An emerging fungal pathogen is associated with increased resting metabolic rate and total evaporative water loss rate in a winter-active snake

Energy allocation trade-offs associated with mounting metabolically costly immune responses may serve as sublethal mechanisms by which pathogens reduce host fitness. The emergence of cutaneous fungal pathogens, which invade the skin of their host and have the potential to disturb energy and water balance, highlight the importance of host physiology in determining individual- and population-level effects of disease. Snake fungal disease (SFD, ophidiomycosis), caused by the fungal pathogen Ophidiomyces ophiodiicola (Oo), is an emerging disease afflicting wild snake populations throughout eastern North America. Emaciation and dehydration are phenotypic correlates of SFD, but it is unknown if such declines in host condition occur via effects of Oo infection on host physiology (i.e. increased rates of metabolism and evaporative water loss respectively). We used flow-through respirometry to assess the energetic and hydric consequences of natural Oo infection in winter-active pygmy rattlesnakes Sistrurus miliarius. We measured resting metabolic rate (CO2 production rate) and total evaporative water loss rate of winter-acclimatized S. miliarius as a function of SFD status and acute temperature (17, 25 and 32 degrees C). We also used regression models characterizing individual variation in the thermal-sensitivity of resting metabolic rate to predict the theoretical effects of behavioural fever on daily resting CO2 production by free-ranging S. miliarius with SFD in winter. Natural infection by Oo was associated with significant increases in resting metabolic rate (30%-45%) and total evaporative water loss rate (30%-40%) across all measurement temperatures. Under simulated scenarios of behavioural fever, Oo infection was predicted to increase daily resting CO2 production rate by 58%-102%. Our results are consistent with the hypothesis that the immune response to Oo infection is energetically costly and may contribute to declining host condition. Our modelling efforts combining the cumulative effects of increased immune activity and increased body temperature on metabolism represent a novel approach in quantifying the total daily energetic cost of infection in ectothermic vertebrates undergoing behavioural fever. A free Plain Language Summary can be found within the Supporting Information of this article.