Geographic variation and within-individual correlations of physiological stress markers in a widespread reptile, the common garter snake (Thamnophis sirtalis)

Abstract

Characterizing the baseline and stress-induced hormonal, metabolite, and immune profiles of wild animals is important to assess the impacts of variable environments, including human-induced landscape changes, on organismal health. Additionally, the extent to which these profiles are coordinated across physiological systems within individuals remains an important question in understanding how stressors can differentially affect aspects of an individual's physiology. Here, we present data from wild populations of the common garter snake (Thamnophis sirtalis) on both baseline and stress-induced biomarkers: plasma corticosterone (CORT) concentration, plasma glucose concentration, and whole blood heterophil:lymphocyte ratio. Using a standardized restraint protocol with individuals from populations in disparate portions of this species' range - the Sierra Nevada Mountains of California and the plains of Iowa - we collected blood plasma samples at nine time points over three days. Both CORT and glucose response curves differed between georegions, with Iowa snakes attaining higher glucose concentration and maintaining elevated CORT and glucose levels for a longer duration. Additionally, both the total amount and proportional increases of CORT and glucose were lower in larger and therefore older snakes, suggesting ontogenetic shifts in stress perception or response. Within-individual correlation among the three physiological indicators was significant at the time of capture, absent after 3h in captivity, and partially restored after 3days in captivity, demonstrating the effect of stress on the relationships among these physiological systems. Together, these results provide further evidence for the great physiological flexibility of ectothermic tetrapods in maintaining homeostasis across a range of factors.

Convergence in reduced body size, head size, and blood glucose in three island reptiles

“…Based on our understanding of the physiological consequences of resource restriction in model organisms and humans, small body size on islands is predicted to involve alteration of physiological mechanisms regulating growth and metabolism (e.g., Clemmons & Underwood, ; Dunn et al., ; Fontana, Klein, Holloszy, & Premachandra, ; Roth et al., ; Smith, Underwood, & Clemmons, ). Blood glucose is a major physiological factor involved in whole‐organism metabolism that is regulated by a feedback mechanism designed to keep levels at or near an average set point, which may vary among species and populations (reviewed in Gangloff et al., ; Polakof, Mommsen, & Soengas, ; Ruiz, Rosenmann, Novoa, & Sabat, ). Vertebrates may obtain glucose either through absorption from digested carbohydrates in the small intestine, or via glycogenolysis (breakdown of glycogen) and gluconeogenesis from noncarbohydrate metabolites.…”

“…In the wild, little is known about how glucose varies with ecological factors, although recent studies suggest that it may vary by year and population (Gladalski et al. ; Gangloff et al., ; Kaliński et al., ; Kaliński et al., ; Ruiz et al., ). Laboratory studies suggest that pancreatic hormones act to regulate blood glucose similarly to mammals in nonmammalian vertebrates, such as reptiles (Miller & Wurster, ; Miller, ; Sidorkiewicz & Skoczylas, ; Putti, Varano, Cavagnuolo, & Laforgia, ; Gangloff, Holden, Telemeco, Baumgard, & Bronikowski, ).…”

“…Blood glucose is a major physiological factor involved in wholeorganism metabolism that is regulated by a feedback mechanism designed to keep levels at or near an average set point, which may vary among species and populations (reviewed in Gangloff et al, 2017;Polakof, Mommsen, & Soengas, 2011;Ruiz, Rosenmann, Novoa, & Sabat, 2002). Vertebrates may obtain glucose either through absorption from digested carbohydrates in the small intestine, or via glycogenolysis (breakdown of glycogen) and gluconeogenesis from noncarbohydrate metabolites.…”

“…In a surprising manner, the dynamics of blood glucose in nonmodel organisms have been little explored, and the majority of our understanding of glucose regulation is based on humans and laboratory rodents. In the wild, little is known about how glucose varies with ecological factors, although recent studies suggest that it may vary by year and population (Gladalski et al 2015;Gangloff et al, 2017;Kaliński et al, 2014;Kaliński et al, 2015;Ruiz et al, 2002).…”

Effects of early nutritional stress on physiology, life-histories and their trade-offs in a model ectothermic vertebrate

“…In vertebrates, glucocorticoid hormones such as CORT mediate daily and seasonal metabolic processes such as energy acquisition, storage and utilization (Landys et al, 2006;Sapolsky et al, 2000). Upon exposure to adverse events such as increased risk of predation, changes in thermal conditions or food deprivation, activity of the hypothalamic-pituitary-adrenal (HPA) axis is upregulated (Greenberg and Wingfield, 1987), increasing the secretion of CORT into circulation (Gangloff et al, 2016(Gangloff et al, , 2017bPalacios et al, 2012). Stress-induced levels of CORT mediate energy balance, such that self-maintenance and survival are prioritized over processes such as immunity and reproduction in the short-term (Greenberg and Wingfield, 1987;Romero et al, 2009).…”