Lag of Immunity Across Seasonal Acclimation States in Gopher Tortoises (Gopherus Polyphemus)

Abstract

Disease outbreaks are of increasing importance to ectothermic vertebrates as one of numerous results of global change. Anthropogenic climate change is predicted to increase climatic instability, thereby altering natural thermal environments. In this study, we evaluated the direct effects of rapid temperature change on immunity in Gopher Tortoises (Gopherus polyphemus). Specifically, we tested the lag hypothesis, which predicts significant misalignment of optimal and realized immunity when temperature rapidly changes. We assayed constitutive innate immunity, B-cell humoral responses, and heterophil: lymphocyte ratios in response to rapid temperature changes corresponding to realistic changes in body temperature between winter and summer. We found that during summer, rapid temperature reduction caused a series of changes in immunity, including reduced bactericidal ability (P = 0.002), reduced humoral response (P < 0.0001), and increased heterophil:lymphocyte ratios (P < 0.0001). During winter, we found that a temperature increase provided no benefit to immunity. Specifically, there was no increase in bactericidal ability as was predicted by the lag hypothesis. In winter, humoral responses were significantly reduced as a result of rapid warming (P = 0.011) and the rapid warming caused a significant reduction in heterophil:lymphocyte ratios (P < 0.0001). Independent of temperature, we found a significant acclimation effect of winter relative to summer conditions in humoral response (P < 0.001), which showed an overall increase in this parameter during winter. Our findings demonstrate that rapid temperature change, regardless of its direction, is a constraint on immunity in ectothermic vertebrates.

Rapid thermal immune acclimation in common musk turtles (Sternotherus odoratus)

“…This responsiveness is present in the unchanged BA in control S. odoratus subjected to different temperatures, and the temperature‐dependent increase in humoral immunity in LPS‐injected S. odoratus . Two different experiments have demonstrated a significant constraint in gopher tortoises: when freely thermoregulating tortoises reduced body temperature they also reduced immunity (Goessling et al, ) and when tortoises were exposed to a rapid temperature reduction, immunity was reduced after 48 hr (Goessling et al, ). In this study, S. odoratus rapidly compensated for the change in temperature to maintain stable immunity, whereas G. polymphemus in prior studies did not compensate for a change in temperature.…”

“…Understanding the nexus between thermal physiology and immunology is a critical link to elucidate mechanisms by which organisms are constrained by and respond to environmental change ( sensu Raffel, Rohr, Kieseck, & Hudson, ). Recent evidence has shown that climate change, specifically climatic variability, can have significant negative effects on immunity in ectothermic vertebrates (Goessling, Guyer, & Mendonҫa, ; Raffel et al, ; Raffel, Halstead, McMahon, & Davis, ). Reptiles are ideal models for experimentally assessing how changes in environmental temperature affect population susceptibility to disease because of the direct relationship between thermal environments and reptile body temperatures.…”

Introduction to ecoimmunology: An integrative approach

“…How the immune responses of different insects will react to changing environmental conditions remains an open question, as it is clear that one strategy does not fit all. Along these same lines, the paper by Goessling, Koler, Overman, Hiltbold, Guyer, and Mendonça () evaluated the direct effects of rapid temperature change on immunity in gopher tortoises and showed that during summer, but not winter, rapid temperature reduction caused a series of changes in immunity. Their findings demonstrate that rapid temperature changes constrain immunity in ectothermic vertebrates, which has implications for global climate change (Goessling et al., ).…”

“…Along these same lines, the paper by Goessling, Koler, Overman, Hiltbold, Guyer, and Mendonça () evaluated the direct effects of rapid temperature change on immunity in gopher tortoises and showed that during summer, but not winter, rapid temperature reduction caused a series of changes in immunity. Their findings demonstrate that rapid temperature changes constrain immunity in ectothermic vertebrates, which has implications for global climate change (Goessling et al., ). Two of the studies in this special issue fall into this final theme but are focused on species of conservation concern (golden eagles and polar bears) and illustrate the utility of ecoimmunological approaches in conservation.…”

“…Avian species include the house wren ( Troglodytes aedon ), the golden eagle ( Aquila chrysaetos ), the song sparrow ( Melospiza melodia ), the European starling ( Sturnus vulgaris ), and the zebra finch ( Taeniopygia guttata ) (Bowers, Sakaluk, & Thompson, ; Grindstaff & Merrill, ; Kelly et al., ; MacColl et al., ; Pryor & Casto, ). Reptilian species represented in the current issue are the green anole ( Anolis carolinensis ), the gopher tortoise ( Gopherus polyphemus ), and the snapping turtle ( Chelydra serpentina ) (Beck, Thompson, & Hopkins, ; Goessling et al., ; Tylan & Langkilde, ). Finally, one mammalian species is also represented, the polar bear ( Ursus maritimus ) (Neuman‐Lee et al., ).…”