skip to main content


Title: Effects of latitudinal, seasonal, and daily temperature variations on chytrid fungal infections in a North American frog
Abstract

As human activities alter environmental conditions, the emergence and spread of disease represents an increasing threat to wildlife. Studies that examine how host–pathogen relationships play out across seasons and latitudes can serve as proxies for understanding how natural and anthropogenic changes in climate may influence infection and disease dynamics. Amphibians are ideal host organisms for studying the impacts of climate on disease because they are ectothermic and threatened by chytridiomycosis, a recently emerged and globally important disease caused by fungal pathogens in the genusBatrachochytrium. Previous studies suggest that temperature affects the interaction between amphibians andBatrachochytriumpathogens. However, a clearer understanding of this host–pathogen–environment interaction is needed to predict how the risk of chytridiomycosis will vary in space and time. Here, we investigate how daily, seasonal, and latitudinal variations in temperature affect the incidence and impact ofBatrachochytrium dendrobatidis(Bd) infection in a broadly distributed host, the northern cricket frog (Acris crepitans), using a combination of field and laboratory studies. In a four‐year field study conducted at three latitudes, we found that daily maximum air temperature over a 15‐d period prior to sampling best predicted patterns ofBdinfection and that the lightest infection loads followed periods when these temperatures exceeded 25°C. In a laboratory exposure experiment, we found pathogen load and mortality to be greater at temperatures that mimic winter temperatures at the southern extent of this host's range than for scenarios that mimic temperature conditions experienced in other areas and seasons. Taken together, our findings suggest that changes in temperature across timescales and latitudes interact to influence the dynamics of infection and disease in temperate amphibians.

 
more » « less
NSF-PAR ID:
10373130
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecosphere
Volume:
10
Issue:
11
ISSN:
2150-8925
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    To combat the loss of species due to emerging infectious diseases, scientists must incorporate ecological parameters, such as temperature and humidity, to understand how the environment affects host–pathogen interactions. The fungal disease chytridiomycosis is a compelling case study to investigate the role of both temperature and humidity on infectious disease, as both the fungal pathogen (Batrachochytrium dendrobatidis, Bd) and the host (amphibians) are heavily influenced by these abiotic factors. We performed two experiments to investigate the importance of relative humidity and temperature on frog immunity (production of antimicrobial skin secretions) and disease development in captive golden frogs (Atelopus zeteki) of Panama. We found that the quantity of skin secretions significantly decreased over time in frogs moved from low to medium and high relative humidity treatments. FollowingBdexposure, frogs in high temperature (26–27 °C) and high relative humidity (80–90%) had lower pathogen loads and survived significantly longer than frogs kept in all other treatment conditions, including high temperature and low relative humidity. These results suggest that high relative humidity may be an important, although less understood, mediator ofBdinfection and the survival of golden frogs. Because the environment can drastically alter disease dynamics, understanding how temperature and humidity influence chytridiomycosis outcomes in golden frogs may be essential for the success of the reintroduction of captive frogs.

     
    more » « less
  2. Abstract

    Life processes of ectothermic vertebrates are intimately linked to the temperature of their environment, influencing their metabolism, reproduction, behaviour and immune responses. In amphibians infected by the generalist chytrid pathogenBatrachochytrium dendrobatidis(Bd), host survival, infection prevalence and infection intensity are often temperature‐ and/or seasonally dependent. However, the transcriptional underpinnings of thermal differences in infection responses remain unknown. Measuring the impact of temperature on host responses to infection is a key component for understanding climatic influences on chytrid disease dynamics. TheBd‐responsive gene pathways in frogs are well documented, but our understanding of salamander immune expression profiles during infection with chytrids remains limited. Here we characterize the transcriptomic responses ofPlethodon cinereususing RNA sequencing by comparing skin and splenic gene expression of individuals uninfected, succumbing toBdinfection and naturally cleared ofBdinfection at three temperatures. We suggest that amphibian temperature‐dependent susceptibility toBdis probably driven by shifts in expression of the innate and adaptive immune axes. Our study shows increased expression of transcripts associated with inflammation at lower temperatures and a shift towards increased expression of adaptive immune genes, including MHC (major histocompatibility complex), at higher temperatures. In the face of climate change, and as concerns for the spread of emergent chytrid pathogens increase, our results provide important functional genomic resources to help understand how these pathogenic fungi may continue to affect amphibian communities globally in the future.

     
    more » « less
  3. Emerging infectious diseases have been especially devastating to amphibians, the most endangered class of vertebrates. For amphibians, the greatest disease threat is chytridiomycosis, caused by one of two chytridiomycete fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans ( Bsal ). Research over the last two decades has shown that susceptibility to this disease varies greatly with respect to a suite of host and pathogen factors such as phylogeny, geography (including abiotic factors), host community composition, and historical exposure to pathogens; yet, despite a growing body of research, a comprehensive understanding of global chytridiomycosis incidence remains elusive. In a large collaborative effort, Bd -Maps was launched in 2007 to increase multidisciplinary investigations and understanding using compiled global Bd occurrence data ( Bsal was not discovered until 2013). As its database functions aged and became unsustainable, we sought to address critical needs utilizing new technologies to meet the challenges of aggregating data to facilitate research on both Bd and Bsal . Here, we introduce an advanced central online repository to archive, aggregate, and share Bd and Bsal data collected from around the world. The Amphibian Disease Portal ( https://amphibiandisease.org ) addresses several critical community needs while also helping to build basic biological knowledge of chytridiomycosis. This portal could be useful for other amphibian diseases and could also be replicated for uses with other wildlife diseases. We show how the Amphibian Disease Portal provides: (1) a new repository for the legacy Bd- Maps data; (2) a repository for sample-level data to archive datasets and host published data with permanent DOIs; (3) a flexible framework to adapt to advances in field, laboratory, and informatics technologies; and (4) a global aggregation of Bd and Bsal infection data to enable and accelerate research and conservation. The new framework for this project is built using biodiversity informatics best practices and metadata standards to ensure scientific reproducibility and linkages across other biological and biodiversity repositories. 
    more » « less
  4. Abstract

    To combat the threat of emerging infectious diseases in wildlife, ecoimmunologists seek to understand the complex interactions among pathogens, their hosts, and their shared environments. The cutaneous fungal pathogen Batrachochytrium dendrobatidis (Bd), has led to the decline of innumerable amphibian species, including the Panamanian golden frog (Atelopus zeteki). Given that Bd can evade or dampen the acquired immune responses of some amphibians, nonspecific immune defenses are thought to be especially important for amphibian defenses against Bd. In particular, skin secretions constitute a vital component of amphibian innate immunity against skin infections, but their role in protecting A. zeteki from Bd is unknown. We investigated the importance of this innate immune component by reducing the skin secretions from A. zeteki and evaluating their effectiveness against Bd in vitro and in vivo. Following exposure to Bd in a controlled inoculation experiment, we compared key disease characteristics (e.g., changes in body condition, prevalence, pathogen loads, and survival) among groups of frogs that had their skin secretions reduced and control frogs that maintained their skin secretions. Surprisingly, we found that the skin secretions collected from A. zeteki increased Bd growth in vitro. This finding was further supported by infection and survival patterns in the in vivo experiment where frogs with reduced skin secretions tended to have lower pathogen loads and survive longer compared to frogs that maintained their secretions. These results suggest that the skin secretions of A. zeteki are not only ineffective at inhibiting Bd but may enhance Bd growth, possibly leading to greater severity of disease and higher mortality in this highly vulnerable species. These results differ from those of previous studies in other amphibian host species that suggest that skin secretions are a key defense in protecting amphibians from developing severe chytridiomycosis. Therefore, we suggest that the importance of immune components cannot be generalized across all amphibian species or over time. Moreover, the finding that skin secretions may be enhancing Bd growth emphasizes the importance of investigating these immune components in detail, especially for species that are a conservation priority.

     
    more » « less
  5. Abstract

    Numerous species of amphibians declined in Central America during the 1980s and 1990s. These declines mostly affected highland stream amphibians and have been primarily linked to chytridiomycosis, a deadly disease caused by the chytrid fungusBatrachochytrium dendrobatidis(Bd). Since then, the majority of field studies on Bd in the Tropics have been conducted in midland and highland environments (>800 m) mainly because the environmental conditions of mountain ranges match the range of ideal abiotic conditions for Bd in the laboratory. This unbalanced sampling has led researchers to largely overlook host–pathogen dynamics in lowlands, where other amphibian species declined during the same period. We conducted a survey testing for Bd in 47 species (n = 348) in four lowland sites in Costa Rica to identify local host–pathogen dynamics and to describe the abiotic environment of these sites. We detected Bd in three sampling sites and 70% of the surveyed species. We found evidence that lowland study sites exhibit enzootic dynamics with low infection intensity and moderate to high prevalence (55% overall prevalence). Additionally, we found evidence that every study site represents an independent climatic zone, where local climatic differences may explain variations in Bd disease dynamics. We recommend more detection surveys across lowlands and other sites that have been historically considered unsuitable for Bd occurrence. These data can be used to identify sites for potential disease outbreaks and amphibian rediscoveries.

     
    more » « less