The fact that body temperature can rise or fall following exposure to stressors has been known for nearly two millennia; however, the functional value of this phenomenon remains poorly understood. We tested two competing hypotheses to explain stress-induced changes in temperature, with respect to surface tissues. Under the first hypothesis, changes in surface temperature are a consequence of vasoconstriction that occur to attenuate blood loss in the event of injury and serve no functional purpose per se; defined as the 'haemoprotective hypothesis'. Under the second hypothesis, changes in surface temperature reduce thermoregulatory burdens experienced during activation of a stress response, and thus hold a direct functional value: the 'thermoprotective hypothesis'. To understand whether stress-induced changes in surface temperature have functional consequences, we tested predictions of these two hypotheses by exposing black-capped chickadees (n=20) to rotating stressors across an ecologically relevant ambient temperature gradient, while non-invasively monitoring surface temperature (eye region temperature) using infrared thermography. Our results show that individuals exposed to rotating stressors reduce surface temperature and dry heat loss at low ambient temperature and increase surface temperature and dry heat loss at high ambient temperature, when compared with controls. These results support the thermoprotective hypothesis and suggest that changes in surface temperature following stress exposure have functional consequences and are consistent with an adaptation. Such findings emphasize the importance of the thermal environment in shaping physiological responses to stressors in vertebrates, and in doing so, raise questions about their suitability within the context of a changing climate.
Authors' contributions: CMP, GB and CCW conceived the ideas and designed methodology; 15 CMP collected the data; CMP and JR analysed the data; CMP led the writing of the manuscript. 16 All authors contributed critically to manuscript drafts and gave final approval for publication. 18Lay summary: Adult lake trout held at two temperatures were interbred to study the influence of 19 parental thermal environments on the next generation's thermal physiology. Offspring 20 performance reflected both their own rearing environment and parental influences, although 21 parental effects on offspring physiology were limited and not always beneficial. 22 23 Word count: 8,205 24 25 26 27 28 29 2 Abstract 30The capacity of ectotherms to cope with rising temperatures associated with climate change is a 31 significant conservation concern as the rate of warming is likely too fast for adaptation to occur 32 in some populations. Transgenerational plasticity, if present, could potentially buffer some of the 33 negative impacts of warming on future generations. We examined transgenerational plasticity in 34 lake trout to assess their inter-generational potential to cope with anticipated warming. We 35 acclimated adult lake trout to cold or warm temperatures for several months, then bred them to 36 produce offspring from parents of matched and mismatched temperatures. At the fry stage, 37 offspring were also acclimated to cold or warm temperatures and their thermal performance was 38 assessed by measuring their critical thermal maximum and metabolic rate during an acute 39 temperature challenge. Overall, transgenerational plasticity was evident: thermal performance of 40 offspring reflected both maternal and paternal environmental conditions, and offspring 41 performed better when their environment matched that of their parents. There was little variation 42 in offspring critical thermal maximum or peak metabolic rate, although cold-acclimated 43 offspring from warm-acclimated parents exhibited elevated standard metabolic rates, suggesting 44 that transgenerational effects can be detrimental when parent and offspring environments 45 mismatch. These results demonstrate both the occurrence and limitations of transgenerational 46 plasticity in a coldwater salmonid in response to elevated temperature, as well as potential 47 50
Coping with stressors can require substantial energetic investment, and when resources are limited, such investment can preclude simultaneous expenditure on other biological processes. Among endotherms, energetic demands of thermoregulation can be immense, yet our understanding of whether a stress response is sufficient to induce changes in thermoregulatory investment is limited. Using the black-capped chickadee as a model species, we tested a hypothesis that stress-induced changes in surface temperature, a well-documented phenomenon across vertebrates, stem from trade-offs between thermoregulation and stress responsiveness. Because social subordination is known to constrain access to resources in this species, we predicted that surface temperature and dry heat loss of social subordinates, but not social dominants, would fall under stress exposure at low ambient temperatures (“Ta”), and rise under stress exposure at high Ta, thus permitting a reduction in expenditure toward thermoregulation. To test our predictions, we exposed four social groups of chickadees to repeated stressors and control conditions across a Ta gradient (ndays/treatment/group=30), whilst remotely monitoring social interactions and surface temperatures. Supporting our hypothesis, we show that: 1) social subordinates (n=12), who fed less than social dominants and alone experienced stress-induced mass-loss, displayed significantly larger changes in surface temperature following stress exposure than social dominants (n=8), and 2) stress-induced changes in surface temperature significantly increased heat conservation at low Tas and heat dissipation at high Tas among social subordinates alone. These results suggest that chickadees adjust their thermoregulatory strategies under stress when resources are limited by ecologically relevant processes.
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