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.     

Environmental Determinants of Recent Endemism of Batrachochytrium dendrobatidis Infections in Amphibian Assemblages in the Absence of Disease Outbreaks

The inconsistent distribution of large‐scale infection mediated die‐offs and the subsequent population declines of several animal species, urges us to understand how, when, and why species are affected by disease. It is often unclear when or under what conditions a pathogen constitutes a threat to a host. Often, variation of environmental conditions plays a role. Globally Batrachochytrium dendrobatidis (Bd) causes amphibian declines; however, host responses are inconsistent and this fungus appears equally capable of reaching a state of endemism and subsequent co‐existence with native amphibian assemblages. We sought to identify environmental and temporal factors that facilitate host–pathogen coexistence in northern Europe. To do this, we used molecular diagnostics to examine archived and wild amphibians for infection and general linear mixed models to explore relationships between environmental variables and prevalence of infection in 5 well‐sampled amphibian species. We first detected infection in archived animals collected in 1999, and infection was ubiquitous, but rare, throughout the study period (2008–2010). Prevalence of infection exhibited significant annual fluctuations. Despite extremely rare cases of lethal chytridiomycosis in A. obstetricans, Bd prevalence was uncorrelated with this species’ population growth. Our results suggest context dependent and species‐specific host susceptibility. Thus, we believe recent endemism of Bd coincides with environmentally driven Bd prevalence fluctuations that preclude the build‐up of Bd infection beyond the critical threshold for large‐scale mortality and host population crashes. Determinantes Ambientales del Endemismo Reciente de Infecciones de Batrachochytrium dendrobatidis en Conjuntos de Anfibios en Ausencia de Brotes de Enfermedades Spitzen et al.     

Differences in sensitivity to the fungal pathogen Batrachochytrium dendrobatidis among amphibian populations

Contributing to the worldwide biodiversity crisis are emerging infectious diseases, which can lead to extirpations and extinctions of hosts. For example, the infectious fungal pathogen Batrachochytrium dendrobatidis (Bd) is associated with worldwide amphibian population declines and extinctions. Sensitivity to Bd varies with species, season, and life stage. However, there is little information on whether sensitivity to Bd differs among populations, which is essential for understanding Bd‐infection dynamics and for formulating conservation strategies. We experimentally investigated intraspecific differences in host sensitivity to Bd across 10 populations of wood frogs (Lithobates sylvaticus) raised from eggs to metamorphosis. We exposed the post‐metamorphic wood frogs to Bd and monitored survival for 30 days under controlled laboratory conditions. Populations differed in overall survival and mortality rate. Infection load also differed among populations but was not correlated with population differences in risk of mortality. Such population‐level variation in sensitivity to Bd may result in reservoir populations that may be a source for the transmission of Bd to other sensitive populations or species. Alternatively, remnant populations that are less sensitive to Bd could serve as sources for recolonization after epidemic events.     

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.     

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.     

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 chytrid fungus and a glyphosate-based herbicide on survival and growth of wood frogs (Lithobates sylvaticus)

Anthropogenic-derived stressors in the environment, such as contaminants, are increasingly considered important cofactors that may decrease the immune response of amphibians to pathogens. Few studies, however, have integrated amphibian disease and contaminants to test this multiple-stressor hypothesis for amphibian declines. We examined whether exposure to sublethal concentrations of a glyphosate-based herbicide and two strains of the pathogenic chytrid fungus, Batrachochrytrium dendrobatidis (Bd) could: (1) sublethally affect wood frogs (Lithobates sylvaticus) by altering the time to and size at metamorphosis, and (2) directly affect survivability of wood frogs after metamorphosis. Neither Bd strain nor herbicide exposure alone significantly altered growth or time to metamorphosis. The two Bd strains did not differ in their pathogenicity, and both caused mortality in post-metamorphic wood frogs. There was no evidence of an interaction between treatments, indicating a lack of herbicide-induced susceptibility to Bd. However, the trends in our data suggest that exposure of wood frogs to a high concentration of glyphosate-based herbicide may reduce Bd-caused mortality compared to animals exposed to Bd alone. These results exemplify the complexities inherent when populations are coping with multiple stressors. In this case, the perceived stressor, glyphosate-based herbicide, appeared to affect the pathogen more than the host's immune system, relieving the host from disease-caused effects. This suggests caution when invoking multiple stressors as a cause for increased disease susceptibility and indicates that the effects of multiple stressors on disease outcome depend on the interrelationships of stressors to both the pathogen and the host.     

Regional Decline of an Iconic Amphibian Associated with Elevation,Land‐Use Change,and Invasive Species

Abstract: Ecological theory predicts that species with restricted geographic ranges will have the highest probability of extinction, but species with extensive distributions and high population densities can also exhibit widespread population losses. In the western United States populations of northern leopard frogs (Lithobates pipiens)—historically one of the most widespread frogs in North America—have declined dramatically in abundance and geographic distribution. To assess the status of leopard frogs in Colorado and evaluate causes of decline, we coupled statewide surveys of 196 historically occupied sites with intensive sampling of 274 wetlands stratified by land use. We used an information‐theoretic approach to evaluate the contributions of factors at multiple spatial extents in explaining the contemporary distribution of leopard frogs. Our results indicate leopard frogs have declined in Colorado, but this decline was regionally variable. The lowest proportion of occupied wetlands occurred in eastern Colorado (2–28%), coincident with urban development and colonization by non‐native bullfrogs (Lithobates catesbeianus). Variables at several spatial extents explained observed leopard frog distributional patterns. In low‐elevation wetlands introduced fishes, bullfrogs, and urbanization or suburbanization associated negatively with leopard frog occurrence, whereas wetland area was positively associated with occurrence. Leopard frogs were more abundant and widespread west of the Continental Divide, where urban development and bullfrog abundance were low. Although the pathogenic chytrid Batrachochytrium dendrobatidis (Bd) was not selected in our best‐supported models, the nearly complete extirpation of leopard frogs from montane wetlands could reflect the individual or interactive effects of Bd and climate patterns. Our results highlight the importance of considering multiple, competing hypotheses to explain species declines, particularly when implicated factors operate at different spatial extents.     

Thermal Physiology,Disease, and Amphibian Declines on the Eastern Slopes of the Andes

Rising temperatures, a widespread consequence of climate change, have been implicated in enigmatic amphibian declines from habitats with little apparent human impact. The pathogenic fungus Batrachochytrium dendrobatidis (Bd), now widespread in Neotropical mountains, may act in synergy with climate change causing collapse in thermally stressed hosts. We measured the thermal tolerance of frogs along a wide elevational gradient in the Tropical Andes, where frog populations have collapsed. We used the difference between critical thermal maximum and the temperature a frog experiences in nature as a measure of tolerance to high temperatures. Temperature tolerance increased as elevation increased, suggesting that frogs at higher elevations may be less sensitive to rising temperatures. We tested the alternative pathogen optimal growth hypothesis that prevalence of the pathogen should decrease as temperatures fall outside the optimal range of pathogen growth. Our infection‐prevalence data supported the pathogen optimal growth hypothesis because we found that prevalence of Bd increased when host temperatures matched its optimal growth range. These findings suggest that rising temperatures may not be the driver of amphibian declines in the eastern slopes of the Andes. Zoonotic outbreaks of Bd are the most parsimonious hypothesis to explain the collapse of montane amphibian faunas; but our results also reveal that lowland tropical amphibians, despite being shielded from Bd by higher temperatures, are vulnerable to climate‐warming stress. Fisiología Termal, Enfermedades y Disminuciones de Anfibios en las Laderas Orientales de los Andes     

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.     

Demographic Consequences of Terrestrial Habitat Loss for Pool‐Breeding Amphibians: Predicting Extinction Risks Associated with Inadequate Size of Buffer Zones

Abstract: Much of the biodiversity associated with isolated wetlands requires aquatic and terrestrial habitat to maintain viable populations. Current federal wetland regulations in the United States do not protect isolated wetlands or extend protection to surrounding terrestrial habitat. Consequently, some land managers, city planners, and policy makers at the state and local levels are making an effort to protect these wetland and neighboring upland habitats. Balancing human land‐use and habitat conservation is challenging, and well‐informed land‐use policy is hindered by a lack of knowledge of the specific risks of varying amounts of habitat loss. Using projections of wood frog (Rana sylvatica) and spotted salamander (Ambystoma maculatum) populations, we related the amount of high‐quality terrestrial habitat surrounding isolated wetlands to the decline and risk of extinction of local amphibian populations. These simulations showed that current state‐level wetland regulations protecting 30 m or less of surrounding terrestrial habitat are inadequate to support viable populations of pool‐breeding amphibians. We also found that species with different life‐history strategies responded differently to the loss and degradation of terrestrial habitat. The wood frog, with a short life span and high fecundity, was most sensitive to habitat loss and isolation, whereas the longer‐lived spotted salamander with lower fecundity was most sensitive to habitat degradation that lowered adult survival rates. Our model results demonstrate that a high probability of local amphibian population persistence requires sufficient terrestrial habitat, the maintenance of habitat quality, and connectivity among local populations. Our results emphasize the essential role of adequate terrestrial habitat to the maintenance of wetland biodiversity and ecosystem function and offer a means of quantifying the risks associated with terrestrial habitat loss and degradation.     

Exposure to metals (Ca,K, Mn) and road salt (NaCl) differentially affect development and survival in two model amphibians

ABSTRACT

Human activity has led to widespread chemical alteration of natural environments. Aquatic ecosystems are especially susceptible to chemical changes, including those caused by runoff and invasive species. Here, we examined the effects of water chemistry, specifically sodium chloride as well as three metals (Ca, K, and Mn) known to differ between native and invasive wetland plant species’ leaf tissues, on the development of two model amphibians: the native Northern leopard frog, Lithobates pipiens, and the non-native African clawed frog, Xenopus laevis. We exposed frog eggs to metal treatment solutions and measured time to hatching (TTH), and following hatching, we exposed tadpoles to a lethal concentration of sodium chloride and recorded time to death (TTD). We found that increasing metal concentrations generally resulted in acceleration of TTH for Xenopus tadpoles, but had no effect on leopard frogs. However, increasing metal concentrations (Ca, Mn) increased leopard frog tadpole susceptibility to NaCl (decreased TTD), while increasing metal concentrations (Ca, K) generally resulted in decreased Xenopus tadpole susceptibility to NaCl. Overall, our data suggest that invasive amphibians may be more tolerant to chemical changes than native amphibians, including those driven by the introduction of invasive plant 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.     

Assessing Changes in Amphibian Population Dynamics Following Experimental Manipulations of Introduced Fish

Abstract: Sport‐fish introductions are now recognized as an important cause of amphibian decline, but few researchers have quantified the demographic responses of amphibians to current options in fisheries management designed to minimize effects on sensitive amphibians. Demographic analyses with mark–recapture data allow researchers to assess the relative importance of survival, local recruitment, and migration to changes in population densities. I conducted a 4‐year, replicated whole‐lake experiment in the Klamath Mountains of northern California (U.S.A.) to quantify changes in population density, survival, population growth rate, and recruitment of the Cascades frog (Rana cascadae) in response to manipulations of non‐native fish populations. I compared responses of the frogs in lakes where fish were removed, in lakes in their naturally fish‐free state, and in lakes where fish remained that were either stocked annually or no longer being stocked. Within 3 years of fish removals from 3 lakes, frog densities increased by a factor of 13.6. The survival of young adult frogs increased from 59% to 94%, and realized population growth and recruitment rates at the fish‐removal lakes were more than twice as high as the rates for fish‐free reference lakes and lakes that contained fish. Population growth in the fish‐removal lakes was likely due to better on‐site recruitment of frogs to later life stages rather than increased immigration. The effects on R. cascadae of suspending stocking were ambiguous and suggested no direct benefit to amphibians. With amphibians declining worldwide, these results show that active restoration can slow or reverse the decline of species affected by fish stocking within a short time frame.     

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.     

Amphibian Encounter Rates on Roads with Different Amounts of Traffic and Urbanization

Abstract: Although amphibians have relatively high rates of road mortality in urban areas, the conditions under which traffic threatens the survival of local amphibian populations remain unclear. In the Sandhills region of North Carolina (U.S.A.), we counted living and dead amphibians along two transects (total length 165 km) established on roads in areas with varying degrees of urbanization. We found 2665 individuals of 15 species, and amphibian encounter rates declined sharply as traffic and urban development increased. Regression‐tree models indicated that 35 amphibians/100 km occurred on roads with <535 vehicles/day, whereas the encounter rate decreased to only 2 amphibians/100 km on roads with >2048 vehicles/day. Although mortality rate peaked at higher traffic levels (47% dead on roads with >5200 vehicles/day), the number of dead amphibians was highest at low levels of traffic. This suggests that areas where amphibian mortality is concentrated may actually contain the largest populations remaining on a given road transect.     

Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, <Emphasis Type="Italic">Batrachochytrium dendrobatidis</Emphasis>

Behaviors have evolved in response to various selection pressures over evolutionary time. However, not all behaviors are adaptive. Some presumably “ancient” behaviors, persistent for millions of years, may be detrimental in the face of novel selection pressures in modern times. These pressures include a multitude of emerging infectious diseases which may be stimulated by environmental changes. We examined how a globally emerging amphibian pathogen, Batrachochytrium dendrobatidis (BD), affected two key evolutionarily persistent behaviors displayed by amphibian larvae: aggregation and thermoregulation. Larval aggregation behavior is often essential for foraging, thermoregulation, and antipredator defense, but varies among species. Thermoregulatory behavior speeds larval development in ephemeral habitats. Specifically, we examined whether aggregation and thermoregulatory behaviors changed when exposed to the BD pathogen in two species (Bufo boreas and Rana cascadae) whose larvae aggregate in nature. In laboratory choice tests, larvae of neither species avoided infected conspecifics. BD-exposed B. boreas larvae aggregated, while unexposed R. cascadae larvae associated more frequently with BD-exposed conspecifics. There was no evidence of behavioral fever or altered thermoregulation in larvae of four species we examined (Pseudacris regilla, Rana aurora, B. boreas, R. cascadae). The absence of behavioral fever may suggest an inability of the larvae of some host species to mediate infection risk by this pathogen. Thermoregulatory behaviors may exhibit a high degree of evolutionary inertia in amphibian hosts because they are linked with host physiology and developmental rates, while altered aggregation behaviors could potentially elevate pathogen transmission rates, leading to increased infection risk in social amphibian species.     

Effects of the Interaction between Genetic Diversity and UV-B Radiation on Wood Frog Fitness

Abstract:  Genetic diversity may buffer amphibian populations against environmental vicissitudes. We hypothesized that wood frogs (  Rana sylvatica ) from populations with lower genetic diversity are more susceptible to ultraviolet-B (UV-B) radiation than those from populations with higher diversity. We used RAPD markers to obtain genetic diversity estimates for 12 wood frog populations. We reared larval wood frogs from these populations and exposed experimental groups of eggs and larvae to one of three treatments: unfiltered sunlight, sunlight filtered through a UV-B-blocking filter (Mylar), and sunlight filtered through a UV-B-transmitting filter (acetate). In groups exposed to UV-B, larval mortality and deformity rates increased significantly, but egg mortality did not. We found a significant negative relationship between genetic diversity and egg mortality, larval mortality, and deformity rates. Furthermore, the interaction between UV-B treatment and genetic diversity significantly affected larval mortality. Populations with low genetic diversity experienced higher larval mortality rates when exposed to UV-B than did populations with high genetic diversity. This is the first time an interaction between genetic diversity and an environmental stressor has been documented in amphibians. Differences in genetic diversity among populations, coupled with environmental stressors, may help explain patterns of amphibian decline.     

Influences of Egg Laying Behavior on Pathogenic Infection of Amphibian Eggs

Mass mortality of developing amphibian eggs and larvae from pathogenic infection has been recently documented in some amphibian populations. For example, the pathogenic fungus, Saprolegnia ferax, has been linked with amphibian embryo mortality in the Pacific Northwest. Continued mortality in early life history stages may ultimately contribute to a population decline. We document the prevalence of S. ferax on embryos of three anuran species (   Bufo boreas, Rana cascadae, and Hyla regilla) common to the Pacific Northwest. These species differ in key aspects of their behavior and ecology, and these differences may lead to differential susceptibility to S. ferax. R. cascadae often lays its eggs communally and B. boreas usually deposits its eggs communally. We observed embryos at natural oviposition sites. Eggs laid communally had higher mortality than those laid away from other egg masses. Field experiments that manipulated both the spatial position and timing of egg laying demonstrated that eggs laid later and in closer proximity to communal masses had higher mortality. Our results suggest that eggs in communal masses are highly susceptible to infection with S. ferax.     

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