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Bioone COMPLETE BioOne COMPLETE Introduction to the Skeleton of Hummingbirds (Aves: Apodiformes, Trochilidae) in Functional and Phylogenetic Contexts Author: Zusi, Richard L., Division of Birds, National Museum of Natural History, P.O. Box 37012, Smithsonian Institution, Washington, D.C. 20013, USA Source: Ornithological Monographs No. 77 Published By: American Ornithological Society URL: https://doi.org/10.1525/om.2013.77.L1 BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Complete website, and all posted and associated content indicates your acceptance of BioOne's Terms of Use, available at www.bioone.org/terms-of-use. Usage of BioOne Complete content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Downloaded From: https://bioone.org/ebooks on 1/14/2019 Terms of Use: https://bioone.org/terms-of-use Access provided by University of New Mexico Ornithological Monographs Volume (2013), No. 77, 1-94 © The American Ornithologists' Union, 2013. Printed in USA. INTRODUCTION TO THE SKELETON OF HUMMINGBIRDS (AVES: APODIFORMES, TROCHILIDAE) IN FUNCTIONAL AND PHYLOGENETIC CONTEXTS R ic h a r d L. Z u s i1 Division of Birds, National Museum of Natural History, P.O. Box 37012, Smithsonian Institution, Washington, D.C. 20013, USA A bstract.—Historically, comparative study of the skeleton of hummingbirds has focused on systematics, emphasizing differences between hummingbirds and other birds and only rarely addressing differences within Trochilidae. This monograph covers both approaches, and comparisons within Trochilidae are framed within recently published, plausible phylogenetic hypotheses. The data are derived mainly from museum collections of anatomical specimens, covering ~256 species of 102 genera of hummingbirds, and 11 genera of other Apodiformes. Although the syringeal skeleton is included, emphasis is on the axial and appendicular skeletons. The first section deals with the syrinx and with skeletal features mainly associated with nectarivory and hovering, emphasizing characters that are unique to hummingbirds within Apodiformes. The syrinx of hummingbirds lies in the neck rather than the thorax and displays a unique bony knob on the surface of the tympanic membrane. During posthatching devel­ opment, the upper jaw of hummingbirds undergoes metamorphic changes that produce a morphology uniquely adapted for nectarivory within Aves. The ventral bars of the upper jaw lengthen and rotate to become lateral walls of an incompletely tubular bill that is completed by the closed mandibula, and lateral bowing (streptognathism) of the mandibula helps to seal the tube while a bird drinks nectar. Streptognathism of the opened jaw is used in display by some Hermits. The lamellar tip of the tongue required for nectar uptake also develops after fledging, while young are still fed by the parent. In Trochilines the nasal region changes from its configu­ ration by bone resorption during posthatching development. Cranial kinesis in hummingbirds is poorly documented, but structural differences in the upper jaw of Hermits and Trochilines imply differences in cranial kinesis. The palatum of hummingbirds is distinguished from that of other apodiforms by extreme reduction of the lateral part of the palatinum, greater width of the ventral choanal region, and by a median spine on the vomer. Otherwise the vomer is variable in shape and not compatible with aegithognathism. Among cranial features, the basipterygoid pro­ cess, lacrimale, and jugale are absent, and the interorbital septum is complete. The hyobranchial apparatus differs from that of other apodiforms in having an epibranchiale that is longer than the ceratobranchiale, and variably elongate in relation to body size. I hypothesize two modes of hyobranchial function—one applicable to moderate protrusion of the tongue (typical nectar eating), and another to extreme protrusion. The pelvis is less strongly supported by the synsa- crum, and the proximal portion of the hind limb is more reduced than in other Apodiformes. By contrast, the tarsometatarsus and flexor muscles of the toes are well developed in association with perching and clinging. In the flight mechanism, features uniquely pertinent to hovering are distinguished from those that support stiff-winged flight—the latter common to both swifts and hummingbirds. Hovering is especially dependent on adaptations for axial rotation of the wing at all major joints, and on extreme development in hummingbirds of the unusual wing proportions (short humerus and forearm, and long hand) and enlarged breast muscles found in swifts. Osteological characters of the Oligocene fossil Eurotrochilus that can be compared with modern hummingbirds do not indicate nectarivory or sustained hovering in that taxon. Present address: 802 NE 62nd Avenue, Apt. F, Hillsboro, Oregon 97124, USA. E-mail: [email protected] Ornithological Monographs, Number 77, pages 1-94. ISBN: 978-0-943610-96-2. © 2013 by The American Ornithologists' Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press's Rights and Permissions website, http://www.ucpressjournals.com/reprintInfo.asp. DOI: 10.1525/om.2013.77.1.1. 1 Downloaded From: https://bioone.org/ebooks on 1/14/2019 Terms of Use: https://bioone.org/terms-of-use Access provided by University of New Mexico 2 ORNITHOLOGICAL MONOGRAPHS NO. 77 In the second section, variations within Trochilidae are described and their distributions within the major clades (Hermits, Topazes, Mangoes, Brilliants, Coquettes, Patagona, Mountain Gems, Bees, and Emeralds) are specified. Most diverse are the jaw mechanism, nasal region and con- chae, hyobranchial apparatus, cranial proportions, crests, and pneumatic inflation, structure of the ribcage based on number of ribs attached to the sternum, pectoral girdle, and various humeral characters. Other noteworthy but largely unexplained variation characterizes the hyobranchial apparatus of H eliodoxa, the humerus of the "P ygm ornis group" of Phaethornis, sexual dimorphism in numbers of thoracic ribs, and synostosis of phalanges of the foot. Although Hermits display distinctive characters, their subfamily status is uncertain for lack of informative outgroups. Major trochilid clades are either weakly supported or unsupported by uniquely derived characters, but apomorphic variation within Mangoes suggests recognition of an Anthracothorax group of genera, and within Emeralds, a large A m azilia group. Each of the major trochilid clades displays con­ siderable diversity in body size and skeletal characters, and numerous characters show parallel evolution within the family. Intraspecific variation is widespread, and selected examples are high­ lighted. Patterns of skeletal variations at multiple levels of phylogeny suggest that some varia­ tions characterizing higher levels had their origins at the intraspecific level. A list of unsolved problems of functional morphology of the skeleton in hummingbirds is offered. Especially intriguing are the many posthatching changes in development of the feeding mechanism and the challenge of incorporating morphological data and their implications into models of evolu­ tion of hummingbird communities. Received 17 September 2012, accepted 8 February 2013. Key words: Trochilidae, Apodiformes, comparative osteology, myology, inter- and intraspecific variation, nectarivory, hovering, Eurotrochilus. Introducción al Esqueleto de los Colibríes (Aves: Apodiformes: Trochilidae) en Contextos Funcionales y Filogenéticos Resumen.—El estudio comparativo del esqueleto de los colibríes históricamente se ha enfo­ cado en la sistemática, enfatizando las diferencias entre los colibríes y otras aves, y rara vez se han evaluado las diferencias dentro de Trochilidae. Esta monografía cubre ambas aproximacio­ nes y las comparaciones dentro de Trochilidae se enmarcan en hipótesis filogenéticas plausibles y publicadas recientemente. Los datos se derivan principalmente de colecciones de museo de especímenes anatómicos, abarcando ~256 especies de 102 géneros de colibríes y 11 géneros de otros Apodiformes. Aunque se considera el esqueleto de la siringe, se hace énfasis en el esqueleto axial y el apendicular. La primera sección trata de la siringe y de las características del esqueleto asociadas prin­ cipalmente con la nectarivoría y el revoloteo, con énfasis en caracteres que son únicos de los colibríes al interior de Apodiformes. La siringe de los colibríes se ubica en el cuello en vez de en el tórax y muestra una protuberancia ósea en la superficie de la membrana timpánica. Durante el desarrollo posterior a la eclosión, la maxila de los colibríes pasa por una metamorfosis que resulta en una morfología adaptada para la nectarivoría que es única entre las aves. Las bar­ ras ventrales de la maxila se elongan y rotan para convertirse en las paredes laterales de un pico tubular incompleto que se completa por la
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