Abstract
Avian evaporative cooling and the maintenance of body temperature (Tb) below lethal limits during heat exposure has received more attention in small species compared to larger-bodied taxa. Here, we examined thermoregulation at air temperatures (Tair) approaching and exceeding normothermic Tb in three larger birds that use gular flutter, thought to provide the basis for pronounced evaporative cooling capacity and heat tolerance. We quantified Tb, evaporative water loss (EWL) and resting metabolic rate (RMR) in the ∼170-g Namaqua sandgrouse (Pterocles namaqua), ∼430-g spotted thick-knee (Burhinus capensis) and ∼670-g spotted eagle-owl (Bubo africanus), using flow-through respirometry and a stepped Tair profile with very low chamber humidities. All three species tolerated Tair of 56–60°C before the onset of severe hyperthermia, with maximum Tb of 43.2°C, 44.3°C, and 44.2°C in sandgrouse, thick-knees and eagle-owls, respectively. Evaporative scope (i.e., maximum EWL/minimum thermoneutral EWL) was 7.4 in sandgrouse, 12.9 in thick-knees and 7.8 in eagle-owls. The relationship between RMR and Tair varied substantially among species: whereas thick-knees and eagle-owls showed clear upper critical limits of thermoneutrality above which RMR increased rapidly and linearly, sandgrouse did not. Maximum evaporative heat loss/metabolic heat production ranged from 2.8 (eagle-owls) to 5.5 (sandgrouse), the latter the highest avian value yet reported. Our data reveal some larger species with gular flutter possess pronounced evaporative cooling capacity and heat tolerance and, when taken together with published data, show thermoregulatory performance varies widely among species larger than 250 g. Our data for Namaqua sandgrouse reveal unexpectedly pronounced variation in the metabolic costs of evaporative cooling within the genus Pterocles.
Highlights
Evaporative cooling and the maintenance of body temperature (Tb) below environmental temperature is critical for terrestrial taxa that encounter operative temperatures (Bakken, 1976; Robinson et al, 1976) exceeding normothermic Tb, or when metabolic heat produced during activity must be dissipated to avoid Tb reaching lethal limits (e.g., Nilsson and Nord, 2018; Thompson et al, 2018)
Together with maximum evaporative heat loss/metabolic heat production (EHL/MHP) values of 2.8–5.5, the high heat tolerance limits of these species support the notion that gular flutter provides the basis for pronounced evaporative cooling and heat tolerance, quantifying the contribution of gular flutter was precluded here by us not partitioning respiratory and cutaneous evaporative water loss (EWL)
We found less support for the idea that patterns of thermoregulation at high Tair remain similar within genera and families, with patterns of thermoregulation in P. namaqua and B. africanus differing to varying extents from those of previously-studied sandgrouse and owls, respectively
Summary
Evaporative cooling and the maintenance of body temperature (Tb) below environmental temperature is critical for terrestrial taxa that encounter operative temperatures (Bakken, 1976; Robinson et al, 1976) exceeding normothermic Tb, or when metabolic heat produced during activity must be dissipated to avoid Tb reaching lethal limits (e.g., Nilsson and Nord, 2018; Thompson et al, 2018). Maximum ratios of evaporative heat loss/metabolic heat production (EHL/MHP) are consistently higher in taxa that use pronounced gular flutter (Dawson and Fisher, 1969; O’Connor et al, 2017) or have the capacity for rapid cutaneous evaporative water loss (Calder and SchmidtNielsen, 1967; Marder and Arieli, 1988; McKechnie et al, 2016a) compared to groups that rely on panting as their primary pathway of evaporative heat loss (Dawson, 1954; Weathers, 1981). Whereas fractional increases in EWL are broadly consistent across taxa, the metabolic heat production associated with panting means that evaporative cooling capacity and heat tolerance limits tend to be lower in passerines, which represent >50% of extant birds, compared to some non-passerine orders (McKechnie et al, 2021a)
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