Exposure to fluctuating temperatures leads to reduced immunity and to stress response in rattlesnakes

Abstract

Ectothermic organisms often experience considerable variation in their body temperature throughout the circadian cycle. However, studies focusing on the measurement of physiological traits are usually performed under constant temperature regimes. This mismatch between thermal exposure in the field and experimental conditions could act as a stressor agent, since physiological functions are strongly influenced by temperature. Herein, we asked the question whether constant thermal regimes would cause a stress response and impact the immunity of the South American rattlesnake (Crotalus durissus) when compared to a fluctuating thermal regime. We addressed this question by determining heterophil:lymphocyte ratio (H:L), plasma bacteria killing ability (BKA) and corticosterone levels (CORT) in snakes kept under a constant temperature regime at 30°C, and under a fluctuating regime that oscillated between 25°C at nighttime to 35°C at daytime. The experiments had a mirrored design, in which half of the snakes were subjected to a fluctuating-to-constant treatment, while the other half was exposed to a constant-to-fluctuating treatment. The shift from constant to fluctuating thermal regime was accompanied by an increase in plasma CORT levels indicating the activation of a stress response. Exposure to a fluctuating thermal regime at the onset of the experiments induced a decrease in the BKA of rattlesnakes. H:L was not affected by treatments and, therefore, the shift between thermal regimes seems to have acted as a low intensity stressor. Our results suggest that the removal from temperatures close to the snakés preferred body temperature triggers a stress response in rattlesnakes.

Glucocorticoids, energy metabolites, and immunity vary across allostatic states for plateau side‐blotched lizards (Uta stansburiana uniformis) residing in a heterogeneous thermal environment

“…Particular immune functions (e.g., phagocytosis, agglutination) can be tolerant of environmental temperature shifts that occur within and outside the natural climates of reptiles (Johnson et al, 1999; Palackdharry et al, 2017; Refsnider et al, 2015). Yet constant or fluctuating exposure to temperature extremes may become a stressor that in turn suppresses immunity (Fabrício‐Neto et al, 2019; Glassman & Bennett, 1978; McNally & Innis, 2020; Turton et al, 1997).…”

“…The potential for T body to be indirectly involved with immune regulation in U. stansburiana uniformis remains; however, considering the inverse relationship between BKA and CORT release. Corresponding increases in CORT seem to result in immunosuppression for those with higher T body , which reflects endocrine‐immune responses to chronic or predictable stressors in other reptiles (Berger et al, 2005; Fabrício‐Neto et al, 2019; French et al, 2017; Saad et al, 1986). CORT has so far been shown to either suppress immunity or yield no effect in reptiles (e.g., Finger et al, 2015; McCormick & Langkilde, 2014; Refsnider et al, 2015; Turton et al, 1997), whereby expedited and/or excessive CORT release facilitates immunosuppression.…”

“…CORT has so far been shown to either suppress immunity or yield no effect in reptiles (e.g., Finger et al, 2015; McCormick & Langkilde, 2014; Refsnider et al, 2015; Turton et al, 1997), whereby expedited and/or excessive CORT release facilitates immunosuppression. Again, the frequency and duration of release seems to be crucial for this relationship (e.g., Fabrício‐Neto et al, 2019; Martin, 2009; Saad, 1988; Seddon & Klukowski, 2012). Any immunomodulatory action of CORT during allostasis is therefore likely to covary with changes in the thermal environment (Dupoué et al, 2013; Telemeco & Addis, 2014).…”

“…Considering the efficacy of CORT release in reptiles can vary with environmental temperatures (Claunch et al, 2017; Dupoué et al, 2013; Gangloff et al, 2016; Lutterschmidt & Mason, 2009; Telemeco et al, 2017), changes in self‐maintenance via allostatic mediation are liable to be influenced by immediate T body . Assumedly, CORT release and action on survival traits directly scales with T body , but such relationships have yet to be fully addressed for reptiles (Fabrício‐Neto et al, 2019).…”

Introduction to the special issue: Ecoimmunology in ectotherms

“…Ectotherms are characterized by the low ability of endogenous control of body temperature, relying mostly on behavioral thermoregulation (Abram et al, 2017; Angilletta et al, 2002; Huey et al, 2003). In this way, ectotherms are particularly sensitive to environmental temperature changes, which reverberate on body temperature changes and affect physiological performance, including endocrine (Fabrício‐Neto et al, 2019; Narayan et al, 2012; Vargas‐Chacoff et al, 2019) and immune (Maniero & Carey, 1997; Marnila & Lilius, 2015; Palackdharry et al, 2017) functions. Finally, the introduction of invasive species also threatens native populations through predation, hybridization, the introduction of diseases, competition, and habitat alteration (Allendorf & Lundquist, 2003; Brown et al, 2020; Falaschi et al, 2020; Mack et al, 2000; Mooney & Cleland, 2001).…”