Cutaneous Microbial Community Variation across Populations of Eastern Hellbenders (Cryptobranchus alleganiensis alleganiensis)

Multicellular hosts maintain complex associations with microbial communities. While microbial communities often serve important functional roles for their hosts, our understanding of the local and regional processes that structure these communities remains limited. Metacommunity analyses provide a promising tool for investigating mechanisms shaping microbiome heterogeneity, which is essential for predicting functional variation between hosts. Using a metacommunity framework, we examined heterogeneity in the skin microbiome of the eastern hellbender (Cryptobranchus alleganiensis alleganiensis). Hellbenders are broadly distributed throughout river systems in the eastern United States, but are present in specific environmental locations throughout their range. The large range of the species and history of population fragmentation suggest that local and regional processes contribute to the distribution of cutaneous symbiont diversity. Therefore, we characterized the skin and environmental bacterial communities at eight rivers throughout the range of the species. We observed variation among hellbender populations in skin microbial community diversity and proportion of shared operational taxonomic units (OTUs) between animal and river water communities. Among populations sampled, we noted significant clumped OTU turnover (i.e., Clementsian structure) resulting in unique cutaneous communities. In addition, we observed a significant positive correlation between skin community divergence and hellbender population genetic divergence. Host-population skin community dissimilarity did not correlate strongly with distance between sampling locations, indicating a weak spatial effect on the distribution of symbionts. These results suggest that species sorting mechanisms (i.e., local processes) structure local skin microbial communities in hellbenders. The variation in skin community composition observed among host populations foreshadows a similar pattern in important functional characteristics (e.g., resistance to dysbiosis). Future work should focus on investigating forces shaping microbiome structure in eastern hellbenders, examining functional variation among populations, and evaluating effectiveness of microbiome management recommendations

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

Ranaviruses have been identified in wild and captive populations of ectothermic vertebrates around the world. Ranavirus epidemics can result in a range of effects on their host populations, from apparently benign infections to mass mortality and local extirpation. In this chapter, we review the current status of ranavirus epidemiology and ecology in amphibians, fish, and reptiles. Ranavirus epidemics in amphibians and fish usually have a rapid onset in the mid-to-late summer while outbreaks in reptiles occur irregularly. Susceptibility to ranavirus differs among host species, and may be influenced by the type of ranavirus and natural or anthropogenic stressors. Ranaviruses can be transmitted within and between host species via several routes, but there is a need for transmission estimates in natural environments. Generally, ranaviruses are locally adapted to their host populations, but movement of infected hosts over long distances can disrupt these associations. There is evidence of increased virulence of ranaviruses in captive fish and amphibian populations raised for production. Given their broad host ranges, potential for high virulence, multiple routes of transmission, and frequent movement of amphibians, fish and reptiles in global trade, it appears that some ranaviruses have the potential to significantly impact host populations and even cause extinctions in the wild

Development and Disease: How Susceptibility to an Emerging Pathogen Changes through Anuran Development

Ranaviruses have caused die-offs of amphibians across the globe. In North America, these pathogens cause more amphibian mortality events than any other pathogen. Field observations suggest that ranavirus epizootics in amphibian communities are common during metamorphosis, presumably due to changes in immune function. However, few controlled studies have compared the relative susceptibility of amphibians to ranaviruses across life stages. Our objectives were to measure differences in mortality and infection prevalence following exposure to ranavirus at four developmental stages and determine whether the differences were consistent among seven anuran species. Based on previous studies, we hypothesized that susceptibility to ranavirus would be greatest at metamorphosis. Our results did not support this hypothesis, as four of the species were most susceptible to ranavirus during the larval or hatchling stages. The embryo stage had the lowest susceptibility among species probably due to the protective membranous layers of the egg. Our results indicate that generalizations should be made cautiously about patterns of susceptibility to ranaviruses among amphibian developmental stages and species. Further, if early developmental stages of amphibians are susceptible to ranaviruses, the impact of ranavirus epizootic events may be greater than realized due to the greater difficulty of detecting morbid hatchlings and larvae compared to metamorphs

Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease

Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a 1‐day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the amphibian fungal pathogen Batrachochytrium salamandrivorans. Despite the inevitable uncertainty, experts suggested and discussed several possible strategies. However, their recommendations were undermined by imperfect initial definitions of the objectives and scope of management. This problem is likely to arise in most real‐world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial–temporal scale of mitigation decisions. Managers are commonly under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes

Data from: Prey responses to fine-scale variation in predation risk from combined predators

While it is well documented that organisms can express phenotypic plasticity in response to single gradients of environmental variation, our understanding of how organisms integrate information along multiple environmental gradients is limited in many systems. Using the freshwater snail Helisoma trivolvis and two common predators (water bugs Belostoma flumineum and crayfish Orconectes rusticus), we explored how prey integrate information along multiple predation risk gradients (i.e. caged predators fed increasing amounts of prey biomass) that induce opposing phenotypes. When exposed to single predators fed increasing amounts of prey biomass, we detected threshold responses; intermediate amounts of consumed biomass induced phenotypic responses, but higher amounts induced little additional induction. This suggests that additional increases in predator-induced traits with greater predator risk offer minimal increases in fitness or that a limit in the response magnitude was reached. Additionally, the response thresholds were contingent on the predator and focal trait. For shell width, responses were generally detected at a lower amount of consumed biomass by water bugs compared to crayfish. Within the crayfish treatments, we found that the shell thickness response threshold was lower than the shell width response threshold. When we combined gradients of consumed biomass from both predators, we found that the magnitude of response to one predator was often reduced when the other predator was present. Interestingly, these effects were often detected at consumed biomass levels that were lower than the threshold concentration necessary to elicit a response in the single-predator treatments. Moreover, our combined predator treatments revealed that snails shifted from discrete responses to more continuous (i.e. graded) responses. Together, our results reveal that organisms experiencing multiple environmental gradients can integrate this information to make phenotypic decisions and demonstrate the novel result that an exposure to multiple species of predators can lower the response threshold of prey

Hoverman & Relyea Oikos 2015 data

Pool means for each of the sample dates of the experiment are provided for each experimental unit. Metadata is provided in the document

Ranavirus-fever data

Toad temperature, mass, and ranaviral load data associated with Sauer et al. 2019 - Functional Ecology. Metadata is included in the excel workbook

Appendix B. Results from analysis of the effects of predator emigration at four times on snail traits.

Results from analysis of the effects of predator emigration at four times on snail traits

Ecology and pathology of amphibian ranaviruses

Mass mortality of amphibians has occurred globally since at least the early 1990s from viral pathogens that are members of the genus Ranavirus, family Iridoviridae. The pathogen infects multiple amphibian hosts, larval and adult cohorts, and may persist in herpetofaunal and osteichthyan reservoirs. Environmental persistence of ranavirus virions outside a host may be several weeks or longer in aquatic systems. Transmission occurs by indirect and direct routes, and includes exposure to contaminated water or soil, casual or direct contact with infected individuals, and ingestion of infected tissue during predation, cannibalism, or necrophagy. Some gross lesions include swelling of the limbs or body, erythema, swollen friable livers, and hemorrhage. Susceptible amphibians usually die from chronic cell death in multiple organs, which can occur within a few days following infection or may take several weeks. Amphibian species differ in their susceptibility to ranaviruses, which may be related to their co-evolutionary history with the pathogen. The occurrence of recent widespread amphibian population die-offs from ranaviruses may be an interaction of suppressed and naïve host immunity, anthropogenic stressors, and novel strain introduction. This review summarizes the ecological research on amphibian ranaviruses, discusses possible drivers of emergence and conservation strategies, and presents ideas for future research directions. We also discuss common pathological signs of ranaviral disease, methods for diagnostic evaluation, and ranavirus surveillance methods. Inasmuch as ranaviral disease is listed as a notifiable disease by the World Organization for Animal Health and is a threat to amphibian survival, we recommend that biosecurity precautions are implemented by nations to reduce the likelihood of transporting ranavirus virions among populations. Biosecurity precautions include disinfecting footwear and equipment that comes in contact with surface water inhabited by amphibians and testing commercially shipped amphibians for the pathogen. We also encourage natural resource organizations to establish routine surveillance programs for ranaviruses in wild amphibian populations