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.     

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.     

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.     

Evaluation of Selective Culling of Infected Individuals to Control Tasmanian Devil Facial Tumor Disease

Abstract: Sustainable strategies to manage infectious diseases in threatened wildlife are still lacking despite considerable concern over the global increase in emerging infectious diseases of wildlife and their potential to drive populations to extinction. Selective culling of infected individuals will often be the most feasible option to control infectious disease in a threatened wildlife host, but has seldom been implemented or evaluated as a management tool for the conservation of threatened species. The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction by an infectious cancer, devil facial tumor disease (DFTD). We assess the success of an adaptive management trial involving selective culling of infected Tasmanian devils to control DFTD. Demographic and epidemiological parameters indicative of disease progression and impact were compared between the management site and a comparable unmanaged control site. Selective culling of infected individuals neither slowed rate of disease progression nor reduced population‐level impacts of this debilitating disease. Culling mortality simply compensated for disease mortality in this system. Failure of selective culling to impede DFTD progress and reduce its impacts in the managed population was attributed to DFTD's frequency‐dependent nature, its long latent period and high degree of infectivity, and the presence of a cryptic hidden disease reservoir or continual immigration of diseased individuals. We suggest that increasing the current removal rate and focusing removal efforts prior to the breeding season are options worth pursuing for future management of DFTD in this population. On the basis of our experience, we suggest that disease‐management programs for threatened wildlife populations be developed on the principles of adaptive management and utilize a wide variety of strategies with regular reviews and adaptation of strategies undertaken as new information is obtained.     

Factors Determining the Choice of Hunting and Trading Bushmeat in the Kilombero Valley,Tanzania

Regulation of illegal bushmeat trade is a major conservation challenge in Africa. We investigated what factors are most likely to induce actors in the bushmeat trade to shift to an alternative occupation by conducting a choice experiment with 325 actors in the bushmeat trade in the Kilombero Valley, Tanzania. Specifically, we asked respondents to choose between hunting or trading bushmeat and alternative salary‐paying work, in a set of hypothetical scenarios where the attributes of these alternatives were varied and included measures of command and control, price of substitute meat, daily salary in the work option, and whether or not cows were donated to the respondent. We modeled the choice contingent on socioeconomic characteristics. The magnitude of fines and patrolling frequency had a significant but very low negative effect on the probability of choosing to engage in hunting or trading bushmeat compared with the salary of an alternative occupation. Donation of livestock and the price of substitute meats in the local market both affected the choice significantly in a negative and a positive direction, respectively. The wealthier a household was the more likely the respondent was to choose to continue hunting or trading bushmeat. On the margin, our results suggest that given current conditions in the Kilombero Valley on any given day 90% of the respondents would choose salary work at US$3.37/day over their activities in the bushmeat trade, all else equal. Factores que Determinan la Elección de Cazar y Vender Carne de Caza en el Valle Kilombero, Tanzania     

Reduced effect of Tasmanian devil facial tumor disease at the disease front

Pathogen-driven declines in animal populations are increasingly regarded as a major conservation issue. The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction by devil facial tumor disease, a unique transmissible cancer. The disease is transmitted through direct transfer of tumor cells, which is possible because the genetic diversity of Tasmanian devils is low, particularly in the major histocompatibility complex genes of the immune system. The far northwest of Tasmania now holds the last remaining disease-free wild devil populations. The recent discovery of unique major histocompatibility complex genotypes in the northwestern region of Tasmania has raised the possibility that some animals may be resilient to the disease. We examined the differences in the epidemiology and population effects of devil facial tumor disease at 3 well-studied affected sites in eastern Tasmania and 1 in western Tasmania (West Pencil Pine). In contrast to the 3 eastern sites, there has been no rapid increase in disease prevalence or evidence of population decline at West Pencil Pine. Moreover, this is the only onsite at which the population age structure has remained unaltered 4 years after the first detection of disease. The most plausible explanations for the substantial differences in population effects and epidemiology of the disease between eastern and western sites are geographic differences in genotypes or phenotypes of devils and functional differences between tumor strains in the 2 regions. We suggest that conservation efforts focus on identifying whether either or both these explanations are correct and then, if resistance alleles exist, to attempt to spread the resistant alleles into affected populations. Such assisted selection has rarely been attempted for the management of wildlife diseases, but it may be widely applicable.     

Setting population targets for mammals using body mass as a predictor of population persistence

Conservation planning and biodiversity assessments need quantitative targets to optimize planning options and assess the adequacy of current species protection. However, targets aiming at persistence require population‐specific data, which limit their use in favor of fixed and nonspecific targets, likely leading to unequal distribution of conservation efforts among species. We devised a method to derive equitable population targets; that is, quantitative targets of population size that ensure equal probabilities of persistence across a set of species and that can be easily inferred from species‐specific traits. In our method, we used models of population dynamics across a range of life‐history traits related to species’ body mass to estimate minimum viable population targets. We applied our method to a range of body masses of mammals, from 2 g to 3825 kg. The minimum viable population targets decreased asymptotically with increasing body mass and were on the same order of magnitude as minimum viable population estimates from species‐ and context‐specific studies. Our approach provides a compromise between pragmatic, nonspecific population targets and detailed context‐specific estimates of population viability for which only limited data are available. It enables a first estimation of species‐specific population targets based on a readily available trait and thus allows setting equitable targets for population persistence in large‐scale and multispecies conservation assessments and planning.     

Practitioner and scientist perceptions of successful amphibian conservation

Conservation requires successful outcomes. However, success is perceived in many different ways depending on the desired outcome. Through a questionnaire survey, we examined perceptions of success among 355 scientists and practitioners working on amphibian conservation from over 150 organizations in more than 50 countries. We also sought to identify how different types of conservation actions and respondent experience and background influenced perceptions. Respondents identified 4 types of success: species and habitat improvements (84% of respondents); effective program management (36%); outreach initiatives such as education and public engagement (25%); and the application of science‐based conservation (15%). The most significant factor influencing overall perceived success was reducing threats. Capacity building was rated least important. Perceptions were influenced by experience, professional affiliation, involvement in conservation practice, and country of residence. More experienced practitioners associated success with improvements to species and habitats and less so with education and engagement initiatives. Although science‐based conservation was rated as important, this factor declined in importance as the number of programs a respondent participated in increased, particularly among those from less economically developed countries. The ultimate measure of conservation success—population recovery—may be difficult to measure in many amphibians; difficult to relate to the conservation actions intended to drive it; and difficult to achieve within conventional funding time frames. The relaunched Amphibian Conservation Action Plan provides a framework for capturing lower level processes and outcomes, identifying gaps, and measuring progress.     

Species composition of the international shark fin trade assessed through a retail‐market survey in Hong Kong

The shark fin trade is a major driver of shark exploitation in fisheries all over the world, most of which are not managed on a species‐specific basis. Species‐specific trade information highlights taxa of particular concern and can be used to assess the efficacy of management measures and anticipate emerging threats. The species composition of the Hong Kong Special Administrative Region of China, one of the world's largest fin trading hubs, was partially assessed in 1999–2001. We randomly selected and genetically identified fin trimmings (n = 4800), produced during fin processing, from the retail market of Hong Kong in 2014–2015 to assess contemporary species composition of the fin trade. We used nonparametric species estimators to determine that at least 76 species of sharks, batoids, and chimaeras supplied the fin trade and a Bayesian model to determine their relative proportion in the market. The diversity of traded species suggests species substitution could mask depletion of vulnerable species; one‐third of identified species are threatened with extinction. The Bayesian model suggested that 8 species each comprised >1% of the fin trimmings (34.1–64.2% for blue [Prionace glauca], 0.2–1.2% for bull [Carcharhinus leucas] and shortfin mako [Isurus oxyrinchus]); thus, trade was skewed to a few globally distributed species. Several other coastal sharks, batoids, and chimaeras are in the trade but poorly managed. Fewer than 10 of the species we modeled have sustainably managed fisheries anywhere in their range, and the most common species in trade, the blue shark, was not among them. Our study and approach serve as a baseline to track changes in composition of species in the fin trade over time to better understand patterns of exploitation and assess the effects of emerging management actions for these animals.     

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.     

Effects of Two Amphibian Pathogens on the Developmental Stability of Green Frogs

Abstract: Developmental instability, measured as fluctuating asymmetry (FA), is often used as a tool to measure stress and the overall quality of organisms. Under FA, it is assumed that control of symmetry during development is costly and that under stress the trajectory of development is disturbed, resulting in asymmetric morphologies. Amphibian emergent infectious diseases (EIDs), such as Ranavirus and chytrid fungus, have been involved in several mortality events, which makes them stressors and allows for the study of FA. We analyzed nine populations of green frogs (Rana clamitans) for the presence or absence of Ranavirus and chytrid fungus. Individuals were measured to determine levels of FA in seven traits under the hypothesis that FA is more likely to be observed in individuals infected by the pathogens. Significantly higher levels of FA were found in individuals with Ranavirus compared with uninfected individuals among all populations and all traits. We did not observe FA in individuals infected with chytrid fungus for any of the traits measured. Additionally, we observed a significant association between Ranavirus infection and levels of FA in both males and females, which may indicate this viral disease is likely to affect both sexes during development. Altogether, our results indicate that some EIDs may have far‐reaching and nonlethal effects on individual development and populations harboring such diseases and that FA can be used as a conservation tool to identify populations subject to such a stress.