Abstract
Recent global declines, extirpations and extinctions of wildlife caused by newly emergent diseases highlight the need to improve our knowledge of common environmental factors that affect the strength of immune defense traits. To achieve this goal, we examined the influence of acidification and shading of the larval environment on amphibian skin-associated innate immune defense traits, pre and post-metamorphosis, across two populations of American Bullfrogs (Rana catesbeiana), a species known for its wide-ranging environmental tolerance and introduced global distribution. We assessed treatment effects on 1) skin-associated microbial communities and 2) post-metamorphic antimicrobial peptide (AMP) production and 3) AMP bioactivity against the fungal pathogen Batrachochytrium dendrobatidis (Bd). While habitat acidification did not affect survival, time to metamorphosis or juvenile mass, we found that a change in average pH from 7 to 6 caused a significant shift in the larval skin microbial community, an effect which disappeared after metamorphosis. Additionally, we found shifts in skin-associated microbial communities across life stages suggesting they are affected by the physiological or ecological changes associated with amphibian metamorphosis. Moreover, we found that post-metamorphic AMP production and bioactivity were significantly affected by the interactions between pH and shade treatments and interactive effects differed across populations. In contrast, there were no significant interactions between treatments on post-metamorphic microbial community structure suggesting that variation in AMPs did not affect microbial community structure within our study. Our findings indicate that commonly encountered variation in the larval environment (i.e. pond pH and degree of shading) can have both immediate and long-term effects on the amphibian innate immune defense traits. Our work suggests that the susceptibility of amphibians to emerging diseases could be related to variability in the larval environment and calls for research into the relative influence of potentially less benign anthropogenic environmental changes on innate immune defense traits.
Highlights
It is well accepted that phenotypes vary between populations and are influenced by environmental conditions, there is increasing interest in the effects of environmental change on traits that affect resistance to newly emerging pathogens [1,2,3]
Many of the diseases associated with amphibian declines either enter the amphibian through the dermal tissue, or directly affect the dermal tissue [14,15,16]
Antimicrobial peptides (AMPs) produced by the granular glands of amphibian skin provide an effective defense against a variety of pathogens by disrupting pathogen cell and viral membranes [24,25,26]
Summary
It is well accepted that phenotypes vary between populations and are influenced by environmental conditions, there is increasing interest in the effects of environmental change on traits that affect resistance to newly emerging pathogens [1,2,3]. Relatively few studies have experimentally examined the effects of environmental change on immune defense traits, which may greatly affect individual health [10,11,12, 13]. Some amphibian skin-associated microbial species produce metabolites that suppress and eliminate some amphibian diseases [18,19,20,21,22,23]. How changes in the environment affect skin-associated microbial communities and AMPs has not been widely examined [27]
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