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.     

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.     

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     

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.     

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.     

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.     

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.     

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.     

Ecology of Chytridiomycosis in Rainforest Stream Frog Assemblages of Tropical Queensland

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

Effects of threat management interactions on conservation priorities

Decisions need to be made about which biodiversity management actions are undertaken to mitigate threats and about where these actions are implemented. However, management actions can interact; that is, the cost, benefit, and feasibility of one action can change when another action is undertaken. There is little guidance on how to explicitly and efficiently prioritize management for multiple threats, including deciding where to act. Integrated management could focus on one management action to abate a dominant threat or on a strategy comprising multiple actions to abate multiple threats. Furthermore management could be undertaken at sites that are in close proximity to reduce costs. We used cost‐effectiveness analysis to prioritize investments in fire management, controlling invasive predators, and reducing grazing pressure in a bio‐diverse region of southeastern Queensland, Australia. We compared outcomes of 5 management approaches based on different assumptions about interactions and quantified how investment needed, benefits expected, and the locations prioritized for implementation differed when interactions were taken into account. Managing for interactions altered decisions about where to invest and in which actions to invest and had the potential to deliver increased investment efficiency. Differences in high priority locations and actions were greatest between the approaches when we made different assumptions about how management actions deliver benefits through threat abatement: either all threats must be managed to conserve species or only one management action may be required. Threatened species management that does not consider interactions between actions may result in misplaced investments or misguided expectations of the effort required to mitigate threats to species.     

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

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

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.     

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.     

A Strategy for Monitoring and Managing Declines in an Amphibian Community

Although many taxa have declined globally, conservation actions are inherently local. Ecosystems degrade even in protected areas, and maintaining natural systems in a desired condition may require active management. Implementing management decisions under uncertainty requires a logical and transparent process to identify objectives, develop management actions, formulate system models to link actions with objectives, monitor to reduce uncertainty and identify system state (i.e., resource condition), and determine an optimal management strategy. We applied one such structured decision‐making approach that incorporates these critical elements to inform management of amphibian populations in a protected area managed by the U.S. National Park Service. Climate change is expected to affect amphibian occupancy of wetlands and to increase uncertainty in management decision making. We used the tools of structured decision making to identify short‐term management solutions that incorporate our current understanding of the effect of climate change on amphibians, emphasizing how management can be undertaken even with incomplete information. Estrategia para Monitorear y Manejar Disminuciones en una Comunidad de Anfibios     

Using empirical models of species colonization under multiple threatening processes to identify complementary threat‐mitigation strategies

Approaches to prioritize conservation actions are gaining popularity. However, limited empirical evidence exists on which species might benefit most from threat mitigation and on what combination of threats, if mitigated simultaneously, would result in the best outcomes for biodiversity. We devised a way to prioritize threat mitigation at a regional scale with empirical evidence based on predicted changes to population dynamics—information that is lacking in most threat‐management prioritization frameworks that rely on expert elicitation. We used dynamic occupancy models to investigate the effects of multiple threats (tree cover, grazing, and presence of an hyperaggressive competitor, the Noisy Miner (Manorina melanocephala) on bird‐population dynamics in an endangered woodland community in southeastern Australia. The 3 threatening processes had different effects on different species. We used predicted patch‐colonization probabilities to estimate the benefit to each species of removing one or more threats. We then determined the complementary set of threat‐mitigation strategies that maximized colonization of all species while ensuring that redundant actions with little benefit were avoided. The single action that resulted in the highest colonization was increasing tree cover, which increased patch colonization by 5% and 11% on average across all species and for declining species, respectively. Combining Noisy Miner control with increasing tree cover increased species colonization by 10% and 19% on average for all species and for declining species respectively, and was a higher priority than changing grazing regimes. Guidance for prioritizing threat mitigation is critical in the face of cumulative threatening processes. By incorporating population dynamics in prioritization of threat management, our approach helps ensure funding is not wasted on ineffective management programs that target the wrong threats or 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.     

Optimal Marking of Threatened Species to Balance Benefits of Information with Impacts of Marking

Abstract: Marking animals so that they are uniquely identifiable provides information that may assist conservation efforts. Nevertheless, some methods used to mark animals can be harmful. We used mathematical methods to assess the trade‐off between the impact of marking threatened species and the value of the information gained. We considered the case where 2 management strategies, each aiming to improve a species' survival rate, are implemented in an experimental phase. The results of the experiment were applied in a postexperimental management phase. We expressed the expected number of survivors in both phases mathematically, accounting for any mortality caused by the experiment, and determined the proportion of animals to mark to maximize this number. The optimal number of animals to mark increased with the number of individuals available for the experiment and with the number of individuals to be managed in the future. The optimal solution was to mark only 25% of the animals when there were 1000 individuals available for the experiment, the results were used to manage 2000 individuals, and marking caused mortality of 1%. Fewer animals were marked when there were fewer animals in either phase or when marking caused higher mortality. In the case of the Helmeted Honeyeater (Lichenostomus melanops cassidix), the optimal proportion to mark was <1 if the mortality rate was >0.15%–1%, with the threshold depending on the number of animals in the experimental and postexperimental phases. The trade‐off between gaining more information about a species and possibly harming individuals of that species by marking them is difficult to assess subjectively. We show how to determine objectively the optimal proportion of animals to mark to enhance the management of threatened species.     

Differential Host Susceptibility to Batrachochytrium dendrobatidis,an Emerging Amphibian Pathogen

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

A framework for allocating conservation resources among multiple threats and actions

Land managers decide how to allocate resources among multiple threats that can be addressed through multiple possible actions. Additionally, these actions vary in feasibility, effectiveness, and cost. We sought to provide a way to optimize resource allocation to address multiple threats when multiple management options are available, including mutually exclusive options. Formulating the decision as a combinatorial optimization problem, our framework takes as inputs the expected impact and cost of each threat for each action (including do nothing) and for each overall budget identifies the optimal action to take for each threat. We compared the optimal solution to an easy to calculate greedy algorithm approximation and a variety of plausible ranking schemes. We applied the framework to management of multiple introduced plant species in Australian alpine areas. We developed a model of invasion to predict the expected impact in 50 years for each species-action combination that accounted for each species’ current invasion state (absent, localized, widespread); arrival probability; spread rate; impact, if present, of each species; and management effectiveness of each species-action combination. We found that the recommended action for a threat changed with budget; there was no single optimal management action for each species; and considering more than one candidate action can substantially increase the management plan's overall efficiency. The approximate solution (solution ranked by marginal cost-effectiveness) performed well when the budget matched the cost of the prioritized actions, indicating that this approach would be effective if the budget was set as part of the prioritization process. The ranking schemes varied in performance, and achieving a close to optimal solution was not guaranteed. Global sensitivity analysis revealed a threat's expected impact and, to a lesser extent, management effectiveness were the most influential parameters, emphasizing the need to focus research and monitoring efforts on their quantification.     

Planning for ex situ conservation in the face of uncertainty

Ex situ conservation strategies for threatened species often require long‐term commitment and financial investment to achieve management objectives. We present a framework that considers the decision to adopt ex situ management for a target species as the end point of several linked decisions. We used a decision tree to intuitively represent the logical sequence of decision making. The first decision is to identify the specific management actions most likely to achieve the fundamental objectives of the recovery plan, with or without the use of ex‐situ populations. Once this decision has been made, one decides whether to establish an ex situ population, accounting for the probability of success in the initial phase of the recovery plan, for example, the probability of successful breeding in captivity. Approaching these decisions in the reverse order (attempting to establish an ex situ population before its purpose is clearly defined) can lead to a poor allocation of resources, because it may restrict the range of available decisions in the second stage. We applied our decision framework to the recovery program for the threatened spotted tree frog (Litoria spenceri) of southeastern Australia. Across a range of possible management actions, only those including ex situ management were expected to provide >50% probability of the species’ persistence, but these actions cost more than use of in situ alternatives only. The expected benefits of ex situ actions were predicted to be offset by additional uncertainty and stochasticity associated with establishing and maintaining ex situ populations. Naïvely implementing ex situ conservation strategies can lead to inefficient management. Our framework may help managers explicitly evaluate objectives, management options, and the probability of success prior to establishing a captive colony of any given species.