Impact and Dynamics of Disease in Species Threatened by the Amphibian Chytrid Fungus, Batrachochytrium dendrobatidis

Abstract:  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.     

Historical Evidence of Widespread Chytrid Infection in North American Amphibian Populations

Abstract:  Emerging infectious diseases may be contributing to the global decline of amphibian populations. In particular, chytridiomycosis, a cutaneous fungal infection of amphibians caused by the chytrid Batrachochytrium dendrobatidis , gained attention in the 1990s as an apparently new pathogen. This fungus has been implicated as the causative agent of widespread mortalities among wild amphibians in geographically disparate parts of the world. To investigate the global distribution, historical occurrence, and infectiousness of this pathogen, we examined 3371 postmetamorphic and adult amphibians collected between 1895 and 2001 from 25 countries for the presence of chytrid fungi in the epidermis. Cutaneous chytrid infection was diagnosed in 383 of 2931 (13.1%) specimens of 12 common amphibian species from five Canadian provinces and seven American states, including 30 of 69 locations examined in the St. Lawrence River Valley of Québec. Chytrids were observed in 7.0% (46/655) of the adults collected in the 1960s, the earliest cases being two green frogs (  Rana clamitans ) collected in 1961 from Saint-Pierre-de-Wakefield, Québec. In recent studies, morbidity and mortality attributable to chytridiomycosis were not observed in infected amphibians from Québec despite a 17.8% (302/1698) prevalence of chytrid infection during the period 1990–2001. The prevalence of infection during this latter period was not statistically different when compared with the period 1960–1969. Epidermal chytrid infections were not observed in 440 amphibians examined from 23 other countries. In light of the fact that infection by B. dendrobatidis is widely distributed and apparently enzootic in seemingly healthy amphibians from eastern North America, lethal outbreaks of chytridiomycosis among amphibian populations appear to have complex causes and may be the result of underlying predisposing factors.     

Ecology of Chytridiomycosis in Rainforest Stream Frog Assemblages of Tropical Queensland

Abstract:  In the wet tropics of Queensland, Australia, eight species of stream-dwelling frogs have experienced population declines. Some declines were associated with an emerging infectious disease of amphibians (chytridiomycosis) caused by the fungus Batrachochytrium dendrobatidis. We examined the spatial and temporal pattern of infection prevalence in a sample of frog populations. Infected adults and tadpoles of all species were found, and infections occurred at every site. Infection prevalence varied among species and was always < 10.0% in adults but ranged from 0.75 to 76.0% in tadpoles. In this system tadpoles and adults of some species may act as disease reservoirs, experiencing avirulent infections, whereas other hosts (declining species) experience virulent infections. Infection prevalence was higher during the cool, dry winter season (May to September) and at high elevations (600–800 m), suggesting regulation by environmental conditions, including temperature and precipitation. We found no relationships between infection prevalence and mean body condition, fluctuating asymmetry of hind limbs, population density, or the presence of metamorphosing tadpoles and juvenile frogs. Although it is not certain whether chytridiomycosis was responsible for past frog population declines in the wet tropics of Queensland, the pathogen is now endemic. Our data indicate that at the landscape level, environmental conditions have strong effects on host-pathogen dynamics. These effects interact with species-specific behavior or immune function and may be important underlying determinants of chytridiomycosis epizootics and emergence.     

Effects of pond salinization on survival rate of amphibian hosts infected with the chytrid fungus

The chytrid fungus Batrachochytrium dendrobatidis has been implicated in the decline and extinction of amphibian populations worldwide, but management options are limited. Recent studies show that sodium chloride (NaCl) has fungicidal properties that reduce the mortality rates of infected hosts in captivity. We investigated whether similar results can be obtained by adding salt to water bodies in the field. We increased the salinity of 8 water bodies to 2 or 4 ppt and left an additional 4 water bodies with close to 0 ppt and monitored salinity for 18 months. Captively bred tadpoles of green and golden bell frog (Litoria aurea) were released into each water body and their development, levels of B. dendrobatidis infection, and survival were monitored at 1, 4, and 12 months. The effect of salt on the abundance of nontarget organisms was also investigated in before and after style analyses. Salinities remained constant over time with little intervention. Hosts in water bodies with 4 ppt salt had a significantly lower prevalence of chytrid infection and higher survival, following metamorphosis, than hosts in 0 ppt salt. Tadpoles in the 4 ppt group were smaller in length after 1 month in the release site than those in the 0 and 2 ppt groups, but after metamorphosis body size in all water bodies was similar . In water bodies with 4 ppt salt, the abundance of dwarf tree frogs (Litoria fallax), dragonfly larvae, and damselfly larvae was lower than in water bodies with 0 and 2 ppt salt, which could have knock‐on effects for community structure. Based on our results, salt may be an effective field‐based B. dendrobatidis mitigation tool for lentic amphibians that could contribute to the conservation of numerous susceptible species. However, as in all conservation efforts, these benefits need to be weighed against negative effects on both target and nontarget organisms.     

Reservoir‐host amplification of disease impact in an endangered amphibian

Emerging wildlife pathogens are an increasing threat to biodiversity. One of the most serious wildlife diseases is chytridiomycosis, caused by the fungal pathogen, Batrachochytrium dendrobatidis (Bd), which has been documented in over 500 amphibian species. Amphibians vary greatly in their susceptibility to Bd; some species tolerate infection, whereas others experience rapid mortality. Reservoir hosts—species that carry infection while maintaining high abundance but are rarely killed by disease—can increase extinction risk in highly susceptible, sympatric species. However, whether reservoir hosts amplify Bd in declining amphibian species has not been examined. We investigated the role of reservoir hosts in the decline of the threatened northern corroboree frog (Pseudophryne pengilleyi) in an amphibian community in southeastern Australia. In the laboratory, we characterized the response of a potential reservoir host, the (nondeclining) common eastern froglet (Crinia signifera), to Bd infection. In the field, we conducted frog abundance surveys and Bd sampling for both P. pengilleyi and C. signifera. We built multinomial logistic regression models to test whether Crinia signifera and environmental factors were associated with P. pengilleyi decline. C. signifera was a reservoir host for Bd. In the laboratory, many individuals maintained intense infections (>1000 zoospore equivalents) over 12 weeks without mortality, and 79% of individuals sampled in the wild also carried infections. The presence of C. signifera at a site was strongly associated with increased Bd prevalence in sympatric P. pengilleyi. Consistent with disease amplification by a reservoir host, P. pengilleyi declined at sites with high C. signifera abundance. Our results suggest that when reservoir hosts are present, population declines of susceptible species may continue long after the initial emergence of Bd, highlighting an urgent need to assess extinction risk in remnant populations of other declined amphibian species.     

The Novel and Endemic Pathogen Hypotheses: Competing Explanations for the Origin of Emerging Infectious Diseases of Wildlife

Abstract:  Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis , is an emerging infectious disease implicated in declines of amphibian populations around the globe. An emerging infectious disease is one that has recently been discovered; has recently increased in incidence, geography, or host range; or is newly evolved. For any given outbreak of an emerging disease, it is therefore possible to state two hypotheses regarding its origin. The novel pathogen hypothesis states that the disease has recently spread into new geographic areas, whereas the endemic pathogen hypothesis suggests that it has been present in the environment but recently has increased in host range or pathogenicity. Distinguishing between these hypotheses is important, because the conservation measures needed to slow or stop the spread of a novel pathogen are likely to differ from those needed to prevent outbreaks of an endemic pathogen. Population genetics may help discriminate among the possible origins of an emerging disease. Current evidence suggests chytridiomycosis may be a novel pathogen being spread worldwide by carriers; until we know how much genetic variation to expect in an endemic strain, however, we cannot yet conclude that B. dendrobatidis is a novel pathogen.     

Chytridiomycosis and Seasonal Mortality of Tropical Stream‐Associated Frogs 15 Years after Introduction of Batrachochytrium dendrobatidis

Assessing the effects of diseases on wildlife populations can be difficult in the absence of observed mortalities, but it is crucial for threat assessment and conservation. We performed an intensive capture‐mark‐recapture study across seasons and years to investigate the effect of chytridiomycosis on demographics in 2 populations of the threatened common mist frog (Litoria rheocola) in the lowland wet tropics of Queensland, Australia. Infection prevalence was the best predictor for apparent survival probability in adult males and varied widely with season (0–65%). Infection prevalence was highest in winter months when monthly survival probabilities were low (approximately 70%). Populations at both sites exhibited very low annual survival probabilities (12–15%) but high recruitment (71–91%), which resulted in population growth rates that fluctuated seasonally. Our results suggest that even in the absence of observed mortalities and continued declines, and despite host–pathogen co‐existence for multiple host generations over almost 2 decades, chytridiomycosis continues to have substantial seasonally fluctuating population‐level effects on amphibian survival, which necessitates increased recruitment for population persistence. Similarly infected populations may thus be under continued threat from chytridiomycosis which may render them vulnerable to other threatening processes, particularly those affecting recruitment success. Quitridiomicosis y Mortalidad Estacional de Ranas Asociadas a Arroyos Tropicales Quince Años Después de la Introducción de Batrachochytrium dendrobatidisvsp     

Batrachochytrium dendrobatidis and the Collapse of Anuran Species Richness and Abundance in the Upper Manu National Park,Southeastern Peru

Abstract: Amphibians are declining worldwide, but these declines have been particularly dramatic in tropical mountains, where high endemism and vulnerability to an introduced fungal pathogen, Batrachochytrium dendrobatidis (Bd), is associated with amphibian extinctions. We surveyed frogs in the Peruvian Andes in montane forests along a steep elevational gradient (1200–3700 m). We used visual encounter surveys to sample stream‐dwelling and arboreal species and leaf‐litter plots to sample terrestrial‐breeding species. We compared species richness and abundance among the wet seasons of 1999, 2008, and 2009. Despite similar sampling effort among years, the number of species (46 in 1999) declined by 47% between 1999 and 2008 and by 38% between 1999 and 2009. When we combined the number of species we found in 2008 and 2009, the decline from 1999 was 36%. Declines of stream‐dwelling and arboreal species (a reduction in species richness of 55%) were much greater than declines of terrestrial‐breeding species (reduction of 20% in 2008 and 24% in 2009). Similarly, abundances of stream‐dwelling and arboreal frogs were lower in the combined 2008–2009 period than in 1999, whereas densities of frogs in leaf‐litter plots did not differ among survey years. These declines may be associated with the infection of frogs with Bd. B. dendrobatidis prevalence correlated significantly with the proportion of species that were absent from the 2008 and 2009 surveys along the elevational gradient. Our results suggest Bd may have arrived at the site between 1999 and 2007, which is consistent with the hypothesis that this pathogen is spreading in epidemic waves along the Andean cordilleras. Our results also indicate a rapid decline of frog species richness and abundance in our study area, a national park that contains many endemic amphibian species and is high in amphibian species richness.     

Effects of Amphibian Chytrid Fungus on Individual Survival Probability in Wild Boreal Toads

Abstract: Chytridiomycosis is linked to the worldwide decline of amphibians, yet little is known about the demographic effects of the disease. We collected capture–recapture data on three populations of boreal toads (Bufo boreas [Bufo = Anaxyrus]) in the Rocky Mountains (U.S.A.). Two of the populations were infected with chytridiomycosis and one was not. We examined the effect of the presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]; the agent of chytridiomycosis) on survival probability and population growth rate. Toads that were infected with Bd had lower average annual survival probability than uninfected individuals at sites where Bd was detected, which suggests chytridiomycosis may reduce survival by 31–42% in wild boreal toads. Toads that were negative for Bd at infected sites had survival probabilities comparable to toads at the uninfected site. Evidence that environmental covariates (particularly cold temperatures during the breeding season) influenced toad survival was weak. The number of individuals in diseased populations declined by 5–7%/year over the 6 years of the study, whereas the uninfected population had comparatively stable population growth. Our data suggest that the presence of Bd in these toad populations is not causing rapid population declines. Rather, chytridiomycosis appears to be functioning as a low‐level, chronic disease whereby some infected individuals survive but the overall population effects are still negative. Our results show that some amphibian populations may be coexisting with Bd and highlight the importance of quantitative assessments of survival in diseased animal populations.     

Interventions for Reducing Extinction Risk in Chytridiomycosis‐Threatened Amphibians

Wildlife diseases pose an increasing threat to biodiversity and are a major management challenge. A striking example of this threat is the emergence of chytridiomycosis. Despite diagnosis of chytridiomycosis as an important driver of global amphibian declines 15 years ago, researchers have yet to devise effective large‐scale management responses other than biosecurity measures to mitigate disease spread and the establishment of disease‐free captive assurance colonies prior to or during disease outbreaks. We examined the development of management actions that can be implemented after an epidemic in surviving populations. We developed a conceptual framework with clear interventions to guide experimental management and applied research so that further extinctions of amphibian species threatened by chytridiomycosis might be prevented. Within our framework, there are 2 management approaches: reducing Batrachochytrium dendrobatidis (the fungus that causes chytridiomycosis) in the environment or on amphibians and increasing the capacity of populations to persist despite increased mortality from disease. The latter approach emphasizes that mitigation does not necessarily need to focus on reducing disease‐associated mortality. We propose promising management actions that can be implemented and tested based on current knowledge and that include habitat manipulation, antifungal treatments, animal translocation, bioaugmentation, head starting, and selection for resistance. Case studies where these strategies are being implemented will demonstrate their potential to save critically endangered species. Intervenciones para Reducir el Riesgo de Extinción en Anfibios Amenazados por la Quitridiomicosis     

Assessing Risk and Guidance on Monitoring of Batrachochytrium dendrobatidis in Europe through Identification of Taxonomic Selectivity of Infection

Amphibians are globally threatened, but not all species are affected equally by different threatening processes. This is true for the threat posed by the chytridiomycete fungus (Batrachochytrium dendrobatidis). We compiled a European data set for B. dendrobatidis to analyze the trends of infection in European amphibians. The risk of infection was not randomly distributed geographically or taxonomically across Europe. Within countries with different prevalence, infection was nonrandom in certain amphibian taxa. Brown frogs of the genus Rana were unlikely to be infected, whereas frogs in the families Alytidae and Bombinatoridae were significantly more likely to be infected than predicted by chance. Frogs in the 2 families susceptible to B. dendrobatidis should form the core of attempts to develop spatial surveillance studies of chytridiomycosis in Europe. Ideally, surveys for B. dendrobatidis should be augmented by sampling the widespread genus Pelophylax because this taxon exhibits geographically inconsistent overinfection with B. dendrobatidis and surveillance of it may facilitate recognition of factors causing spatial variability of infection intensity. Several European amphibian taxa were not represented in our data set; however, surveillance of unsampled species should also occur when warranted. Evaluación de Riesgo y Orientación para el Monitoreo de Batrachochytrium dendrobatidis en Europa Mediante la Identificación de la Selectividad Taxonómica de la Infección     

Emerging infectious disease as a proximate cause of amphibian mass mortality

A newly discovered infectious disease of amphibians, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, is implicated in population declines and possible extinctions throughout the world. The purpose of our study was to examine the effects of B. dendrobatidis on the mountain yellow-legged frog (Rana muscosa) in the Sierra Nevada of California (USA). We (1) quantified the prevalence and incidence of B. dendrobatidis through repeat surveys of several hundred R. muscosa populations in the southern Sierra Nevada; (2) described the population-level effects of B. dendrobatidis on R. muscosa population abundance; and (3) compared the mortality rates of infected and uninfected R. muscosa individuals from pre- through post-metamorphosis using both laboratory and field experiments. Mouthpart inspections conducted in 144 and 132 R. muscosa populations in 2003 and 2004, respectively, indicated that 19% of R. muscosa populations in both years showed indications of chytridiomycosis. Sixteen percent of populations that were uninfected in 2003 became infected by 2004. Rana muscosa population sizes were reduced by an average of 88% following B. dendrobatidis outbreaks at six sites, but at seven B. dendrobatidis-negative sites, R. muscosa population sizes increased by an average of 45% over the same time period. In the laboratory, all infected R. muscosa developed fatal chytridiomycosis after metamorphosis, while all uninfected individuals remained healthy. In the field experiment in which R. muscosa tadpoles were caged at infected and uninfected sites, 96% of the individuals that metamorphosed at infected sites died vs. 5% at the uninfected sites. These studies indicate that chytridiomycosis causes high mortality in post-metamorphic R. muscosa, that this emerging disease is the proximate cause of numerous observed R. muscosa population declines, and that the disease threatens this species with extirpation at numerous sites in California's Sierra Nevada.     

Interspecific Variation in Susceptibility of Frog Tadpoles to the Pathogenic Fungus Batrachochytrium dendrobatidis

Abstract:  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, and the introduction of non-native species and diseases. Several types of pathogens have been implicated in contributing to amphibian population declines: viruses, bacteria, oomycetes, and fungi. One particular fungus, the chytridiomycete Batrachochytrium dendrobatidis may have caused amphibian population declines in several regions. This pathogen causes chytridiomycosis, which is fatal to newly metamorphic and adult amphibians of certain species. We present experimental evidence that larval stages may also be susceptible to exposure to Batrachochytrium . There was, however, differential sensitivity to B. dendrobatidis in larvae we examined. In laboratory experiments, larval western toads (  Bufo boreas ) exposed to B. dendrobatidis experienced increased mortality and behaviors that suggested they were affected by exposure compared with unexposed control tadpoles. Larvae of Cascades frogs (  Rana cascadae ), bullfrogs ( R. catesbeiana ), and Pacific treefrogs ( Hyla regilla ) did not die after exposure to Batrachochytrium and appeared to behave normally. R. cascadae larvae exposed to B. dendrobatidis , however, showed an increase incidence in mouthpart abnormalities, a characteristic effect of chytridiomycosis, compared with unexposed controls. These results show that Batrachochytrium can negatively affect some species of amphibians at the larval stage and not others. The implications of interspecific variation in susceptibility to fungal infection are broad.     

Inconclusiveness of Chytridiomycosis as the Agent in Widespread Frog Declines

Abstract:  Although there is considerable evidence to support the hypothesis that the chytrid fungus Batrachochytrium dendrobatidis is the primary agent responsible for widespread declines in amphibian populations, particularly rainforest frog populations in Australia and Central America, I argue the case has not yet been made conclusively. Few specimens were collected at the time of population declines, so it may never be possible to conclusively determine their cause. It remains unclear whether the pathogen is novel where declines have occurred. Although it is not necessary that the infection be novel for it to be implicated in declines, if a preexisting pathogen has only recently caused extinctions, cofactors must be important. Whether the pattern of outbreaks represents a "wave" of extinctions is unclear, but if it does, the rate of spread in Australia is implausibly high for a waterborne pathogen, given the most likely estimates of epidemiological parameters. Although B. dendrobatidis is an amphibian pathogen according to Koch's postulates, the postulates are neither necessary nor sufficient criteria to identify a pathogen. The following key pieces of information are necessary to better understand the impact of this fungus on frog communities: better knowledge of the means and rate of transmission under field conditions, prevalence of infection among frog populations, as distinct from morbid individuals, and the effect of the fungus on frogs in the wild. It is crucial to determine whether there are strains of the fungus with differing pathogenicity to particular frog species and whether host-pathogen coevolution has occurred or is occurring. Recently developed diagnostic tools bring into reach the possibility of addressing these questions and thus developing appropriate strategies to manage frog communities that may be affected by this fungus.     

Varying responses of northeastern North American amphibians to the chytrid pathogen Batrachochytrium dendrobatidis

Chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd), is widespread among amphibians in northeastern North America. It is unknown, however, whether Bd has the potential to cause extensive amphibian mortalities in northeastern North America as have occurred elsewhere. In the laboratory, we exposed seven common northeastern North American amphibian species to Bd to assess the likelihood of population-level effects from the disease. We exposed larval wood frogs (Lithobates sylvaticus) and postmetamorphic frogs of six other species to two different strains of Bd, a northeastern strain (JEL404) and a strain that caused die-offs of amphibians in Panama (JEL423), under ideal in vitro growth conditions for Bd. Exposed American toads (Anaxyrus americanus) all died; thus, this species may be the most likely to die from Bd-caused disease in the wild. Both Bd strains were associated with mortalities of wood frogs, although half the metamorphs survived. The Bd strain from Panama killed metamorphic green frogs (L. clamitans), whereas the northeastern strain did not, which means novel strains of Bd may lead to death even when local strains may not. No mortality was observed in four species (bullfrogs [L. catesbeianus], northern leopard frogs [L. pipiens], spring peepers [Pseudacris crucifer], and blue-spotted salamanders [Ambystoma laterale]) and in some individuals of green frogs and wood frogs that we exposed. This finding suggests these six species may be Bd vectors. Our results show that systematic exposures of amphibian species to Bd in the laboratory may be a good first step in the identification of species susceptible to Bd-caused declines and in directing regional conservation efforts aimed at susceptible species.     

Amphibian Commerce as a Likely Source of Pathogen Pollution

Abstract: The commercial trade of wildlife occurs on a global scale. In addition to removing animals from their native populations, this trade may lead to the release and subsequent introduction of nonindigenous species and the pathogens they carry. Emerging infectious diseases, such as chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), and ranaviral disease have spread with global trade in amphibians and are linked to amphibian declines and die‐offs worldwide, which suggests that the commercial trade in amphibians may be a source of pathogen pollution. We screened tiger salamanders involved in the bait trade in the western United States for both ranaviruses and Bd with polymerase chain reaction and used oral reports from bait shops and ranavirus DNA sequences from infected bait salamanders to determine how these animals and their pathogens are moved geographically by commerce. In addition, we conducted 2 surveys of anglers to determine how often tiger salamanders are used as bait and how often they are released into fishing waters by anglers, and organized bait‐shop surveys to determine whether tiger salamanders are released back into the wild after being housed in bait shops. Ranaviruses were detected in the tiger salamander bait trade in Arizona, Colorado, and New Mexico, and Bd was detected in Arizona bait shops. Ranaviruses were spread geographically through the bait trade. All tiger salamanders in the bait trade were collected from the wild, and in general they moved east to west and north to south, bringing with them their multiple ranavirus strains. Finally, 26–73% of anglers used tiger salamanders as fishing bait, 26–67% of anglers released tiger salamanders bought as bait into fishing waters, and 4% of bait shops released tiger salamanders back into the wild after they were housed in shops with infected animals. The tiger salamander bait trade in the western United States is a useful model for understanding the consequences of the unregulated anthropogenic movement of amphibians and their pathogens through trade.     

Selecting for Tolerance against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation

Abstract: Some species have insufficient defenses against climate change, emerging infectious diseases, and non‐native species because they have not been exposed to these factors over their evolutionary history, and this can decrease their likelihood of persistence. Captive breeding programs are sometimes used to reintroduce individuals back into the wild; however, successful captive breeding and reintroduction can be difficult because species or populations often cannot coexist with non‐native pathogens and herbivores without artificial selection. In captive breeding programs, breeders can select for host defenses that prevent or reduce pathogen or herbivore burden (i.e., resistance) or traits that limit the effects of parasitism or herbivory on host fitness (i.e., tolerance). We propose that selection for host tolerance may enhance the success of reintroduction or translocation because tolerant hosts generally have neutral effects on introduced pathogens and herbivores. The release of resistant hosts would have detrimental effects on their natural enemies, promoting rapid evolution to circumvent the host resistance that may reduce the long‐term probability of persistence of the reintroduced or translocated species. We examined 2 case studies, one on the pathogenic amphibian chytrid fungus ( Batrachochytrium dendrobatidis [Bd]) and the other on the herbivorous cactus moth ( Cactoblastis cactorum) in the United States, where it is not native. In each case study, we provide recommendations for how captive breeders and managers could go about selecting for host tolerance. Selecting for tolerance may offer a promising tool to rescue hosts species from invasive natural enemies as well as new natural enemies associated with climate change‐induced range shifts.     

Using a Bayesian network to clarify areas requiring research in a host–pathogen system

Bayesian network analyses can be used to interactively change the strength of effect of variables in a model to explore complex relationships in new ways. In doing so, they allow one to identify influential nodes that are not well studied empirically so that future research can be prioritized. We identified relationships in host and pathogen biology to examine disease‐driven declines of amphibians associated with amphibian chytrid fungus (Batrachochytrium dendrobatidis). We constructed a Bayesian network consisting of behavioral, genetic, physiological, and environmental variables that influence disease and used them to predict host population trends. We varied the impacts of specific variables in the model to reveal factors with the most influence on host population trend. The behavior of the nodes (the way in which the variables probabilistically responded to changes in states of the parents, which are the nodes or variables that directly influenced them in the graphical model) was consistent with published results. The frog population had a 49% probability of decline when all states were set at their original values, and this probability increased when body temperatures were cold, the immune system was not suppressing infection, and the ambient environment was conducive to growth of B. dendrobatidis. These findings suggest the construction of our model reflected the complex relationships characteristic of host–pathogen interactions. Changes to climatic variables alone did not strongly influence the probability of population decline, which suggests that climate interacts with other factors such as the capacity of the frog immune system to suppress disease. Changes to the adaptive immune system and disease reservoirs had a large effect on the population trend, but there was little empirical information available for model construction. Our model inputs can be used as a base to examine other systems, and our results show that such analyses are useful tools for reviewing existing literature, identifying links poorly supported by evidence, and understanding complexities in emerging infectious‐disease systems.     

Differential Host Susceptibility to Batrachochytrium dendrobatidis,an Emerging Amphibian Pathogen

Abstract: The amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd) has received considerable attention due to its role in amphibian population declines worldwide. Although many amphibian species appear to be affected by Bd, there is little information on species‐specific differences in susceptibility to this pathogen. We used a comparative experimental approach to examine Bd susceptibility in 6 amphibian species from the United States. We exposed postmetamorphic animals to Bd for 30 days and monitored mortality, feeding rates, and infection levels. In all species tested, Bd‐exposed animals had higher rates of mortality than unexposed (control) animals. However, we found differences in mortality rates among species even though the amount of Bd detected on the different species’ bodies did not differ. Of the species tested, southern toads (Anaxyrus terrestris) and wood frogs (Lithobates sylvaticus) had the highest rates of Bd‐related mortality. Within species, we detected lower levels of Bd on individuals that survived longer and found that the relationship between body size and infection levels differed among species. Our results indicate that, even under identical conditions, amphibian species differ in susceptibility to Bd. This study represents a step toward identifying and understanding species variation in disease susceptibility, which can be used to optimize conservation strategies.     

Testing wetland features to increase amphibian reproductive success and species richness for mitigation and restoration

Aquatic habitat features can directly influence the abundance, species richness, and quality of juvenile amphibians recruited into adult populations. We examined the influences of within-wetland slope, vegetation, and stocked mosquito fish (Gambusia affinis) on amphibian metamorph production and species richness during the first two years post-construction at 18 experimental wetlands in northeast Missouri (U.S.A.) grasslands. We used an information theoretic approach (AICc) to rank regression models representing total amphibian metamorph production, individual amphibian species metamorph production, and larval amphibian species richness. Total amphibian metamorph production was greatest at shallow-sloped, fish-free wetlands during the first year, but shallow-sloped wetlands with high vegetation cover were best the second year. Species richness was negatively associated with fish and positively associated with vegetation in both survey years. Leopard frog (Rana blairi/sphenocephala complex) metamorph quality, based on average metamorph size, was influenced by slope and the number of cohorts in the wetland. However, the tested variables had little influence on the size of American toads (Bufo americanus) or boreal chorus frogs (Pseudacris maculata). Our results indicate that wetlands designed to act as functional reproductive habitat for amphibians should incorporate shallows, high amounts of planted or naturally established vegetation cover, and should be fish-free.