Avian thermoregulation in the heat: efficient evaporative cooling in two southern African nightjars

Abstract

Nightjars represent a model taxon for investigating physiological limits of heat tolerance because of their habit of roosting and nesting in sunlit sites during the heat of the day. We investigated the physiological responses of Rufous-cheeked nightjars (Caprimulgus rufigena) and Freckled nightjars (Caprimulgus tristigma) to high air temperatures (T ) by measuring body temperature (T), resting metabolic rate (RMR) and total evaporative water loss (TEWL) at T ranging from 10 to 56 °C. Both species became hyperthermic at T > T . Lower critical limits of thermoneutrality occurred at T between 35 and 37 °C, whereas we detected no clear upper critical limits of thermoneutrality. Between T ≈ 37.0 and 39.9 °C, rates of TEWL increased rapidly with T. At T ≥ 40 °C, fractional increases in mass-specific TEWL rates were 78-106% of allometric predictions. Increasing evaporative heat dissipation incurred only small metabolic costs, with the RMR of neither species ever increasing by more than 20% above thermoneutral values. Consequently, both species displayed extremely efficient evaporative cooling; maximum evaporative heat dissipation was equivalent to 515% of metabolic heat production (MHP) at T ≈ 56 °C in C. rufigena and 452% of MHP at T ≈ 52 °C in C. tristigma. Our data reiterate that caprimulgids have evolved an efficient mechanism of evaporative cooling via gular fluttering, which minimizes metabolic heat production at high T and reduces total heat loads. This likely aids in reducing TEWL rates and helps nightjars cope with some of the most thermally challenging conditions experienced by any bird.

The functional significance of facultative hyperthermia varies with body size and phylogeny in birds

“…T b data from populations of nine species of wild birds held in outdoor aviaries in mid‐summer in the Kalahari Desert support this prediction; several small (<50 g) songbirds maintained modal diurnal T b values of ~43°C (Thompson, Cunningham, & McKechnie, ). In contrast, mean T b at T a ≥ 38°C in free‐ranging populations of two southern African nightjars was lower, 40°C in freckled nightjars ( Caprimulgus tristigma ) and 42°C in rufous‐cheeked nightjars ( C. rufigena ) (O'Connor et al, ), consistent with our conclusions that hyperthermia is relied upon much less by nightjars. When contrasted with doves and nightjars that have high evaporative efficiencies and rely much less on hyperthermia as a heat tolerance strategy, songbirds rely heavily on hyperthermia as a heat tolerance strategy and we therefore predict tissue‐level differences in optimal temperatures for various functions that would be due to differences in heat stability and sensitivity of metabolic and other enzymes.…”

“…This results in much lower heat loads from metabolism during heat exposure, and thus, evaporative heat loss is only required to dissipate external heat loads. Nightjars (Caprimulgidae), in contrast, use gular flutter, which is the rapid oscillation of the throat pouch (Bartholomew, Lasiewski, & Crawford, 1968), which is also very efficient (O'Connor et al, 2017;Talbot et al, 2017). Currently, it appears that most other orders of birds investigated to date, the songbirds, owls, parrots and sandgrouse, rely primarily on panting (but see Bartholomew et al, 1968).…”

“…pathological hyperthermia) but rather represent a facultative physiological response involving a temporarily increased set point, as has been shown in a number of early (e.g. Dawson, ; Bartholomew & Dawson, ; Dawson & Fisher, and more recent studies Gerson, Smith, Smit, McKechnie, & Wolf, ; O'Connor, Wolf, Brigham, & McKechnie, ; Smit et al, ; Smith, O'Neill, Gerson, & Wolf, ; Whitfield, Smit, McKechnie, & Wolf, ). These recent studies have evaluated T b under conditions of high T e and have shown that a stepwise increase in T e results in a corresponding increase in T b .…”

Diurnal body temperature patterns in free‐ranging populations of two southern African arid‐zone nightjars

“…The average increase in diurnal T b above T b‐mod at T a ≥ 38°C for the two free‐ranging rufous‐cheeked nightjars was similar in magnitude to that of several captive diurnal species at T a = 45°C (Tieleman and Williams ; 3.3 ± 1.28°C). In the laboratory at T a = 38–40°C (O'Connor et al ), this same population of rufous‐cheeked nightjars maintained a mean T b 1.9°C lower than the free‐ranging mean T b of 42°C at similar T a . The dissimilarity in hyperthermia between free‐ranging and captive rufous‐cheeked nightjars at similar T a likely reflects the complexity of natural thermal environments compared to controlled laboratory conditions.…”

“…At T a ≥ 38°C, freckled nightjars did not allow their T b to deviate much above T b‐mod . Under laboratory conditions, the same population of freckled nightjars regulated T b at a similar level (39.5°C) when exposed to T a = 38–42°C, increasing their T b to 40.7°C only at T a = 52°C (O'Connor et al ). These data suggest that freckled nightjars defend T b within a narrow range at T a > T b .…”