis, caused by the fungus Batrachochytrium dendrobatidis, has been linked to extirpations and extinctions of amphibian species in many regions. The pathogen thrives in cool, moist environments, and high amphibian mortality rates have commonly occurred during chytridiomycosis outbreaks in amphibian populations in high-elevation tropical rainforests. In Australia several high-elevation species, including the armored mist frog (Litoria lorica), which is designated as critically endangered by the International Union for the Conservation of Nature (IUCN), were believed to have gone extinct during chytridiomycosis outbreaks in the 1980s and early 1990s. Species with greater elevational ranges disappeared from higher elevations, but remained common in the lowlands. In June 2008, we surveyed a stream in a high-elevation dry sclerophyll forest and discovered a previously unknown population of L. lorica and a population of the waterfall frog (Litoria nannotis). We conducted 6 additional surveys in June 2008, September 2008, March 2009, and August 2009. Prevalences of B. dendrobatidis infection (number infected per total sampled) were consistently high in frogs (mean 82.5%, minimum 69%) of both species and in tadpoles (100%) during both winter (starting July) and summer (starting February). However, no individuals of either species showed clinical signs of disease, and they remained abundant (3.25 - 8.75 individuals of L. lorica and 6.5-12.5 individuals of L. nannotis found/person/100 m over 13 months). The high-elevation dry sclerophyll site had little canopy cover, low annual precipitation, and a more defined dry season than a nearby rainforest site, where L. nannotis was more negatively affected by chytridiomycosis. We hypothesize this lack of canopy cover allowed the rocks on which frogs perched to warm up, thereby slowing growth and reproduction of the pathogen on the hosts. In addition, we suggest surveys for apparently extinct or rare species should not be limited to core environments.

The pathogenic chytrid fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) cause infections that have become primary drivers of amphibian biodiversity loss. While globally widespread, the distribution margins of Bd and Bsal have not been determined, and the presence of these pathogens has probably gone unnoticed in many areas, especially in northern Eurasia. To better understand the presence and distribution of both pathogens in the northern temperate and boreal forest biomes, 243 individuals were sampled from 8 native amphibian species across Estonia. Additionally, 68 amphibians were sampled from captive collections in Estonia and Latvia. Pathogen infection was assessed using metabarcoding of the ITS2 marker. No positive matches for Bsal infection were found. Bd was detected in 13 specimens, 3 of which were sampled at the Riga Zoo (with a prevalence of 5.2%) and 10 in natural environments in Estonia (3.3%). The infected wild individuals belonged to 6 amphibian species and were detected throughout the mainland of Estonia, but not on islands. Prevalence of infection with Bd ranged between 3.1 and 12.5% among native species. In addition, we found molecular evidence for a potentially new sister species to Bd in nature. Although outbreaks of chytridiomycosis have never been observed in Estonia, it cannot be excluded that the dynamics of local amphibian populations are affected by Bd infections. Therefore, further work, including capture-mark-recapture studies and long-term monitoring, are required to clarify the impact of Bd on amphibians in Northern Europe.

Species are being lost at increasing rates due to anthropogenic effects, leading to the recognition that we are witnessing the onset of a sixth mass extinction. Emerging infectious disease has been shown to increase species loss and any attempts to reduce extinction rates need to squarely confront this challenge. Here, we develop a procedure for identifying amphibian species that are most at risk from the effects of chytridiomycosis by combining spatial analyses of key host life-history variables with the pathogen's predicted distribution. We apply our rule set to the known global diversity of amphibians in order to prioritize pecies that are most at risk of loss from disease emergence. This risk assessment shows where limited conservation funds are best deployed in order to prevent further loss of species by enabling ex situ amphibian salvage operations and focusing any potential disease mitigation projects.

One of the major causes of amphibian population decline is the deadly fungal pathogen Batrachochytrium dendrobatidis, Bd Research on pathogenesis and host immunity aims to inform development of targeted conservation interventions. Studies examining global host immune responses as well as effects on lymphocytes in vitro suggest that Bd infection causes immunosuppression. However, it is unknown which hematopoietic tissues are affected and if these effects differ among host species. We investigated the effect of experimental Bd infection on three diverse amphibian species by quantifying the amount of hematopoietic tissue in the spleen, bone marrow and kidney. Upon Bd infection, hematopoietic tissue in the kidney tended to be depleted, while the spleen appeared unaffected. The bone marrow in highly susceptible species was depleted, whereas an increase in hematopoietic tissue was observed in the more resistant species. Our study demonstrates that species and hematopoietic tissues behave differently in response to Bd infection, and may be related to the species' susceptibility to infection.

Amphibian population declines and sudden species' extinctions began to be noted at the beginning of the 1980s. Understanding the causes of the losses is hampered by our poor knowledge of the amphibian fauna in many parts of the world. Amphibian taxa are still being described at a high rate, especially in the tropics, which means that even quantifying species lost as a percentage of the current fauna can be a misleading statistic in some parts of the globe. The number of species that have gone missing is only one measure of the loss of biodiversity. Long-term studies of single-species populations are needed, but this approach has its limits. Amphibian populations often show great annual variation in population size making it difficult, if not impossible, to use short-term studies as a basis for deciding if a population is increasing or decreasing in the long term. Aggregating single studies into databases and searching for patterns of variation is a way of overcoming this limitation. Several databases on species and population time series are available or in development. These records show that declines are continuing worldwide with some species and populations, especially in the tropics and at higher elevations, at greater risk of extinction than others. Unfortunately, amphibian databases with population time series have much less information for the tropics compared to the temperate zone, and less for Africa and Asia compared with Europe and North America. Focusing limited resources using comprehensive statistical designs is a way to maximize the efficiency and effectiveness of monitoring efforts. It is clear that, in the first decades of the twenty-first century, the regions of the globe with the highest diversity of amphibian species will experience the greatest rates of decrease of forests and increase in human population size, fertilizer use, agricultural production, creation of new croplands and irrigation. Many of these changes are likely negatively to affect amphibian species diversity, and their influence must be understood before concluding, at least for amphibians, that the 2010 millennium assessment goal of significantly reversing the rate of loss of Earth's biodiversity can be met.

Emerging infectious diseases in wildlife are increasingly associated with animal mortality and species declines, but their source and genetic characterization often remains elusive. Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has been associated with catastrophic and well-documented amphibian population declines and extinctions at the global scale. We used histology and whole-genome sequencing to describe the lesions caused by, and the genetic variability of, two Bd isolates obtained from a mass mortality event in a captive population of the threatened Chilean giant frog (Calyptocephalella gayi). This was the first time an association between Bd and high mortality had been detected in this charismatic and declining frog species. Pathological examinations revealed that 30 dead metamorphosed frogs presented agnathia or brachygnathia, a condition that is reported for the first time in association with chytridiomycosis. Phylogenomic analyses revealed that Bd isolates (PA1 and PA2) from captive C. gayi group with other Bd isolates (AVS2, AVS4, and AVS7) forming a single highly supported Chilean Bd clade within the global panzootic lineage of Bd (BdGPL). These findings are important to inform the strengthening of biosecurity measures to prevent the impacts of chytridiomycosis in captive breeding programs elsewhere.

The fungal pathogen Batrachochytrium dendrobatidis (B. dendrobatidis) has emerged as a major agent of amphibian extinction, requiring conservation intervention for many susceptible species. Identifying susceptible species is challenging, but many aspects of species biology are predicted to influence the evolution of host resistance, tolerance, or avoidance strategies towards disease. In turn, we may expect species exhibiting these distinct strategies to differ in their ability to survive epizootic disease outbreaks. Here, we test for phylogenetic and trait‐based patterns of B. dendrobatidis infection risk and infection intensity among 302 amphibian species by compiling a global data set of B. dendrobatidis infection surveys across 95 sites. We then use best‐fit models that associate traits, taxonomy and environment with B. dendrobatidis infection risk and intensity to predict host disease mitigation strategies (tolerance, resistance, avoidance) for 122 Neotropical amphibian species that experienced epizootic B. dendrobatidis outbreaks, and noted species persistence or extinction from these events. Aspects of amphibian species life history, habitat use and climatic niche were consistently linked to variation in B. dendrobatidis infection patterns across sites around the world. However, predicted B. dendrobatidis infection risk and intensity based on site environment and species traits did not reveal a consistent pattern between the predicted host disease mitigation strategy and extinction outcome. This suggests that either tolerant or resistant species may have no advantage in ameliorating disease during epizootic events, or that other factors drive the persistence of amphibian populations during chytridiomycosis outbreaks. These results suggest that using a trait‐based approach may allow us to identify species with resistance or tolerance to endemic B. dendrobatidis infections, but that this approach may be insufficient to ultimately identify species at risk of extinction from epizootics.