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1. Metabolites from the fungal pathogen Batrachochytrium dendrobatidis (bd) reduce Bd load in Cuban treefrog tadpoles

   https://doi.org/10.1111/1365-2664.14242  

   Nordheim, Caitlin L. ; Detmering, Sarah E. ; Civitello, David J. ; Johnson, Pieter T. J. ; Rohr, Jason R. ; McMahon, Taegan A. ( June 2022 , Journal of Applied Ecology)

   Batrachochytrium dendrobatidis(Bd) has been associated with massive amphibian population declines worldwide. Wildlife vaccination campaigns have proven effective for mitigating damage from other pathogens, and there is evidence that adult frogs can acquire resistance to Bd when exposed to killed Bd zoospores and the metabolites they produced.

   Here, we investigated whether Cuban treefrogs tadpolesOsteopilus septentrionaliscan gain protection from Bd through exposure to a prophylaxis treatment composed of killed zoospores or soluble Bd metabolites. We used a 2 × 2 factorial design, crossing the presence or absence of killed zoospores with the presence or absence of Bd metabolites. All hosts were subsequently exposed to live Bd to evaluate susceptibility.

   Exposure to killed zoospores did not induce a protective response. However, tadpoles exposed to Bd metabolites had significantly lower Bd intensity and prevalence than tadpoles that were not exposed to metabolites.

   The metabolites Bd produce pose no risk of Bd infection and therefore make an epidemiologically safe prophylaxis treatment, protecting tadpoles against Bd. This work provides a promising potential for protecting amphibians in the wild as a disease management strategy for controlling Bd‐associated declines.

    

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2. Variability in environmental persistence but not per capita transmission rates of the amphibian chytrid fungus leads to differences in host infection prevalence

   https://doi.org/10.1111/1365-2656.13612  

   Rumschlag, Samantha L. ; Roth, Sadie A. ; McMahon, Taegan A. ; Rohr, Jason R. ; Civitello, David J. ( November 2021 , Journal of Animal Ecology)

   Heterogeneities in infections among host populations may arise through differences in environmental conditions through two mechanisms. First, environmental conditions may alter host exposure to pathogens via effects on survival. Second, environmental conditions may alter host susceptibility, making infection more or less likely if contact between a host and pathogen occurs. Further, host susceptibility might be altered through acquired resistance, which hosts can develop, in some systems, through exposure to dead or decaying pathogens and their metabolites. Environmental conditions may alter the rates of pathogen decomposition, influencing the likelihood of hosts developing acquired resistance.

   The present study primarily tests how environmental context influences the relative contributions of pathogen survival and per capita transmission on host infection prevalence using the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) as a model system. Secondarily, we evaluate how environmental context influences the decomposition of Bd because previous studies have shown that dead Bd and its metabolites can illicit acquired resistance in hosts. We conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition and per capita transmission rates vary among water sources [e.g. artificial spring water (ASW) or water from three ponds].

   We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd, rather than differences in per capita transmission rates. Bd mortality rates varied among pond water treatments and were lower in ASW compared to pond water.

   These results suggest that variation in Bd infection dynamics could be a function of environmental factors in waterbodies that result in differences in exposure of hosts to live Bd. In contrast to the persistence of live Bd, we found that the rates of decomposition of dead Bd did not vary among water sources, which may suggest that exposure of hosts to dead Bd or its metabolites might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the environmental dependence of free‐living pathogens could lead to a deeper understanding of the patterns of outbreak heterogeneity, which could inform surveillance and management strategies.

    

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3. Preparatory immunity: Seasonality of mucosal skin defences and Batrachochytrium infections in Southern leopard frogs

   https://doi.org/10.1111/1365-2656.13386  

   Le Sage, Emily H. ; LaBumbard, Brandon C. ; Reinert, Laura K. ; Miller, Brian T. ; Richards‐Zawacki, Corinne L. ; Woodhams, Doug C. ; Rollins‐Smith, Louise A. ; Bielby, ed., Jon ( November 2020 , Journal of Animal Ecology)

   Accurately predicting the impacts of climate change on wildlife health requires a deeper understanding of seasonal rhythms in host–pathogen interactions. The amphibian pathogen,Batrachochytrium dendrobatidis(Bd), exhibits seasonality in incidence; however, the role that biological rhythms in host defences play in defining this pattern remains largely unknown.

   The aim of this study was to examine whether host immune and microbiome defences againstBdcorrespond with infection risk and seasonal fluctuations in temperature and humidity.

   Over the course of a year, five populations of Southern leopard frogs (Rana[Lithobates]sphenocephala) in Tennessee, United States, were surveyed for host immunity, microbiome and pathogen dynamics. Frogs were swabbed for pathogen load and skin bacterial diversity and stimulated to release stored antimicrobial peptides (AMPs). Secretions were analysed to estimate total hydrophobic peptide concentrations, presence of known AMPs and effectiveness ofBdgrowth inhibition in vitro. The diversity and proportion of bacterial reads with a 99% match to sequences of isolates known to inhibitBdgrowth in vitro were used as an estimate of predicted anti‐Bdfunction of the skin microbiome.

   Batrachochytrium dendrobatidisdynamics followed the expected seasonal fluctuations—peaks in cooler months—which coincided with when host mucosal defences were most potent againstBd. Specifically, the concentration and expression of stored AMPs cycled synchronously withBddynamics. Although microbiome changes followed more linear trends over time, the proportion of bacteria that can function to inhibitBdgrowth was greatest when risk ofBdinfection was highest.

   We interpret the increase in peptide storage in the fall and the shift to a more anti‐Bdmicrobiome over winter as a preparatory response for subsequent infection risk during the colder periods when AMP synthesis and bacterial growth is slow and pathogen pressure from this cool‐adapted fungus is high. Given that a decrease in stored AMP concentrations as temperatures warm in spring likely means greater secretion rates, the subsequent decrease in prevalence suggests seasonality ofBdin this host may be in part regulated by annual immune rhythms, and dominated by the effects of temperature.

    

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4. Impacts of thermal mismatches on chytrid fungus Batrachochytrium dendrobatidis prevalence are moderated by life stage, body size, elevation and latitude

   https://doi.org/10.1111/ele.13239  

   Cohen, Jeremy M. ; McMahon, Taegan A. ; Ramsay, Chloe ; Roznik, Elizabeth A. ; Sauer, Erin L. ; Bessler, Scott ; Civitello, David J. ; Delius, Bryan K. ; Halstead, Neal ; Knutie, Sarah A. ; et al ( February 2019 , Ecology Letters)

   Global climate change is increasing the frequency of unpredictable weather conditions; however, it remains unclear how species‐level and geographic factors, including body size and latitude, moderate impacts of unusually warm or cool temperatures on disease. Because larger and lower‐latitude hosts generally have slower acclimation times than smaller and higher‐latitude hosts, we hypothesised that their disease susceptibility increases under ‘thermal mismatches’ or differences between baseline climate and the temperature during surveying for disease. Here, we examined how thermal mismatches interact with body size, life stage, habitat, latitude, elevation, phylogeny and International Union for Conservation of Nature (IUCN) conservation status to predict infection prevalence of the chytrid fungusBatrachochytrium dendrobatidis(Bd) in a global analysis of 32 291 amphibian hosts. As hypothesised, we found that the susceptibility of larger hosts and hosts from lower latitudes toBdwas influenced by thermal mismatches. Furthermore, hosts of conservation concern were more susceptible than others following thermal mismatches, suggesting that thermal mismatches might have contributed to recent amphibian declines.

    

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5. Batrachochytrium dendrobatidis (Bd) exposure damages gill tissue and inhibits crayfish respiration

   https://doi.org/10.3354/dao03623  

   Nordheim, CL ; Grim, JM ; McMahon, TA ( October 2021 , Diseases of Aquatic Organisms)

   Batrachochytrium dendrobatidis(Bd) is a pathogenic fungus known to infect amphibians and crayfish. In crayfish,Bdcauses gill tissue damage, and in some cases, mortality. Most research has focused on the amphibian-Bdsystem, so to date, little is known about the effects ofBdon the crayfish host. Here, we studied the effects of sublethal exposure toBdand the metabolites produced byBdon crayfishProcambarus allenisurvival, gill damage, and oxygen consumption (as a proxy for mass-specific metabolic rate). Oxygen consumption increased 24 h post-exposure to liveBd, indicative of a stress response, followed by a decrease in oxygen consumption over time (χ²₁= 6.39, p = 0.012). There was no difference in response when comparing the crayfish exposure to liveBdandBd-metabolites alone (χ²₁= 2.70, p = 0.101), indicating that the metabolites may have been the causative agent responsible for the response. Additionally, oxygen consumption decreased with gill damage (tissue recession) inBd-exposed individuals. We found that high doses ofBdcause outright mortality in crayfish, and we show here that sublethalBd-induced inhibition of oxygen consumption could negatively impact crayfish in the field, possibly reducing their overall fitness. More research is needed to understand this understudied host-parasite system. It is essential that we incorporate the disease dynamics associated withBdand crayfish in conservation disease models, as this is the only way to develop comprehensive community-based models.

    

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