Interaction between temperature and sublethal infection with the amphibian chytrid fungus impacts a susceptible frog species

Lachlan Campbell,John Clulow,Michael Mahony,Michelle Stockwell,Deborah S Bower,Simon Clulow

doi:10.1038/s41598-018-35874-7

Abstract

The amphibian chytrid fungus Batrachochytrium dendrobatidis is an emerging infectious pathogen present on every continent except Antarctica. It causes the disease chytridiomycosis in a subset of species but does not always result in disease or death for every host. Ambient temperature influences both amphibian metabolism and chytrid pathogenicity, however the interactive effects on host physiology is not well understood. We investigated the sublethal effect of B. dendrobatidis infection on a susceptible host, Litoria aurea to test (1) whether the infection load, metabolic activity, body fat and gonad size differed in L. aurea at either 24 °C or 12 °C ambient temperatures and (2) whether previous Bd infection caused long-term changes to body fat and gonad size. Litoria aurea in 12 °C treatments had higher infection loads of B. dendrobatidis and lower survivorship. Metabolic rate was higher and fat mass was lower in infected individuals and in animals in 24 °C treatments. Male L. aurea previously infected with B. dendrobatidis had smaller testes 5 months-post clearance of infection, an effect likely to translate to fitness costs in wild populations. These experiments demonstrate a physiological cost to sublethal B. dendrobatidis infection, which suggests a reduction in host fitness mediated by temperature in the host’s environment regardless of whether infection leads to mortality.

Highlights

Chronic sublethal infections can cause a range of deleterious impacts in the host[1], placing a substantial and often unpredictable stress on host fitness[2]
We aimed to test (1) whether the infection load, metabolic activity, and fat storage differed between L. aurea at high (24 °C) and low (12 °C) ambient temperatures following infection with B. dendrobatidis and (2) whether body fat and gonad size differed in frogs previously infected, but subsequently cleared of infection
Temperature significantly affected the growth of B. dendrobatidis; infection loads were much higher in infected frogs at 12 °C than 24 °C (F = 22.28, df = 1, P = 0.001; Fig. 1a)

Summary

Introduction

Chronic sublethal infections can cause a range of deleterious impacts in the host[1], placing a substantial and often unpredictable stress on host fitness[2]. Hosts exhibit costly defence responses against parasites, including complex immune systems, behavioural and chemosensory driven avoidance, fever responses and terminal investment strategies to increase fitness[7] These complex interactions in species susceptible to emerging infectious diseases will be better understood by first understanding the key driving mechanisms in which pathogens directly affect their host. Previous studies on sublethal impacts of Batrachochytrium dendrobatidis infection have demonstrated lower respiration rate[12], reduced body mass[26,27] and locomotion metrics[28] and retarded growth rates[29,30] Reproductive metrics such as calling activity may increase in infected individuals[31] while call frequency remains unchanged[32]. We aimed to test (1) whether the infection load, metabolic activity, and fat storage differed between L. aurea at high (24 °C) and low (12 °C) ambient temperatures following infection with B. dendrobatidis and (2) whether body fat and gonad size differed in frogs previously infected, but subsequently cleared of infection

Objectives

Methods

Results

Conclusion