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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References
Alström P, Ericson PG, Olsson U, Sundberg P (2006) Phylogeny and classification of the avian superfamily Sylvioidea. Mol Phylogenet Evol 38:381–397
Barker FK, Barrowclough GF, Groth JG (2002) A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc R Soc Lond B Biol Sci 269:295–308
Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci USA 101:11040–11045
Baumel JJ (1993) Systema cardiovasculare. In: Baumel JJ, King AS, Breazile JE, Evans HE, Vanden Berge JC (eds) Handbook of avian anatomy: nomina anatomica avium, 2nd edn. Nuttall Ornithological Club, Cambridge, pp 407–475
Baumel JJ, Witmer LM (1993) Osteologia. In: Baumel JJ, King AS, Breazile JE, Evans HE, Vanden Berge JC (eds) Handbook of avian anatomy: nomina anatomica avium, 2nd edn. Nuttall Ornithological Club, Cambridge, pp 45–132
Bech C, Reinertsen RE (1989) Physiology of cold adaptation in birds. Plenum, New York
Bubién-Waluszewska A (1981) The cranial nerves. In: King AS, McLelland J (eds) Form and function in birds, vol 2. Academic Press, London, pp 385–438
Burgoon DA, Kilgore DL, Motta PJ (1987) Brain temperature in the Calliope Hummingbird (Stellula calliope): a species lacking a rete mirabile ophthalmicum. J Comp Physiol B Biochem Syst Environ Physiol 157:583–588
Cords E (1904) Beiträge zur Lehre vom Kopfnervensystem der Vögel. Anat Hefte 26:49–100
Del Hoyo J, Collar NJ (2016) HBW and BirdLife International illustrated checklist of the birds of the world. Volume 2: Passerines. Lynx Edicions, Barcelona
Ericson PGP, Johansson US (2003) Phylogeny of Passerida (Aves: Passeriformes) based on nuclear and mitochondrial sequence data. Mol Phylogenet Evol 29:126–138
Ericson PGP, Johansson US, Parsons TJ (2000) Major divisions in oscines revealed by insertions in the nuclear gene c-myc: a novel gene in avian phylogenetics. Auk 117:1069–1078
Ericson PGP, Christidis L, Cooper A, Irestedt M, Jackson J, Johansson US, Norman JA (2002) A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens. Proc R Soc Lond B Biol Sci 269:235–241
Ericson PGP, Irestedt M, Johansson US (2003) Evolution, biogeography, and patterns of diversification in passerine birds. J Avian Biol 34:3–15
Fjeldså J (2013) Avian classification in flux. In: del Hoyo J, Elliott A, Sargatal J, Christie D (eds) Handbook of birds of the world. Special volume: new species and global index. Lynx Edicions, Barcelona, pp 77–146
Fregin S, Haase M, Olsson U, Alström P (2012) New insights into family relationships within the avian superfamily Sylvioidea (Passeriformes) based on seven molecular markers. BMC Evol Biol 12:157
Fuchs J, Bowie RC, Fjeldså J, Pasquet E (2004) Phylogenetic relationships of the African bush-shrikes and helmet-shrikes (Passeriformes: Malaconotidae). Mol Phylogenet Evol 33:428–439
Fuchs J, Fjeldså J, Bowie RC, Voelker G, Pasquet E (2006) The African warbler genus Hyliota as a lost lineage in the Oscine songbird tree: molecular support for an African origin of the Passerida. Mol Phylogenet Evol 39:186–197
Fuchs J, Irestedt M, Fjeldså J, Couloux A, Pasquet E, Bowie RC (2012) Molecular phylogeny of African bush-shrikes and allies: tracing the biogeographic history of an explosive radiation of corvoid birds. Mol Phylogenet Evol 64:93–105
James HF, Ericson PGP, Slikas B, Lei FM, Gill FB, Olson SL (2003) Pseudopodoces humilis, a misclassified terrestrial tit (Paridae) of the Tibetan Plateau: evolutionary consequences of shifting adaptive zones. Ibis 145:185–202
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448
Johansson US, Fjeldså J, Bowie RC (2008) Phylogenetic relationships within Passerida (Aves: Passeriformes): a review and a new molecular phylogeny based on three nuclear intron markers. Mol Phylogenet Evol 48:858–876
Jønsson KA, Fjeldså J (2006) A phylogenetic supertree of oscine passerine birds (Aves: Passeri). Zool Scr 35:149–186
Kesteven HL (1925) The parabasal canal and nerve formina and canals in the bird skull. J Proc R Soc New South Wales 59:108–123
Kilgore DL, Bernstein MH, Hudson DM (1976) Brain temperatures in birds. J Comp Physiol B Biochem Syst Environ Physiol 110:209–215
Mayr G (2018) Size and number of the hypoglossal nerve foramina in the avian skull and their potential neuroanatomical significance. J Morphol 279:274–285
Midtgård U (1983) Scaling of the brain and the eye cooling system in birds: a morphometric analysis of the rete ophthalmicum. J Exp Zool A Ecol Genet Physiol 225:197–207
Midtgård U (1984) The blood vascular system in the head of the Herring Gull (Larus argentatus). J Morphol 179:135–152
Moyle RG, Cracraft J, Lakim M, Nais J, Sheldon FH (2006) Reconsideration of the phylogenetic relationships of the enigmatic Bornean Bristlehead (Pityriasis gymnocephala). Mol Phylogenet Evol 39:893–898
Moyle RG, Oliveros CH, Andersen MJ, Hosner PA, Benz BW, Manthey JD, Travers SL, Brown RM, Faircloth BC (2016) Tectonic collision and uplift of Wallacea triggered the global songbird radiation. Nat Commun 7:12709
Müller HJ (1961) Die Morphologie und Entwicklung des Craniums von Rhea americana Linné. I. Das knorpelige Neurocranium. Z Wiss Zool 165:221–319
Müller HJ (1963) Die Morphologie und Entwicklung des Craniums von Rhea americana Linné. II. Viszeralskelett, Mittelohr und Osteocranium. Z Wiss Zool 168:35–118
Njabo KY, Bowie RC, Sorenson MD (2008) Phylogeny, biogeography and taxonomy of the African wattle-eyes (Aves: Passeriformes: Platysteiridae). Mol Phylogenet Evol 48:136–149
Pettit TN, Whittow GC, Grant GS (1981) Rete mirabile ophthalmicum in Hawaiian seabirds. Auk 98:844–846
Pohlman AG (1921) The position and functional interpretation of the elastic ligaments in the middle-ear region of Gallus. J Morphol 35:229–262
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926
Saiff EI (1974) The middle ear of the skull of birds: the Procellariiformes. Zool J Linn Soc 54:213–240
Saiff E (1976) Anatomy of the middle ear region of the avian skull: Sphenisciformes. Auk 93:749–759
Saiff EI (1978) The middle ear of the skull of birds: the Pelecaniformes and Ciconiiformes. Zool J Linn Soc 63:315–370
Saiff EI (1981) The middle ear of the skull of birds: the ostrich, Struthio camelus L. Zool J Linn Soc 73:201–212
Saiff E (1988) The anatomy of the middle ear of the Tinamiformes (Aves: Tinamidae). J Morphol 196:107–116
Saiff E (2006) The middle ear region of the Falconiformes. Ann Carnegie Mus 75:69–96
Saiff E (2011) The middle ear region of the Cariamiformes (Aves). Ann Carnegie Mus 80:29–33
Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven
Spellman GM, Cibois A, Moyle RG, Winker K, Barker FK (2008) Clarifying the systematics of an enigmatic avian lineage: what is a bombycillid? Mol Phylogenet Evol 49:1036–1040
Starck JM (1995) Comparative anatomy of the external and middle ear of palaeognathous birds. Adv Anat Embryol Cell Biol 131:1–137
Stellbogen E (1930) Über das äussere und mittlere Ohr des Waldkauzes (Syrnium aluco L.). Z Morphol Ökol Tiere 19:686–731
Witmer LM (1990) The craniofacial air sac system of Mesozoic birds (Aves). Zool J Linn Soc 100:327–378
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I thank Sven Tränkner for taking the photographs and an anonymous reviewer for comments that improved the manuscript.
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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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DOI: https://doi.org/10.1007/s10336-018-1588-2