Habitat-specific divergence of air conditioning structures in bird bills

Abstract

We used high precision computed tomography (CT) and traditional radiography to study the nasal conchae, complex structures within the nasal cavity that condition air via countercurrent heat exchange. Air conditioning in the conchae assists thermoregulation and water balance, both of which pose challenges for many birds. We hypothesized that hot and water-limited environments would select for larger or more complex conchae to maximize moisture recapture during exhalation and in turn cause the evolution of deeper and wider bills. We provide the first intraspecific comparison of concha size and structure in birds based on CT scans of 15 individuals and radiographs of 39 individuals of 2 subspecies of Song Sparrow (Melospiza melodia) that inhabit climatically distinct habitats. CT scans revealed that middle and rostral conchae filled the nasal cavities and had larger surface areas in individuals with larger nasal cavities. The subspecies that inhabits hot and dry coastal dunes (M. m. atlantica) had relatively larger conchae and greater overlap of middle and rostral conchae than a nearby inland subspecies that inhabits moister environments (M. m. melodia). Radiographs revealed deeper and wider nasal cavities in the dune-endemic subspecies, further indicating they have larger conchae. Locations of maximum complexity of both conchae were more distal in the dune endemic subspecies. These anatomical differences suggest current or past divergent selection pressures on conchae; the larger conchae in the dune subspecies may allow greater water recapture while exhaling. The conchae and external bill are nested structures that were positively related in size and play functionally related roles in thermoregulation, therefore suggesting phenotypic integration. We hypothesize that the typically deeper and wider bill of the dune subspecies has evolved, at least in part, to accommodate larger conchae.