Avian adaptive thermoregulation correlated with temperature and humidity

Abstract

Extreme heat events and increasing global air temperatures pose serious challenges for the persistence of endothermic animals. Physiologically, it remains unclear whether thermoregulatory capacity and mechanisms used to maintain sublethal body temperatures at high environmental temperatures vary among species, particularly those from contrasting climatic regions which may have evolved differently in response to past and current climatic conditions. Moreover, our understanding of how abiotic variables such as humidity affect the thermoregulatory performance of species within such climatic regions and whether species experience selection for thermal traits to overcome such conditions also remains unexplored. To address these questions, I conducted four related studies (each a chapter in this thesis) to disentangle the effects of air temperature and humidity on avian thermoregulation under hot conditions, and how thermoregulatory performance and limits vary with climate.

In my first chapter, I hypothesised that the maximum tolerable body temperature (Tbmax) of birds has evolved in response to climate, with raised Tbmax associated with species exposed to high environmental heat loads or humidity-related constraints on evaporative heat dissipation. Making use of flow-through respirometry, I collected thermoregulatory data for 53 bird species at air temperatures between 28-56°C under standardised very dry air from three contrasting climatic regions (hot arid, mesic montane and lowland humid) with varying maximum air temperatures, across South Africa. When analysed in a phylogenetically-informed comparative framework, my data revealed novel macrophysiological patterns supporting recent suggestions that endothermic animals have evolved thermal generalisation vs thermal specialisation analogous to the corresponding continuum among ectothermic animals. Among arid-zone birds, hyperthermia tolerance was relatively low, whereas evaporative cooling was characterised by higher ratios of evaporative heat loss/metabolic heat production (evaporative cooling efficiency). In contrast, among birds from more mesic and particularly humid regions hyperthermia tolerance was elevated but evaporative cooling was modest suggesting thermal generalisation. This study provides evidence that hyperthermia tolerance has evolved in response to climate.

Next, I investigated whether birds from humid habitats had evolved physiological mechanisms to reduce the impact of humidity-impeded scope for evaporative heat dissipation. Using a similar approach to my first chapter, I tested the thermal responses of 30 bird species from three contrasting climatic regions under both dry and humid conditions. I found that the effect of humidity on evaporative cooling and heat tolerance limits was less among birds occupying humid lowlands compared to arid-zone birds. My findings suggest that humid environments have resulted in selection for pronounced hyperthermic tolerance to mitigate the effects of impeded evaporative cooling efficiency, permitting lowland birds to persist during extreme heat coupled with humidity. In contrast, thermoregulatory performance among birds from less humid habitats was more strongly affected by high humidity and they experienced substantial decreases in heat tolerance limits.

In my third and fourth chapters, I investigated the hyperthermic abilities of a small, highly gregarious passeriform bird, the red-billed quelea (Quelea quelea). Red-billed queleas experience extreme heat loads by foraging on the ground in direct solar radiation for long periods, often under conditions of raised humidity. The findings of this study revealed queleas to be capable of extreme hyperthermia well above known limits for endotherms, with average maximum body temperature reaching 48.0 ± 0.7 °C without any apparent ill effects. The highest body temperature recorded in this study was 49.1°C. The study sheds light on the differing hyperthermic capabilities of endotherms which may be beneficial for mitigating the impeding effects of environmental conditions such as humidity on avian thermoregulation. The impressive hyperthermia tolerance of queleas makes them an ideal model species to investigate whether hypothermia can be beneficially used as a thermoregulatory strategy to reduce the effects of extreme heat loads and impeding effects of environmental conditions.

Finally, again using red-billed queleas as a model I assessed whether the evolution of hyperthermia tolerance could be functionally linked to tolerating high heat loads and accommodating humidity-associated curtailment of evaporative cooling. My findings suggest that thermoregulatory response variables under different humidity treatments were largely similar, with queleas essentially becoming poikilothermic at very high Tair. No significant difference was detected in maximum tolerable body temperature and limited differences were found for heat tolerance limits. The study provides evidence that hyperthermia tolerance is functionally linked with accommodating the impeding effects of humidity on evaporative water loss and maintaining heat tolerance capacity.

In conclusion, my findings add to an increasing pool of literature regarding adaptive differences in endothermic thermoregulation in response to climate. My thesis also highlights the importance of understanding both avian species-specific thermal capabilities and conducting macro-physiological assessments for making predictions regarding responses to future predicted climatic changes.