Exposure to Batrachochytrium dendrobatidis affects chemical defences in two anuran amphibians, Rana dalmatina and Bufo bufo

János Ujszegi,Dániel Krüzselyi,Attila Hettyey,Krisztina Ludányi,Márk Z. Németh,Trenton W. J. Garner,László Drahos,Tamás Drexler,Ágnes M. Móricz,Judit Vörös

doi:10.1186/s12862-021-01867-w

Abstract

BackgroundBatrachochytrium dendrobatidis (Bd) is the causative agent of chytridiomycosis, one of the major causes of worldwide amphibian biodiversity loss. Many amphibians exhibit skin-based chemical defences, which may play an important role against invading pathogens, but whether the synthesis of these chemical compounds is enhanced or suppressed in the presence of pathogens is largely unknown. Here we investigated direct and indirect effects of larval exposure to the globally distributed and highly virulent Bd-GPL strain on skin secreted chemical defences and life history traits during early ontogeny of agile frogs (Rana dalmatina) and common toads (Bufo bufo).ResultsExposure to Bd during the larval stage did not result in enhanced synthesis of the antimicrobial peptide Brevinin-1 Da in R. dalmatina tadpoles or in increased production of bufadienolides in B. bufo tadpoles. However, exposure to Bd during the larval stage had a carry-over effect reaching beyond metamorphosis: both R. dalmatina and B. bufo froglets contained smaller quantities of defensive chemicals than their Bd-naïve conspecifics in the control treatment. Prevalence of Bd and infection intensities were very low in both larvae and metamorphs of R. dalmatina, while in B. bufo we observed high Bd prevalence and infection intensities, especially in metamorphs. At the same time, we did not find a significant effect of Bd-exposure on body mass or development rate in larvae or metamorphs in either species.ConclusionsThe lack of detrimental effect of Bd-exposure on life history traits, even parallel with high infection intensities in the case of B. bufo individuals, is surprising and suggests high tolerance of local populations of these two species against Bd. However, the lowered quantity of defensive chemicals may compromise antimicrobial and antipredatory defences of froglets, which may ultimately contribute to population declines also in the absence of conspicuous mass-mortality events.

Highlights

Batrachochytrium dendrobatidis (Bd) is the causative agent of chytridiomycosis, one of the major causes of worldwide amphibian biodiversity loss
Treatment had no effect on the relative amount of Brevinin-1 Da in pooled samples of tadpoles (GLM: F2,15 = 2.31, P = 0.13; Fig. 2A)
Bd-exposure during the larval stage negatively affected chemical defences in metamorphosed individuals of both species. These results suggest that neither larvae nor freshly metamorphosed individuals respond to Bd-exposure with enhanced synthesis of antimicrobial chemicals, and that infection during the larval stage may rather carries costs that manifest in decreased quantities of chemical defences in metamorphs

Summary

Introduction

Batrachochytrium dendrobatidis (Bd) is the causative agent of chytridiomycosis, one of the major causes of worldwide amphibian biodiversity loss. There may be no single main cause of declines [3], diseases caused by infection with viral, bacterial or fungal agents are clearly among the most devastating factors [4,5,6]. Chytridiomycosis, a disease affecting amphibians, is caused by the chytrid fungi Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) [10]. Bd infects keratinous epidermal layers of the skin [15] and impairs its osmoregulatory function. This effect can cause shifts in electrolyte balance leading to cardiac asystolic death in juveniles and adults [16]. Tadpoles exhibit keratinous elements only in their mouthparts, so that they are less susceptible to Bd infection than later life-stages [17, 18], and can act as reservoirs in natural habitats [19,20,21]

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