Regulation of Heat Exchange across the Hornbill Beak: Functional Similarities with Toucans?

Abstract

Beaks are increasingly recognised as important contributors to avian thermoregulation. Several studies supporting Allen’s rule demonstrate how beak size is under strong selection related to latitude and/or air temperature (Ta). Moreover, active regulation of heat transfer from the beak has recently been demonstrated in a toucan (Ramphastos toco, Ramphastidae), with the large beak acting as an important contributor to heat dissipation. We hypothesised that hornbills (Bucerotidae) likewise use their large beaks for non-evaporative heat dissipation, and used thermal imaging to quantify heat exchange over a range of air temperatures in eighteen desert-living Southern Yellow-billed Hornbills (Tockus leucomelas). We found that hornbills dissipate heat via the beak at air temperatures between 30.7°C and 41.4°C. The difference between beak surface and environmental temperatures abruptly increased when air temperature was within ~10°C below body temperature, indicating active regulation of heat loss. Maximum observed heat loss via the beak was 19.9% of total non-evaporative heat loss across the body surface. Heat loss per unit surface area via the beak more than doubled at Ta > 30.7°C compared to Ta < 30.7°C and at its peak dissipated 25.1 W m-2. Maximum heat flux rate across the beak of toucans under comparable convective conditions was calculated to be as high as 61.4 W m-2. The threshold air temperature at which toucans vasodilated their beak was lower than that of the hornbills, and thus had a larger potential for heat loss at lower air temperatures. Respiratory cooling (panting) thresholds were also lower in toucans compared to hornbills. Both beak vasodilation and panting threshold temperatures are potentially explained by differences in acclimation to environmental conditions and in the efficiency of evaporative cooling under differing environmental conditions. We speculate that non-evaporative heat dissipation may be a particularly important mechanism for animals inhabiting humid regions, such as toucans, and less critical for animals residing in more arid conditions, such as Southern Yellow-billed Hornbills. Alternatively, differences in beak morphology and hardness enforced by different diets may affect the capacity of birds to use the beak for non-evaporative heat loss.

Spatial variation in avian bill size is associated with humidity in summer among Australian passerines

“…Given the diverse range of species included in this study, reliance on the bill for cooling in humid summer conditions may be a common strategy in Australian birds. Bird bills may no longer be effective in dissipating heat when air temperatures exceed body temperature because bills become a source of heat gain, drawing heat into the body rather than dissipating it [9,12]. Our results show that the strength of the association between bill size and humidity was mediated by maximum summer temperature, with stronger associations with humidity at cooler summer temperatures.…”

“…Similarly, among 13 subspecies of the yellow warbler, Setophaga petechia, distributed throughout North and Central America, there was a strong positive relationship between bill size and ambient temperature in habitats experiencing mean maximum July (summer) temperatures in the range 18-41°C [11]. Larger bill size may be a particularly important adaptation in hot, arid environments where water availability is limited in summer [9,12,14] since heat dissipation via the bill does not involve evaporative water loss, thereby improving water conservation [2,[15][16][17]. However, in extremely hot environments large bill size may be costly due to the risk of heat uptake.…”

“…Although bill morphology is strongly associated with diet and foraging niche [4,5], there is also growing evidence of its significance in body temperature regulation [6][7][8] and heat exchange via the bill has been found in all species investigated to date [9]. The keratinized outer layer of the bill, the rhamphotheca, covers an extensive network of blood vessels into which blood may be pumped during exposure to high temperatures to achieve dissipation of excess metabolic heat via radiation and convection [10].…”

“…Thus, for example, the Toco toucan, Ramphastos toco can shunt up to 60% of its heat load through the bill when air temperatures exceed 28°C, reducing the need for evaporative cooling [6]. Southern yellow-billed hornbills, Tockus leucomelas, also use their bills as radiators to dump heat in hot conditions [9]. Heat loss via the bill can also be important in species with relatively small bills [11]; for example, although the bill of the song sparrow, Melospiza melodia, accounts for only about 2% of the bird's total surface area, it can shed up to 10% of the heat load [12].…”

“…In such conditions, birds may rely on heat loss from the bill via radiation and convection, the efficiency of which is unaffected by humidity (Andrew McKechnie and Blair Wolf, pers comm). This suggests adaptive advantages of larger bill sizes in hot, humid conditions [9,12,[19][20][21]. Allen's rule may therefore apply to humidity gradients as well as temperature gradients: large appendages should be particularly advantageous to birds inhabiting hot climates that are also humid [9,12].…”