Temperature Extreme Events Decrease Endocrine and Immune Reactive Scope in Bullfrogs (Lithobates catesbeianus)

Abstract

Currently, effects of increased atmospheric temperature, in the context of ongoing climate change, have been investigated in multiple organisms and levels of biological organization. While there has been a focus on the impacts of increased mean temperature, an emergent and equally important point is the consequences of recurrent exposure to extreme temperature events, simulating heat waves. This study investigated the effects of serial exposure to high temperatures on immune and endocrine variables before and after exposure to an acute secondary stressor in bullfrogs (Lithobates catesbeianus). Adult males were divided into three groups and subjected to three thermal regimes: Control (C; constant 22°C); Experimental 1 (E1; kept at 22°C and exposed to 4 days of 30°C every 16 days); and Experimental 2 (E2; kept at 22°C and exposed to 4 days of 30°C every 6 days). Blood samples were collected on the last day of key extreme heat events. Two weeks after the last extreme heat event, animals were subjected to restraint stress (1h) and sampled again. Blood samples were used to determine neutrophil: lymphocyte ratio, plasma bacterial killing ability, as well as corticosterone and plasma testosterone levels. Overall, we found exposure to extreme heat events did not affect immune and endocrine variables over time. Meanwhile, the previous exposure to extreme heat events modulated the responsiveness to restraint. The amplitude of increased corticosterone plasma levels and neutrophil: lymphocyte ratio in response to restraint decreased with the number of previous exposures to extreme heat events. These results suggest that exposure to extreme climatic events has hidden effects on bullfrog's stress response, expressed as diminished reactive scope to a novel stressor. This represents a highly deleterious facet of climate change since diminished responsiveness prevents proper coping with wildlife challenges.

Contrasting effects of transdermal and implant corticosterone treatments in the American bullfrog wound healing

“…Further validation show that the transdermal delivery of the CORT solution (2 µg 10 µl −1 ) resulted in an increase of CORT plasma levels 30 min after the treatment. The CORT plasma levels achieved after the hormonal transdermal delivery (mean: 8.98 ng ml −1 ) were similar to what individuals of this species experience during reproductive/calling behaviour ( [33], mean: 9 ng ml −1 ) and higher than what is observed in this species after movement restriction [48], which confirms that the transdermal delivery resulted in transient elevation of CORT plasma levels similar to what males experience during their natural life history [33]. As expected, individuals that received the CORT-filled implants (group 4) had a 27-fold increase in CORT plasma levels compared with the baseline.…”

Introduction to the special issue Amphibian immunity: stress, disease and ecoimmunology

“…Stress-induced immunomodulation has been described when animals are facing environmental changes (e.g. temperature variation, dehydration and pollution) [13,15,[65][66][67][68] and well-established stress-induced protocols (e.g. restraint and captivity maintenance) [27,29,[69][70][71].…”

“…In addition to environmental changes like temperature shifts, changes in rainfall regimes, loss of habitats, fragmentation, pollution, infectious diseases significantly contribute to this scenario [2][3][4][5][6][7]. In addition, there are a multitude of documented shifts in behaviour and physiology that occur in native populations dealing with climate change and infectious diseases, which have been associated with alterations in hormonal and immune modulation, possibly leading to systemic failure and death [8][9][10][11][12][13]. Among physiological changes, alterations in stress-related measures such as increased glucocorticoid levels may have critical implications on disease resistance and host survival [7,9,11,13,14].…”

“…In addition, there are a multitude of documented shifts in behaviour and physiology that occur in native populations dealing with climate change and infectious diseases, which have been associated with alterations in hormonal and immune modulation, possibly leading to systemic failure and death [ 8 – 13 ]. Among physiological changes, alterations in stress-related measures such as increased glucocorticoid levels may have critical implications on disease resistance and host survival [ 7 , 9 , 11 , 13 , 14 ].…”

A mathematical representation of the reactive scope model

“… 2022 ; Lima et al. 2022 ; Pahuja and Narayan 2021 ; Roast et al. 2019 ; Romero 2012 ; Schoenle et al.…”