skip to main content


Title: Amphibian species vary in their learned avoidance response to the deadly fungal pathogen Batrachochytrium dendrobatidis
Abstract

Lethal and sublethal effects of pathogens should theoretically select for host avoidance of these pathogenic organisms. Some amphibians can learn to avoid the pathogenic fungusBatrachochytrium dendrobatidis(Bd) after one infection‐clearance event.

Here, we investigated whether four taxonomically distinct amphibians, Cuban tree frogsOsteopilus septentrionalis, southern toadsAnaxyrus(Bufo)terrestris, greenhouse frogsEleutherodactylus planirostrisand pine woods tree frogsHyla femoralis, exhibited any innate or learned avoidance of Bd on a moist substrate and, if so, what cues they used to identify the fungus.

Cuban tree frogs, pine woods tree frogs and greenhouse frogs did not appear to exhibit detectable innate or learned avoidance of Bd. However, southern toads learned to avoid Bd after only one exposure. Southern toads avoided any treatment containing Bd metabolites but did not avoid treatments that lacked Bd metabolites even when dead zoospores were present.

Bd metabolites appeared to be the cues that amphibians use to avoid Bd. These metabolites may have a distinct smell or may cause discomfort, which would be consistent with a classical or Pavlovian conditioning response.

Synthesis and applications. Not all species of amphibians respond the same way to Bd exposure; some can learn to avoid Bd and the metabolites it produces, while others do not. These findings have important implications for both management practices and policy, and should be considered when developing disease models and conservation plans for amphibians.

 
more » « less
Award ID(s):
1754862 2017785 1947573
NSF-PAR ID:
10446337
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Applied Ecology
Volume:
58
Issue:
8
ISSN:
0021-8901
Page Range / eLocation ID:
p. 1613-1620
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    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.

     
    more » « less
  2. The pathogenic fungusBatrachochytrium dendrobatidis(Bd)is associated with drastic global amphibian declines. Prophylactic exposure to killed zoospores and the soluble chemicals they produce (Bdmetabolites) can induce acquired resistance toBdin adult Cuban treefrogsOsteopilus septentrionalis. Here, we exposed metamorphic frogs of a second species, the Pacific chorus frogPseudacris regilla, to one of 2 prophylactic treatments prior to liveBdexposures: killedBdzoospores with metabolites, killed zoospores alone, or a water control. Prior exposure to killedBdzoospores with metabolites reducedBdinfection intensity in metamorphic Pacific chorus frogs by 60.4% compared to control frogs. Interestingly,Bdintensity in metamorphs previously exposed to killed zoospores alone did not differ in magnitude relative to the control metamorphs, nor to those treated with killed zoospores plus metabolites. Previous work indicated thatBdmetabolites alone can induce acquired resistance in tadpoles, and so these findings together indicate that it is possible that the solubleBdmetabolites may contain immunomodulatory components that drive this resistance phenotype. Our results expand the generality of this prophylaxis work by identifying a second amphibian species (Pacific chorus frog) and an additional amphibian life stage (metamorphic frog) that can acquire resistance toBdafter metabolite exposure. This work increases hopes that aBd-metabolite prophylaxis might be widely effective across amphibian species and life stages.

     
    more » « less
  3. Dillman, Adler R. (Ed.)

    Ivermectin is a broad-spectrum antiparasitic medicine, which is often used as a treatment for parasites or as a prophylaxis. While studies have looked at the long-term effects of Ivermectin on helminths, studies have not considered the long-term impacts of this treatment on host health or disease susceptibility. Here, we tracked the effects of early life Ivermectin treatment in Cuban tree frogs (Osteopilus septentrionalis) on growth rates, mortality, metabolically expensive organ size, and susceptibility toBatrachochytrium dendrobatidis(Bd) infection. One year after exposure, there was no effect of Ivermectin exposure on frog mass (X21= 0.904, p = 0.34), but when tracked through the exponential growth phase (~2.5 years) the Ivermectin exposed individuals had lower growth rates and were ultimately smaller (X21= 7.78,p= 0.005;X21= 5.36,p= 0.02, respectively). These results indicate that early life exposure is likely to have unintended impacts on organismal growth and potentially reproductive fitness. Additionally, we exposed frogs to Bd, a pathogenic fungus that has decimated amphibian populations globally, and found early life exposure to Ivermectin decreased disease susceptibility (disease load:X21= 17.57,p= 0.0002) and prevalence (control: 55%; Ivermectin: 22%) over 2 years after exposure. More research is needed to understand the underlying mechanism behind this phenomenon. Given that Ivermectin exposure altered disease susceptibility, proper controls should be implemented when utilizing this drug as an antiparasitic treatment in research studies.

     
    more » « less
  4. Abstract

    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.

     
    more » « less
  5. Abstract

    Batrachochytrium dendrobatidis(Bd) is a pathogenic fungus that has devastated amphibian populations globally by causing the disease chytridiomycosis.Batrachochytrium dendrobatidisis capable of infecting non‐amphibian hosts, such as crayfish, and has been detected on reptile and bird species. Given the taxonomic heterogeneity in the known hosts and vectors of Bd, it is likely that there is a diversity of undiscovered non‐amphibian hosts of the fungus.

    Here, we investigated whether Bd could survive on freshwater snails (Physella acuta) andCladophoraalgae. We exposed small and large snails (n = 15 snails/size category),Cladophoraalgae (n = 5), and artificial spring water controls (ASW;n = 5) to live Bd. We also maintained Bd‐free control snails (n = 5 snails/size category) in ASW. All treatments were maintained for 7 weeks at 18°C. Mortality was checked three times a week, snails were weighed every 2 weeks, and 7 weeks after exposure, the snails, algae, and water were tested for Bd using quantitative polymerase chain reaction.

    We found that Bd did not grow on live snails, algae, or ASW long term. Additionally, live snails (n = 20) collected from Bd‐positive ponds in California were all negative for Bd, as well. Given that we found no Bd on the experimentally exposed or field swabbed snails, snails are probably not a reservoir host of Bd.

    While negative results are often not published, Bd is one of the deadliest pathogens on earth; it is essential to know what is and is not capable of maintaining Bd for well‐designed disease models.

     
    more » « less