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

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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.

Zusammenfassung

Ein bisher unbeschriebenes Gefäßmerkmal im Mittelohr legt nahe, dass eine Wärmeaustauschstruktur zur Radiation kälteangepasster Singvögel beitrug.

Sperlingsvögel zeigen bisher nicht beschriebene Unterschiede im Verlauf der Arteria ophthalmica externa im Mittelohr, welche durch Untersuchung der beteiligten Knochenstrukturen einfach festgestellt werden können. In den Suboscines und den meisten Oscines außerhalb der Passerida verläuft die Arteria ophthalmica externa in demselben knöchernen Kanal wie die Vena ophthalmica externa. Dies stellt den plesiomorphen Zustand dar, der auch in Nicht-Sperlingsvögeln gefunden wird. In allen Muscicapoidea, Passeroidea, und Certhioidea, sowie in einigen anderen Taxa der Passerida und in wenigen Singvögeln außerhalb dieses Monophylums, verläuft die A. ophthalmica externa allerdings in einem eigenen Kanal und ist weit getrennt von der V. ophthalmica externa. Dieses abgeleitete Gefäßmerkmal stellt die erste morphologische Apomorphie einer größeren Untergruppe der Passerida dar und hat vermutlich eine physiologische Bedeutung. A. ophthalmica externa versorgt das Rete ophthalmicum, welches als Wärmeaustauschstruktur dient und die Augen- und Gehirntemperatur reguliert. Der abgeleitete Verlauf der A. ophthalmica externa wird hier als Anpassung zur Minimierung eines Wärmeverlustes des arteriellen Blutes interpretiert, bevor dieses das Auge und das Gehirn erreicht. Der abgeleitete Merkmalszustand tritt vor allem in Taxa auf, die in kalten Klimata vorkommen und könnte ein Schlüsselmerkmal darstellen, welches ein ganzjähriges Vorkommen dieser Vögel in hohen nördlichen Breiten ermöglicht.

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Acknowledgements

I thank Sven Tränkner for taking the photographs and an anonymous reviewer for comments that improved the manuscript.

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Correspondence to Gerald Mayr.

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Communicated by F. Bairlein.

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Mayr, G. A previously unnoticed vascular trait of the middle ear suggests that a cranial heat-exchange structure contributed to the radiation of cold-adapted songbirds. J Ornithol 160, 173–184 (2019). https://doi.org/10.1007/s10336-018-1588-2

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