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.

Fig 1. Measurements taken from Southern Yellow-billed Hornbills (Tockus leucomelas) to calculate surface areas for estimates of heat transfer.

Fig 2. Beak surface area increases as a function of body mass in Southern Yellow-billed Hornbills (Tockus leucomelas).

Data for nine males and nine females are shown.

Fig 3. A lateral image of a female Southern Yellow-billed Hornbill (Tockus leucomelas) with the beak backlit with a handheld flashlight, revealing the high degree of vascularity.

Fig 4. Thermal images of a female Southern Yellow-billed Hornbill (Tockus leucomelas) at different air temperatures.

Surface temperature (°C) is shown by the scale bar to the left of each image. Top left: the hornbill at air temperature (T_a) = 15°C: beak surface temperature (T_s__beak) matches background T_s. Top right: the hornbill at threshold T_a = 30.7°C, T_{s_beak} is changing, lower mandible first. Bottom left: the hornbill at air temperature (T_a) = 32.2°C, note that T_s__beak is much higher than that of the rest of the body and the environment, indicative of heat being radiated from the beak. Bottom right: the hornbill at T_a >T_b (T_a = 43°C). The beak is cooler than the surrounding environment and the bird is using evaporative water loss to keep cool, as indicated by the open beak panting behaviour.

Fig 5. Difference between surface temperature and air temperature (T_s-T_a) plotted against air temperature (T_a) of the torso (T_s__torso), gular skin (T_s__skin), the beak as a whole and lower mandible of the beak in Southern Yellow-billed Hornbills (Tockus leucomelas).

Error bars represent SE. Note that the scaling of the y-axes of the top two panels is different to that of the bottom two panels.