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

Abstract

1. 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 populationlevel effects of disease. Snake fungal disease (SFD, ophidiomycosis), caused by the fungal pathogenOphidiomyces 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).3. 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 (CO 2 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°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 CO 2 production by free-ranging S. miliarius with SFD in winter. Natural infection byOo 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 CO 2 production rate by 58%-102%. 5. 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. | 487Functional Ecology AGUGLIARO et AL.

The metabolic response to an immune challenge in a viviparous snake, Sistrurus miliarius

“…In the current study, metabolism was measured at an ecologically relevant body temperature at or above temperatures associated with behavioral fever in snakes (Burns et al, 1996;Tetzlaff et al, 2017) and consistent with field body temperatures taken from summer-active S. miliarius in central Florida (May et al, 1996). In a study on the costs of coping with ophidiomycosis, afflicted S. miliarius exhibited elevated RMR compared with healthy individuals across three ecologically relevant temperatures (17, 25 and 32°C;Agugliaro et al, 2020). Snakes with ophidiomycosis exhibited a mean metabolic increment of 35% (45% at 17°C, 30% at 25°C, 30% at 32°C), demonstrating that coping costs are detectable across a broad range of body temperatures and potentially higher at lower temperatures.…”

“…Costs associated with immune performance are becoming increasingly appreciated as drivers of energetic tradeoffs (Demas et al, 2012;Downs et al, 2014;Lochmiller and Deerenberg, 2000), and recent studies implicate energetic costs of infection as a proximate mechanism contributing to the impacts of emergent pathogens on individuals and populations (e.g. Agugliaro et al, 2020;Mayack and Naug, 2009;Reeder et al, 2012;Wu et al, 2018). However, for many groups of organisms, immune-associated energetic costs have not been quantified, and the intrinsic and extrinsic factors that impact allocation priorities have not been identified.…”

Genetic mechanisms and biological processes underlying host response to ophidiomycosis (Snake Fungal Disease) inferred from tissue-specific transcriptome analyses

“…SFD studies in free ranging and captive snakes have documented behavioral and physiological changes in infected snakes such as lethargy (80) and higher metabolic rates (82). Much of SFD-related mortality is attributed to less frequent foraging and anorexia (30).…”

“…SFD studies in free ranging and captive snakes have documented behavioral and physiological changes in infected snakes such as lethargy ( 80) and higher metabolic rates (82).…”

Ophidiomycosis, an emerging fungal disease of snakes: Targeted surveillance on military lands and detection in the western US and Puerto Rico

“…Specifically, snakes with ophidiomycosis have shown a decrease in body condition with increasing severity of infection, but severity was not associated with recapture rate, and severely affected snakes apparently cleared infection [ 54 ]. It was also observed that the resting metabolic rate in this species was increased in ophidiomycosis-positive individuals, which may contribute to declining individual health during the disease process [ 55 ]. An increase in fetal mortality was observed following supplemental feeding of ophidiomycosis-positive gravid females [ 56 ], and a decrease in sex hormones in both positive males and females was observed, indicating subclinical reproductive effects from ophidiomycosis [ 57 ].…”