The evolution of the avian bill as a thermoregulatory organ

Abstract

The avian bill is a textbook example of how evolution shapes morphology in response to changing environments. Bills of seed-specialist finches in particular have been the focus of intense study demonstrating how climatic fluctuations acting on food availability drive bill size and shape. The avian bill also plays an important but under-appreciated role in body temperature regulation, and therefore in energetics. Birds are endothermic and rely on numerous mechanisms for balancing internal heat production with biophysical constraints of the environment. The bill is highly vascularised and heat exchange with the environment can vary substantially, ranging from around 2% to as high as 400% of basal heat production in certain species. This heat exchange may impact how birds respond to heat stress, substitute for evaporative water loss at elevated temperatures or environments of altered water availability, or be an energetic liability at low environmental temperatures. As a result, in numerous taxa, there is evidence for a positive association between bill size and environmental temperatures, both within and among species. Therefore, bill size is both developmentally flexible and evolutionarily adaptive in response to temperature. Understanding the evolution of variation in bill size however, requires explanations of all potential mechanisms. The purpose of this review, therefore, is to promote a greater understanding of the role of temperature on shaping bill size over spatial gradients as well as developmental, seasonal, and evolutionary timescales.

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

“…In combination with our finding for environmental determination of the species-level association between humidity and bill size, our results suggest that responses to contemporary change in climate will vary among populations of the same species. Our results support those of others who have emphasized the role of multiple environmental factors in shaping the evolution of bill morphology [8]. They also add to growing evidence that a narrow focus on temperature alone in studies of responses to climate change is overly simplistic and limits our understanding of species' sensitivities to climate change, and their capacity to adapt.…”

“…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].…”

It Takes Time to Be Cool: On the Relationship between Hyperthermia and Body Cooling in a Migrating Seaduck

“…Unlike endothermic mammals, however, birds lack sweat glands and thus rely on other mechanisms of effective heat loss. The respiratory tract, through panting or gular fluttering, plays an important role in evaporative heat loss in some species, while the plumage, skin, bill as well as the legs and feet are known important sites of heat exchange that may assist in alleviating the large water loss through the respiratory tract (Steen and Steen, 1965; Dawson, 1982; Giladi and Pinshow, 1999; Tattersall et al, 2016). Evaporative heat loss through the limbs has been well documented, notably in seabirds (Steen and Steen, 1965; Baudinette et al, 1976).…”

A test of a corollary of Allen's rule suggests a role for population density

“…We found a negative relationship between bill size and latitude (Fig. Consequently, saltmarsh sparrows are an indirect point of support for the Greenberg-Tattersall corollary, the positive correlation between bill surface area and summer temperatures (Tattersall et al 2017) in freshwater-limited environments, but highlight that this pattern can be obscured by other selective gradients. 3).…”

“…We did not include tarsus measurements, a standard metric of bird body size, because, like the bill, bird legs are keratinized extremities that could also be under selection for increased surface area in high environmental temperatures (Tattersall et al 2017). 3.02 (R Core Team) based on wing chord and the cubed root of mass (to convert this measurement to its one-dimensional component).…”