Physiological avenues of heat dissipation in Afrotropical forest hornbills

Abstract

Worldwide, most research regarding the direct impacts of more frequent heat waves on birds has focused on arid-zone species due to their vulnerability to rising air temperatures (Tair). In contrast, mesic lowlands have often been considered climatically benign and physiologically unchallenging in terms of thermal physiology and consequently, there is limited understanding of how tropical birds, particularly those associated with forests, cope with heat exposure. The only way for birds to effectively cool themselves in hot environments is through evaporative cooling when environmental temperatures exceed body temperature (Tb). The effects of humidity and heat on Tb regulation in birds has not been as thoroughly examined compared to the impacts of high Tair alone. Raised humidity will impede evaporative water loss in birds at elevated Tair, particularly when the water vapour pressures in the surrounding air approach that of the evaporative surfaces responsible for dissipating heat. The prevalence of raised humidity and heat is more common in sub-tropical regions than in other climatic zones, prompting tropical, lowland-associated birds to rely on facultative hyperthermia for dry heat dissipation as it may overcome limitations posed by reduced scope for evaporative cooling. In addition, another mechanism of cooling includes non-evaporative heat dissipation through body structures, known as “thermal windows”. The beak, limbs and unfeathered skin in particular, have been identified as key adaptive thermoregulatory structures of birds by minimising the demand for evaporative cooling when Tair approaches Tb. However, sources of interspecific variation in heat exchange capacity of these regions remain unclear and may include body mass, surface area and possibly adaptive variation correlated with climate. Although it is now clear that the use of controllable heat radiators is widespread among birds, several questions pertaining the effectiveness of the beak and casque remain unanswered. Our understanding of the physiological responses of lowland birds to the combined effects of humidity and heat are still incipient, therefore, my Master's dissertation aimed to investigate two main questions: 1) how does the combination of heat and humidity affect forest hornbill thermoregulation, and 2) are the beak and casques of large Afrotropical hornbills utilized as thermal radiators? In my first chapter, using trumpeter hornbills (Bycanistes bucinator) as a model large forest frugivore, I tested the hypothesis that thermoregulatory performance (i.e., the ability to maintain Tb below lethal limits through evaporative cooling) at environmental temperatures approaching or exceeding normothermic Tb is impeded by high atmospheric humidity. Making use of flow-through respirometry, I collected thermoregulatory data for 28 trumpeter hornbills at increasing Tair under three experimental treatments of humidity; 6, 13 and 25 g H2O m-3. As expected, I found that raised humidity levels with increasing Tair hampered the efficiency of hornbills to offload heat through evaporative cooling forcing hornbills to increase thermoregulatory efforts. At high experimental Tair, hornbills were unable to maintain Tb below Tair as only 37% of metabolic heat was lost through evaporative cooling. This resulted in an increased reliance on hyperthermia (the elevation of Tb above normothermic values during heat exposure), with Tb reaching up to 46.55°C, in an attempt mitigate negative effects on heat tolerance capacity. As such, with increases in Tair and humidity predicted for future climatic scenarios and the possible overlap with the heat tolerance of hornbills, these data reveal the trumpeter hornbills’ narrow thermal safety margin (i.e., the difference between the maximum Tb a species can tolerate and its normothermic Tb) outside of shaded microsites and highlight the importance of considering environmental conditions when making predictions or modelling endotherm responses to climate change. This chapter underscores the critical importance of conserving and restoring cool microsites that buffer species from direct solar radiation and consequently high operative temperatures that exacerbate thermal stress under humid conditions. In my second chapter, I investigated whether Afrotropical forest hornbills have evolved non-evaporative mechanisms via the use of the beak and casque as thermal radiators. To do this, I collected thermography data over Tair ranging from 15 to 34°C for three species of Afrotropical hornbills. The beak, casque and facial skin of all three species displayed signs of active regulation and heat loss at higher Tair (> 24 - 25°C). I found that the beak accounted for up to 50-53% of metabolic heat loss across hornbill species with maximum heat loss capacity amounting to 97 – 120 W m-2. Whereas facial skin only made up 3-5% of metabolic heat loss at 0.3 - 0.6 W m-2. Interestingly, when comparing all species investigated to date with these three species, the point of inflection has an inverse relationship with body size, i.e., larger species use their beaks as thermal windows at lower Tair relative to smaller species. In this chapter, I show that large forest hornbills use their beaks, casque and facial skin for heat loss as an effective thermoregulatory process. This is important as these species are exposed to conditions characterised by humid heat that impedes the efficiency of evaporative cooling (Chapter 1). Furthermore, the data from this chapter, and that from other studies, provide novel insights into the variation in threshold temperatures and heat loss capacity of the beak depending on a bird’s body size. In conclusion, my findings add to a growing body of literature regarding endotherm heat tolerance to increasing Tair and humidity in the context of a changing climate and add to the evidence for the avian beak being a vital thermoregulatory organ. The findings from both chapters complement each other and raise the possibility that, because reliance on hyperthermia tolerance under humid conditions favours Tb > Tair, hyperthermic body temperatures may maximise non-evaporative cooling via the beak. My dissertation highlights the importance of understanding species-specific thermal traits and capacities, as these directly contribute to what extent species are vulnerable to rising Tair. This dissertation contains empirical data of the different avenue’s hornbills use to maintain body temperature and ultimately body condition. Such data can be used to make inferences on the responses of species of similar body sizes and habitats. Furthermore, in light of research moving towards less-invasive protocols, the interacting effects of evaporative (i.e., chapter 1) and non-evaporative heat loss (i.e., chapter 2) need to be well-understood should we rely on biophysical modelling to make sound predictions on the thermoregulatory responses of animals and studies such as these may form the foundation to moving in this direction.