Organismal effects of heat in a fixed ecological niche: Implications on the role of behavioral buffering in our changing world

Increasingly frequent and intense heatwaves generate new challenges for many organisms. Our understanding of the ecological predictors of thermal vulnerability is improving, yet, at least in endotherms, we are still only beginning to understand one critical component of predicting resilience: exactly how do wild animals cope with sub-lethal heat? In wild endotherms, most prior work focuses on one or a few traits, leaving uncertainty about organismal consequences of heatwaves. Here, we experimentally generated a 2.8 °C heatwave for free-living nestling tree swallows (Tachycineta bicolor). Over a week-long period coinciding with the peak of post-natal growth, we quantified a suite of traits to test the hypotheses that (a) behavioral or (b) physiological responses may be sufficient for coping with inescapable heat. Heat-exposed nestlings increased panting and decreased huddling, but treatment effects on panting dissipated over time, even though heat-induced temperatures remained elevated. Physiologically, we found no effects of heat on: gene expression of three heat shock proteins in blood, muscle, and three brain regions; secretion of circulating corticosterone at baseline or in response to handling; and telomere length. Moreover, heat had a positive effect on growth and a marginal, but not significant, positive effect on subsequent recruitment. These results suggest that nestlings were generally buffered from deleterious effects of heat, with one exception: heat-exposed nestlings exhibited lower gene expression for superoxide dismutase, a key antioxidant defense. Despite this one apparent cost, our thorough organismal investigation indicates general resilience to a heatwave that may, in part, stem from behavioral buffering and acclimation. Our approach provides a mechanistic framework that we hope will improve understanding of species persistence in the face of climate change.

日趋频繁且强度加剧的热浪对诸多生物均构成全新挑战。尽管我们对热易感性的生态预测因子的认知正逐步加深，但至少在恒温动物（endotherms）中，我们仍刚起步理解预测种群恢复力的关键一环：野生动物究竟如何应对亚致死高温胁迫。针对野生恒温动物的既往研究多聚焦于单一或少数性状，这使得我们难以明确热浪对生物体带来的整体影响。本研究通过实验为自由生活的树燕（Tachycineta bicolor）雏鸟构建了2.8℃的热浪环境。在恰逢产后生长峰值的一周周期内，我们量化了多组性状，以验证两项假说：（a）行为响应或（b）生理响应足以应对无法规避的高温胁迫。受热暴露的雏鸟会增加喘息行为并减少集群取暖，但即便热浪诱导的高温仍持续存在，处理组对喘息行为的影响会随时间消退。生理层面上，我们未观察到高温对以下指标产生影响：血液、肌肉及三个脑区中三种热休克蛋白（heat shock proteins）的基因表达；基础状态或应激处理后循环皮质酮（corticosterone）的分泌水平；以及端粒长度。此外，高温对雏鸟生长具有正向影响，且对后续招募率存在边际正向效应，但该效应未达到统计学显著性水平。上述结果表明，雏鸟整体上可免受高温的有害影响，但存在一项例外：受热暴露的雏鸟体内作为关键抗氧化防御机制的超氧化物歧化酶（superoxide dismutase）的基因表达水平更低。尽管存在这一明显的代价，但我们全面的生物体层面研究表明，雏鸟对热浪整体具备恢复力，这一现象或许部分源自行为缓冲与适应性驯化。本研究的方法构建了一套机制性框架，我们期望该框架可增进人们对气候变化背景下物种存续机制的认知。