Novel findings on the impact of chytridiomycosis on the cardiac function of anurans: sensitive vs. tolerant species

Abstract

BackgroundUnderstanding of the physiological effects of chytridiomycosis is crucial to worldwide amphibian conservation. Therefore, we analyzed the cardiac function of two anuran species (Xenopus laevis and Physalaemus albonotatus) with different susceptibilities to infection by the causative agent of chytridiomycosis, Batrachochytrium dendrobatidis (hereafter Bd).MethodsWe analyzed the in situ heart rate (fH - bpm), relative ventricular mass (RVM -%), and Ca2+ handling in heart of Bd infected animals compared to uninfected controls of both study species.ResultsBd infection resulted in a 78% decrease in contraction force values in P. albonotatus when compared to the less susceptible X. laevis. This negative effect was even more evident (82%) for the cardiac pumping capacity. The time to reach peak tension was 125% longer in P. albonotatus than in X. laevis, and cardiac relaxation was 57% longer.DiscussionThese results indicate a delay in the cardiac cycle of P. albonotatus on a beat-to-beat basis, which was corroborated by the bradycardia observed in situ. In summary, Bd-sensitive species present impaired cardiac function, which could be a factor in mortality risk. The more pronounced effects of Bd in P. albonotatus may not only result from electrolyte imbalance, as previously reported, but also could be an effect of toxins produced by Bd. For X. laevis, the ability to promote cardiac adjustments seems to be an important homeostatic feature that allows greater tolerance to chytridiomycosis. This study provides new physiological mechanisms underlying the tolerance or susceptibility of amphibian species to chytridiomycosis, which determine their adaptability to survive in the affected environments.

Habitat split as a driver of disease in amphibians

“…In one example, reduced water availability under cool temperatures or droughts caused rainforest frogs to clump together, and this change in behaviour increased mortality from chytridiomycosis (Longo, Burrowes & Joglar, 2010). Given that chytridiomycosis causes water and ion balance disruption (Voyles et al, 2007), leads to substantial increases in water loss rate (Russo et al, 2018), puts stress on cardiac function (Salla et al, 2018), and can also stimulate an increase in corticosterone levels (Fig. S5A; Gabor, Fisher & Bosch, 2013; but see Hammond et al, 2020), the potential for synergy between chytridiomycosis and additional dehydration stress imposed by migratory behaviour through disturbed matrix habitats is an important direction for future research in landscapes with high levels of habitat split (Moura-Campos et al, 2021).…”

Pathogen load predicts host functional disruption: A meta‐analysis of an amphibian fungal panzootic

“…To demonstrate the relationship between infection intensity and functional disruption across species using meta‐analytic approaches, amphibians and the chytrid fungus pathogen provide an ideal case model, due to the number of experimental studies testing the effects of chytrid exposure on sublethal responses relating to behaviour, physiology and reproduction across multiple species (Brannelly, Webb, et al, 2021; Fisher et al, 2021; Ohmer et al, 2017; Salla et al, 2018). Chytridiomycosis is a cutaneous disease caused by the fungal pathogen Batrachochytrium dendrobatidis ( Bd ) and Batrachochytrium salamandrivorans ( Bsal ).…”

The role of sloughing on the pathophysiology of chytridiomycosis in amphibians

“…The water retention results in osmotic dilution in the surrounding cavity system, which in excess can cause an increase in water muscle content and a decrease in plasma osmolality, as observed in infected frogs in this study. Impairment of skin function in relation to water balance can therefore lead to disruption of the blood volume, capillary filtration, lymphatic function (Hillman et al, 2004), and ultimately cardiovascular homeostasis as seen Bd-infected animals (Voyles et al, 2009;Salla et al, 2018).…”

“…The disruption of kidney function may also alter blood pressure and flow that may in turn affect cardiac output causing arrhythmia (Guyton, 1991;Sarnak et al, 2003). There is evidence of decreased contractile force and increased cardiac relaxation from frogs infected with Bd (Salla et al, 2018). How Bd causes this internal damage remains to be tested.…”