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Terence M. Farrell

Publications and source records attributed to Terence M. Farrell.

7 recordsLinked to original sources

Glucocorticoid and glycemic responses to immune challenge in a viviparous snake afflicted with an emerging mycosis

Disease may be both a cause and consequence of stress, and physiological responses to infectious disease may involve stress coping mechanisms that have important fitness consequences. For example, glucocorticoid and glycemic responses may affect host fitness by altering resource allocation and use in hosts, and these responses may be affected by competing stressors. To better understand the factors that affect host responses to infection, we challenged the immune system of field acclimatized pygmy rattlesnakes, Sistrurus miliarius , with a sterile antigen, lipopolysaccharide (LPS), and measured the glucocorticoid and glycemic response in healthy non-reproductive snakes, snakes afflicted with an emerging mycosis (ophidiomycosis), and pregnant snakes. We hypothesized that LPS challenge would result in a glucocorticoid and glycemic response typical of the vertebrate acute phase response (APR), and therefore predicted that LPS challenge would result in an acute increase in plasma corticosterone (CORT) and a decline in plasma glucose in all individuals. Additionally, we hypothesized that the APR would be attenuated in individuals simultaneously coping with additional challenges to homeostasis (i.e., disease or reproduction). As predicted, immune challenge elicited an acute increase in plasma CORT and a decrease in plasma glucose. Snakes coping with ophidiomycosis and pregnant snakes were able to mount a robust glucocorticoid and hypoglycemic response to LPS challenge, which was contrary to our hypothesis. Our findings clarify directions of causality linking infection, glucocorticoids, and glucose, and emphasize the importance of future research examining the fitness consequences of interactions between stress and disease in wildlife threatened by emerging pathogens.

Journal of Experimental Biology

The population genetics of the causative agent of snake fungal disease indicate recent introductions to the USA

Snake fungal disease (SFD; ophidiomycosis), caused by the pathogen Ophidiomyces ophiodiicola ( Oo ), has been documented in wild snakes in North America and Eurasia, and is considered an emerging disease in the eastern United States of America. However, a lack of historical disease data has made it challenging to determine whether Oo is a recent arrival to the USA or whether SFD emergence is due to other factors. Here, we examined the genomes of 82 Oo strains to determine the pathogen’s history in the eastern USA. Oo strains from the USA formed a clade (Clade II) distinct from European strains (Clade I), and molecular dating indicated that these clades diverged too recently (approximately 2,000 years ago) for transcontinental dispersal of Oo to have occurred via natural snake movements across Beringia. A lack of nonrecombinant intermediates between clonal lineages in Clade II indicates that Oo has actually been introduced multiple times to North America from an unsampled source population, and molecular dating indicates that several of these introductions occurred within the last few hundred years. Molecular dating also indicated that the most common Clade II clonal lineages have expanded recently in the USA, with time of most recent common ancestor mean estimates ranging from 1985 to 2007 CE. The presence of Clade II in captive snakes worldwide demonstrates a potential mechanism of introduction and highlights that additional incursions are likely unless action is taken to reduce the risk of pathogen translocation and spillover into wild snake populations.

PLoS Biology

Interactive effects of food supplementation and snake fungal disease on pregnant Pygmy Rattlesnakes and their offspring

In viviparous organisms, the ability to feed while pregnant may mitigate energetic trade-offs experienced during the reproductive process and enhance fecundity. However, anorexia during pregnancy has been reported in many crotaline snakes. The potential costs and benefits of feeding while pregnant are not completely described in the literature, and experimental studies have been conducted in a limited number of taxa, rendering our understanding of the forces that may underlie the evolution of anorexia in pregnant snakes incomplete. Here, we examine the impact of food supplementation during mid to late pregnancy on mothers and offspring in a viviparous crotaline snake species, the Pygmy Rattlesnake ( Sistrurus miliarius ). Specifically, we offered multiple large meals to mothers held in outdoor enclosures and measured a suite of maternal and offspring traits including maternal body condition, offspring length and mass, maternal disease state, and offspring foraging behaviors. We focused on interactions between feeding, clinical signs of snake fungal disease (SFD), and the presence of its causative agent, Ophidiomyces ophiodiicola , in mothers. Pregnant females fed readily when offered food, but feeding did not impact offspring traits. Food supplementation significantly increased maternal postparturient body condition, but also increased clinical signs of disease in mothers and led to a significantly higher reproductive failure rate in the treatment group, particularly in mothers afflicted with SFD. Our results suggest that food supplementation during pregnancy may disrupt the reproductive process in pregnant rattlesnakes, and that such disruption is particularly pronounced in mothers suffering from SFD.

Journal of Herpetology

Evidence of vertical transmission of the snake fungal pathogen Ophidiomyces ophiodiicola

Snake fungal disease (ophidiomycosis) is an emerging infection of snakes caused by Ophidiomyces ophiodiicola . Little is known about mechanisms of this pathogen's transmission and its implications for conservation of wild snake populations. We report four cases with evidence of vertical transmission of O. ophiodiicola from dam to offspring.

Journal of Wildlife Diseases

Seasonal sex steroids indicate reproductive costs associated with snake fungal disease

Emergent diseases may result in population declines by inducing mortality directly or through sublethal effects on host reproduction. Snake fungal disease (SFD) is an emerging threat to biodiversity, but the sublethal impacts of disease on host fitness are poorly characterized in snakes. The cryptic nature of most snakes makes direct assessment of the fitness consequences of SFD challenging. In such contexts, measurement sex steroids that correlate positively with seasonal reproductive investment may be useful in inferring the scope of disease impacts. To test the hypothesis that SFD is associated with reproductive suppression, we measured testosterone and estradiol in free-ranging pygmy rattlesnakes with varying clinical signs of SFD. We also used real-time PCR to validate the relationship between clinical signs and Ophidiomyces ophiodiicola (Oo) DNA presence on the skin. Infected males had lower testosterone compared to uninfected males during summer spermatogenesis and the fall breeding season. Infected females were less likely to have elevated estradiol compared to uninfected females during spring vitellogenesis. Approximately 85% of individuals with clinical signs were Oo DNA positive. Our findings are consistent with the hypothesis that coping with SFD comes at a cost to the reproductive success of afflicted individuals, and that seasonal sex steroids may be valuable early indicators of sublethal effects.

Journal of Zoology

Patterns of circulating corticosterone in a population of rattlesnakes afflicted with snake fungal disease: Stress hormones as a potential mediator of seasonal cycles in disease severity and outcomes

Snake fungal disease (SFD) is an emerging threat to snake populations in the United States. Fungal pathogens are often associated with a physiological stress response mediated by the hypothalamo-pituitary-adrenal axis (HPA), and afflicted individuals may incur steep coping costs. The severity of SFD can vary seasonally; however, little is known regarding (1) how SFD infection relates to HPA activity and (2) how seasonal shifts in environment, life history, or HPA activity may interact to drive seasonal patterns of infection severity and outcomes. To test the hypothesis that SFD is associated with increased HPA activity and to identify potential environmental or physiological drivers of seasonal infection, we monitored baseline corticosterone, SFD infection severity, foraging success, body condition, and reproductive status in a field-active population of pigmy rattlesnakes. Both plasma corticosterone and the severity of clinical signs of SFD peaked in the winter. Corticosterone levels were also elevated in the fall before the seasonal rise in SFD severity. Severely symptomatic snakes were in low body condition and had elevated corticosterone levels compared to moderately infected and uninfected snakes. The monthly mean severity of SFD in the population was negatively related to population-wide estimates of body condition and temperature measured in the precedent month and positively correlated with corticosterone levels measured in the precedent month. Symptomatic females were less likely to enter reproductive bouts compared to asymptomatic females. We propose the hypothesis that the seasonal interplay among environment, host energetics, and HPA activity initiates trade-offs in the fall that drive the increase in SFD prevalence, symptom severity, and decline in condition observed in the population through winter.

Physiological and Biochemical Zoology

Snake fungal disease: An emerging threat to wild snakes

Since 2006, there has been a marked increase in the number of reports of severe and often fatal fungal skin infections in wild snakes in the eastern USA. The emerging condition, referred to as snake fungal disease (SFD), was initially documented in rattlesnakes, where the infections were believed to pose a risk to the viability of affected populations. The disease is caused by Ophidiomyces ophiodiicola , a fungus recently split from a complex of fungi long referred to as the Chrysosporium anamorph of Nannizziopsis vriesii (CANV). Here we review the current state of knowledge about O. ophiodiicola and SFD. In addition, we provide original findings which demonstrate that O. ophiodiicola is widely distributed in eastern North America, has a broad host range, is the predominant cause of fungal skin infections in wild snakes and often causes mild infections in snakes emerging from hibernation. This new information, together with what is already available in the scientific literature, advances our knowledge of the cause, pathogenesis and ecology of SFD. However, additional research is necessary to elucidate the factors driving the emergence of this disease and develop strategies to mitigate its impacts.

Philosophical Transactions of the Royal Society B: