A previously unnoticed vascular trait of the middle ear suggests that a cranial heat-exchange structure contributed to the radiation of cold-adapted songbirds

Abstract

Passeriform birds exhibit previously unreported differences in the course of the arteria ophthalmica externa in the middle ear, which can easily be traced through examination of the involved osseous structures. In the Suboscines and most of the Oscines outside the clade Passerida, the arteria ophthalmica externa runs in the same osseous canal as the vena ophthalmica externa, which is the plesiomorphic condition that is also found in non-passeriform birds. In all Muscicapoidea, Passeroidea, and Certhioidea, as well as in several other taxa of the Passerida and a few songbirds outside this clade, however, the arteria ophthalmica externa is enclosed in its own canal and is widely separated from the vena ophthalmica externa. This derived vascular trait constitutes the first morphological apomorphy of a major subclade of the Passerida and is likely to be of physiological significance. The ophthalmic artery supplies the rete ophthalmicum, which serves as a heat-exchange structure and regulates the brain and eye temperature. The derived course of the arteria ophthalmica externa is here interpreted as an adaptation towards the minimization of heat loss of the arterial blood before it reaches the eye and the brain. The derived state predominantly occurs in taxa that occur in cool climates and may constitute a critical trait enabling the all-season occurrence of songbirds in far northern latitudes.