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.     

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.     

Multiple stressors and amphibian declines: dual impacts of pesticides and fish on yellow-legged frogs.

More than 40% of Earth's 5700+ amphibian species have undergone recent declines. Despite the likely involvement of multiple factors in driving these declines, most studies continue to focus on single stressors. In California (USA), separate studies have implicated either introduced fish or pesticides as causal agents. To date, however, no study has simultaneously evaluated the respective roles of these two potential stressors nor attempted to assess their relative importance, information critical for the development of effective conservation efforts and environmental policies. We examined the role and relative effect of fish and pesticides on the mountain yellow-legged frog (Rana muscosa) using unusually detailed data sets for a large portion of R. muscosa's historic range in California's Sierra Nevada. Habitat characteristics and presence/absence of R. muscosa and fish were quantified at each of 6831 sites during field surveys. Pesticide use upwind of each site was calculated from pesticide application records and predominant wind directions. Using generalized additive models, we found that, after accounting for habitat effects, the probability of R. muscosa presence was significantly reduced by both fish and pesticides, with the landscape-scale effect of pesticides much stronger than that of fish. The degree to which a site was sheltered from the predominant wind (and associated pesticides) was also a significant predictor of R. muscosa presence. Taken together, these results represent the strongest evidence to date that windborne pesticides are contributing to amphibian declines in pristine locations. Our results suggest that amphibian declines may have complex multi-factorial causes, and caution that single-factor studies that demonstrate the importance of one factor should not be used as evidence against the importance of other 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.     

Environmental refuge from disease-driven amphibian extinction

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.     

Introduced trout sever trophic connections in watersheds: consequences for a declining amphibian

Trophic linkages between terrestrial and aquatic ecosystems are increasingly recognized as important yet poorly known features of food webs. Here we describe research to understand the dynamics of lake food webs in relation to a native riparian amphibian and its interaction with introduced trout. The mountain yellow-legged frog Rana muscosa is endemic to alpine watersheds of the Sierra Nevada Mountains and the Transverse Ranges of California, but it has declined to a small fraction of its historical distribution and abundance. Although remaining frogs and introduced trout feed in different habitats of alpine lakes, our stable-isotope analyses clearly show that the same resource base of benthic invertebrates sustains their growth. During one period, insect emergence from naturally fishless lakes was nearly 20-fold higher compared to adjacent lakes with trout, showing that fish reduce availability of aquatic prey to amphibious and terrestrial consumers. Although trout cannot prey on adult frogs due to gape limitation, foraging post-metamorphic frogs are 10 times more abundant in the absence of trout, suggesting an important role for competition for prey by trout in highly unproductive alpine watersheds. Most Sierran lakes contain fish, and those that do not are usually small isolated ponds; in our study, these two lake types supported the lowest densities of post-metamorphic frogs, and these frogs were less reliant on local, benthic sources of productivity. Since Rana muscosa was formerly the most abundant vertebrate in the Sierra Nevada, the reduction in energy flow from lake benthos to this consumer due to fish introductions may have had negative consequences for its numerous terrestrial predators, many of which have also declined. We suggest that disruptions of trophic connections between aquatic and terrestrial food webs are an important but poorly understood consequence of fish introduction to many thousands of montane lakes and streams worldwide and may contribute to declines of native consumers in riparian habitats.     

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.     

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     

Non-Native Fish Introductions and the Decline of the Mountain Yellow-Legged Frog from within Protected Areas

Abstract: One of the most puzzling aspects of the worldwide decline of amphibians is their disappearance from within protected areas. Because these areas are ostensibly undisturbed, habitat alterations are generally perceived as unlikely causes. The introduction of non-native fishes into protected areas, however, is a common practice throughout the world and may exert an important influence on amphibian distributions. We quantified the role of introduced fishes (several species of trout) in the decline of the mountain yellow-legged frog (   Rana muscosa ) in California's Sierra Nevada through surveys openface> 1700 sites in two adjacent and historically fishless protected areas that differed primarily in the distribution of introduced fish. Negative effects of fishes on the distribution of frogs were evident at three spatial scales. At the landscape scale, comparisons between the two protected areas indicated that fish distribution was strongly negatively correlated with the distribution of frogs. At the watershed scale, the percentage of total water-body surface area occupied by fishes was a highly significant predictor of the percentage of total water-body surface area occupied by frogs. At the scale of individual water bodies, frogs were three times more likely to be found and six times more abundant in fishless than in fish-containing waterbodies, after habitat effects were accounted for. The strong effect of introduced fishes on mountain yellow-legged frogs appears to result from the unique life history of this amphibian which frequently restricts larvae to deeper water bodies, the same habitats into which fishes have most frequently been introduced. Because fish populations in at least some Sierra Nevada lakes can be removed with minimal effort, our results suggest that the decline of the mountain yellow-legged frog might be relatively easy to reverse.     

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     

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.     

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.     

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.     

Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies <Emphasis Type="Italic">Poecilia reticulata</Emphasis>

Understanding how individuals modify their social interactions in response to infectious disease is of central importance for our comprehension of how disease dynamics operate in real-world populations. Whilst a significant amount of theoretical work has modelled disease transmission using network models, we have comparatively little understanding of how infectious disease impacts on the social behaviour of individuals and how these effects scale up to the level of the population. We experimentally manipulated the parasite load of female guppies (Poecilia reticulata) and introduced fish either infected with the ectoparasites Gyrodactylus spp. (experimental) or uninfected (control) into replicated semi-natural populations of eight size-matched female guppies. We quantified the behaviour and social associations of both the introduced fish and the population fish. We found that infected experimental fish spent less time associating with the population fish than the uninfected control fish. Using information on which fish initiated shoal fission (splitting) events, our results demonstrate that the population fish actively avoided infected experimental fish. We also found that the presence of an infected individual resulted in a continued decline in social network clustering up to at least 24 h after the introduction of the infected fish, whereas in the control treatment, the clustering coefficient showed an increase at this time point. These results demonstrate that the presence of a disease has implications for both the social associations of infected individuals and for the social network structure of the population, which we predict will have consequences for infectious disease transmission.     

Ambient Ultraviolet B Radiation and Prevalence of Infection by Batrachochytrium dendrobatidis in Two Amphibian Species

Abstract: Chytridiomycosis, the emerging disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd) is responsible for declines and extirpations of amphibian populations worldwide. Environmental covariates modify the host‐Bd interaction and thus affect the ongoing spread of the pathogen. One such covariate may be the intensity of ultraviolet B (UV‐B) radiation. In a field experiment conducted in Laguna Grande de Peñalara (central Spain), a mountainous region where the presence of Bd has been documented since 1997, we analyzed the potential effect of environmental UV‐B (daily maximum 2.5–3.9 W/m²) on the susceptibility of larvae of the common toad (Bufo bufo) to Bd. The proportion of infected individuals increased as tadpoles developed. The prevalence of Bd was significantly lower in tadpoles exposed to environmental UV‐B intensities (2.94%) than in tadpoles not exposed to the radiation (9.72%). This finding mirrors that seen for a second amphibian species, the European midwife toad (Alytes obstetricans), for which conditional prevalence (i.e., prevalence of infection conditioned on the probability of a site being infected) across the Iberian Peninsula was inversely correlated with the intensity of UV‐B.     

Simulated potential effects of ecological factors on a hypothetical population of Chiricahua leopard frog (Rana chiricahuensis)

Simulations provide an opportunity to examine how single or multiple perturbations may impact a specific species. The objectives of this study were to identify thresholds at which changes in stream peak flow, stream base flow, and/or chytrid fungus presence alter long-term Rana chiricahuensis populations. We used scenarios with varying peak flow mortality rates, base flow mortality rates, and chytrid fungus mortality rates. Sensitivity analysis was also conducted. Over 50 years, populations in six scenarios increased and 13 scenarios decreased. Eight scenarios resulting with fewer than 100 individuals included stochastic effects for at least two of three perturbations and the remaining scenarios included chronic effects of 30% or higher. Scenarios with population increases had either no chytrid fungus effect or chronic effects from perturbations totaling less than 30%. In the absence of chytrid fungus, populations increased and became stable. At a 10% annual death rate caused by chytrid fungus, the R. chiricahuensis population decreased 46.8%. At a 20% death rate, the population decreased 98.6%. Model scenarios were sensitive to peak flow death rates. As peak flow mortality increased to 10 and 20%, extinction rates increased to 91.7 and 99.9%, respectively. With model parameters and the no base flow mortality, R. chiricahuensis populations declined by 92% with a 3.2% extinction rate at 50 years. Models with base flow mortality rates of 10 and 20% resulted in population extinction rates of 48.7 and 96.1%, respectively. Scenario analysis of perturbations on a hypothetical R. chiricahuensis population provided a framework in which to view combined effects on a species. Analysis supports supposition that chytrid fungus is the proximate cause of many amphibian declines, but the added effect of base flow and peak flow has the potential to hasten declines.     

Citation Rate and Perceived Subject Bias in the Amphibian‐Decline Literature

Abstract: As a result of global declines in amphibian populations, interest in the conservation of amphibians has grown. This growth has been fueled partially by the recent discovery of other potential causes of declines, including chytridiomycosis (the amphibian chytrid, an infectious disease) and climate change. It has been proposed that researchers have shifted their focus to these novel stressors and that other threats to amphibians, such as habitat loss, are not being studied in proportion to their potential effects. We tested the validity of this proposal by reviewing the literature on amphibian declines, categorizing the primary topic of articles within this literature (e.g., habitat loss or UV‐B radiation) and comparing citation rates among articles on these topics and impact factors of journals in which the articles were published. From 1990 to 2009, the proportion of papers on habitat loss remained fairly constant, and although the number of papers on chytridiomycosis increased after the disease was described in 1998, the number of published papers on amphibian declines also increased. Nevertheless, papers on chytridiomycosis were more highly cited than papers not on chytridiomycosis and were published in journals with higher impact factors on average, which may indicate this research topic is more popular in the literature. Our results were not consistent with a shift in the research agenda on amphibians. We believe the perception of such a shift has been supported by the higher citation rates of papers on chytridiomycosis.     

Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.     

Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep

Evidence of inbreeding depression is commonly detected from the fitness traits of animals, yet its effects on population growth rates of endangered species are rarely assessed. We examined whether inbreeding depression was affecting Sierra Nevada bighorn sheep (Ovis canadensis sierrae), a subspecies listed as endangered under the U.S. Endangered Species Act. Our objectives were to characterize genetic variation in this subspecies; test whether inbreeding depression affects bighorn sheep vital rates (adult survival and female fecundity); evaluate whether inbreeding depression may limit subspecies recovery; and examine the potential for genetic management to increase population growth rates. Genetic variation in 4 populations of Sierra Nevada bighorn sheep was among the lowest reported for any wild bighorn sheep population, and our results suggest that inbreeding depression has reduced adult female fecundity. Despite this population sizes and growth rates predicted from matrix-based projection models demonstrated that inbreeding depression would not substantially inhibit the recovery of Sierra Nevada bighorn sheep populations in the next approximately 8 bighorn sheep generations (48 years). Furthermore, simulations of genetic rescue within the subspecies did not suggest that such activities would appreciably increase population sizes or growth rates during the period we modeled (10 bighorn sheep generations, 60 years). Only simulations that augmented the Mono Basin population with genetic variation from other subspecies, which is not currently a management option, predicted significant increases in population size. Although we recommend that recovery activities should minimize future losses of genetic variation, genetic effects within these endangered populations-either negative (inbreeding depression) or positive (within subspecies genetic rescue)-appear unlikely to dramatically compromise or stimulate short-term conservation efforts. The distinction between detecting the effects of inbreeding depression on a component vital rate (e.g., fecundity) and the effects of inbreeding depression on population growth underscores the importance of quantifying inbreeding costs relative to population dynamics to effectively manage endangered populations.