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1. Putative resistance and tolerance mechanisms have little impact on disease progression for an emerging salamander pathogen

   https://doi.org/10.1111/1365-2435.13754  

   Wilber, Mark Q. ; Carter, Edward Davis ; Gray, Matthew J. ; Briggs, Cheryl J. ; Pedersen, ed., Amy ( January 2021 , Functional Ecology)

   Resistance and tolerance are unique host defence strategies that can limit the impacts of a pathogen on a host. However, for most wildlife–pathogen systems, there are still fundamental uncertainties regarding (a) how changes in resistance and tolerance can affect disease outcomes and (b) the mechanisms underlying resistance and tolerance in host populations.

   Here, we first compared observed patterns of resistance and tolerance and their effects on disease outcomes among salamander species that are susceptible to infection and mortality from the emerging fungal pathogenBatrachochytrium salamandrivorans(Bsal). We then tested whether two putative mechanisms that contribute to host resistance and tolerance, skin sloughing and skin lesion reduction, predicted reducedBsalgrowth rate or increased host survival during infection, respectively.

   We performed multi‐doseBsalchallenge experiments on four species of Salamandridae found throughout North America. We combined the laboratory experiments with dynamic models and sensitivity analysis to examine how changes in load‐dependent resistance and tolerance functions affectedBsal‐induced mortality risk. Finally, we used our disease model to test whether skin sloughing and lesion reduction predicted variability in infection outcomes not described byBsalinfection intensity.

   We found that resistance and tolerance differed significantly among salamander species, with the most susceptible species being both less resistance and less tolerant ofBsalinfection. Our dynamic model showed that the relative influence of resistance versus tolerance on host survival was species‐dependent—increasing resistance was only more influential than increasing tolerance for the least tolerant species where changes in pathogen load had a threshold‐like effect on host survival. Testing two candidate mechanisms of resistance and tolerance, skin sloughing and lesion reduction, respectively, we found limited support that either of these processes were strong mechanisms of host defence.

   Our study contributes to a broader understanding of resistance and tolerance in host–pathogen systems by showing that differences in host tolerance can significantly affect whether changes in resistance or tolerance have larger effects on disease outcomes, highlighting the need for species and even population‐specific management approaches that target host defence strategies.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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2. Inhibitory Bacterial Diversity and Mucosome Function Differentiate Susceptibility of Appalachian Salamanders to Chytrid Fungal Infection

   https://doi.org/10.1128/aem.01818-21  

   Jiménez, Randall R. ; Carfagno, Amy ; Linhoff, Luke ; Gratwicke, Brian ; Woodhams, Douglas C. ; Chafran, Liana Soares ; Bletz, Molly C. ; Bishop, Barney ; Muletz-Wolz, Carly R. ( April 2022 , Applied and Environmental Microbiology)

   Reguera, Gemma (Ed.)

   ABSTRACT Mucosal defenses are crucial in animals for protection against pathogens and predators. Host defense peptides (antimicrobial peptides, AMPs) as well as skin-associated microbes are key components of mucosal immunity, particularly in amphibians. We integrate microbiology, molecular biology, network-thinking, and proteomics to understand how host and microbially derived products on amphibian skin (referred to as the mucosome) serve as pathogen defenses. We studied defense mechanisms against chytrid pathogens, Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), in four salamander species with different Batrachochytrium susceptibilities. Bd infection was quantified using qPCR, mucosome function (i.e., ability to kill Bd or Bsal zoospores in vitro ), skin bacterial communities using 16S rRNA gene amplicon sequencing, and the role of Bd-inhibitory bacteria in microbial networks across all species. We explored the presence of candidate-AMPs in eastern newts and red-backed salamanders. Eastern newts had the highest Bd prevalence and mucosome function, while red-back salamanders had the lowest Bd prevalence and mucosome function, and two-lined salamanders and seal salamanders were intermediates. Salamanders with highest Bd infection intensity showed greater mucosome function. Bd infection prevalence significantly decreased as putative Bd-inhibitory bacterial richness and relative abundance increased on hosts. In co-occurrence networks, some putative Bd-inhibitory bacteria were found as hub-taxa, with red-backs having the highest proportion of protective hubs and positive associations related to putative Bd-inhibitory hub bacteria. We found more AMP candidates on salamanders with lower Bd susceptibility. These findings suggest that salamanders possess distinct innate mechanisms that affect chytrid fungi. IMPORTANCE How host mucosal defenses interact, and influence disease outcome is critical in understanding host defenses against pathogens. A more detailed understanding is needed of the interactions between the host and the functioning of its mucosal defenses in pathogen defense. This study investigates the variability of chytrid susceptibility in salamanders and the innate defenses each species possesses to mediate pathogens, thus advancing the knowledge toward a deeper understanding of the microbial ecology of skin-associated bacteria and contributing to the development of bioaugmentation strategies to mediate pathogen infection and disease. This study improves the understanding of complex immune defense mechanisms in salamanders and highlights the potential role of the mucosome to reduce the probability of Bd disease development and that putative protective bacteria may reduce likelihood of Bd infecting skin. 

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3. Environmental DNA ‐based detection of pathogens in trade and captive settings: Best practices and validation for Batrachochytrium salamandrivorans

   https://doi.org/10.1111/2041-210X.14217  

   Brunner, Jesse L. ; Yarber, Christian M. ; Pearhill, Robert A. I. ; Goldberg, Caren S. ( September 2023 , Methods in Ecology and Evolution)

   Detecting pathogens in the live animal trade is critical for tracking and preventing their movement, introduction and spillover into susceptible fauna. However, the scale of the live animal trade makes individually testing animals infeasible for all but the most economically important taxa. For instance, while the fungal pathogen,Batrachochytrium salamandrivorans(Bsal), threatens amphibian, particularly caudate diversity, in Europe and the Americas, screening even a fraction of the millions of live amphibians imported into the United States, alone, is impractically laborious and expensive. A promising alternative to individual‐level sampling (e.g. swabbing the skin of salamanders) is to instead collect DNA from the animals' environment (e.g. housing container or water) which allows us to screen a whole group of animals at a time.

   We used a series of experiments withBsal‐spiked water and substrates and experimentally infected rough‐skinned newts (Taricha granulosa) to determine which methods yield the mostBsalenvironmental DNA (eDNA) and evaluate the capacity of these methods to detectBsal‐infected animals in conditions found in captive settings and trade.

   We found that filtering water housing infected animals for even an hour can consistently recover detectable levels ofBsaleDNA, that there is little evidence ofBsaleDNA being clumped in housing containers or swamped or inhibited by dirty housing containers, and that eDNA‐based methods achieves an equivalent or higher chance of detectingBsalinfections in a (virtual) population of co‐housed newts with fewer samples than individual swabs.

   By sampling the genetic materials accumulated from a whole group of animals, eDNA‐based methods are a powerful means of detecting pathogens, such asBsal, in shipments and captive populations. These methods bring routine pathogen surveillance into reach in many more contexts and can thus be an important tool in conservation and disease control.

    

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4. Reducing environmentally mediated transmission to moderate impacts of an emerging wildlife disease

   https://doi.org/10.1111/1365-2664.14371  

   Hoyt, Joseph R. ; Parise, Katy L. ; DePue, John E. ; Kaarakka, Heather M. ; Redell, Jennifer A. ; Scullon, William H. ; O'Reskie, Rich ; Foster, Jeffrey T. ; Kilpatrick, A. Marm ; Langwig, Kate E. ; et al ( March 2023 , Journal of Applied Ecology)

   Emerging infectious diseases have caused population declines and biodiversity loss. The ability of pathogens to survive in the environment, independent of their host, can exacerbate disease impacts and increase the likelihood of species extinction. Control of pathogens with environmental stages remains a significant challenge for conservation and effective management strategies are urgently needed.

   We examined the effectiveness of managing environmental exposure to reduce the impacts of an emerging infectious disease of bats, white‐nose syndrome (WNS). We used a chemical disinfectant, chlorine dioxide (ClO₂), to experimentally reducePseudogymnoascus destructans, the fungal pathogen causing WNS, in the environment. We combined laboratory experiments with 3 years of field trials at four abandoned mines to determine whether ClO₂could effectively removeP. destructansfrom the environment, reduce host infection and limit population impacts.

   ClO₂was effective at killingP. destructansin vitro across multiple concentrations. In field settings, higher concentrations of ClO₂treatment were needed to sufficiently reduce viableP. destructansconidia in the environment.

   The reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was also higher in little brown bats (Myotis lucifugus), and trended higher for tricolored bats (Perimyotis subflavus).

   Synthesis and applications. Our results highlight that targeted management of sources for environmental transmission can be an effective control strategy for wildlife disease. We found that successfully reducing pathogen in the environment decreased disease severity and increased survival, but required higher treatment exposure than was effective in laboratory experiments, and the effects varied among species. More broadly, our findings have implications for other emerging wildlife diseases with free‐living pathogen stages by highlighting how the degree of environmental contamination can have cascading impacts on hosts, presenting an opportunity for intervention.

    

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5. Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans

   https://doi.org/10.1371/journal.ppat.1009234  

   Carter, Edward Davis ; Bletz, Molly C. ; Le Sage, Mitchell ; LaBumbard, Brandon ; Rollins-Smith, Louise A. ; Woodhams, Douglas C. ; Miller, Debra L. ; Gray, Matthew J. ( February 2021 , PLOS Pathogens)

   Wang, Chengshu (Ed.)

   Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans ( Bsal ), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N . viridescens , adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N . viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy. 

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