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Comparative anatomy of the postural mechanisms of the forelimbs of birds and mammals

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Abstract

One of the many differences between quadrupedal mammals and birds is that during standing, the forelimbs in mammals are involved in locomotion and support of the body, whereas the forelimbs of birds are involved in locomotion but not in body support. This dichotomy is reflected in the morphology and fiber types of the forelimb muscles. In mammals, the forelimb musculature forms a “pectoral sling” that suspends the trunk. Since mammals use the same muscles for postural and dynamic movements, their muscles possess a combination of slow and fast-contracting muscle fiber types that function in postural and dynamic activities. In a specific muscle, slow muscle fibers can perform postural actions via isometric contraction with minimal fatigue, whereas fast fibers can elicit dynamic, rapid, and forceful actions for locomotion. In contrast, the forelimb muscles of birds need only hold the wing folded while not in use. The muscles specialized for avian forelimb posture are comparatively small and consist entirely of slow fibers, and likely do not function in locomotion. In soaring birds, muscles with slow fibers also function isometrically and maintain the outstretched wing for extended lengths of time. Thus birds and mammals have evolved different strategies to deal with their forelimb postures and have different muscles specialized for posture.

Zusammenfassung

Einer der vielen Unterschiede zwischen vierbeinigen Säugetieren und Vögeln besteht darin, dass die Vorderbeine von Säugetieren sowohl an der Fortbewegung und als auch an der Unterstützung des Körpers beteiligt sind, wohingegen die Vorderbeine von Vögeln wohl an der Fortbewegung, jedoch nicht an der Körperunterstützung beteiligt sind. Dieser Unterschied spiegelt sich in der Struktur und den Muskelfasertypen der Vorderbeine wider. Bei Säugetieren bildet die Vorderbeinmuskulatur eine Brustschlinge, die den Rumpf aufhängt. Da Säugetiere die gleichen Muskeln für Haltung und Bewegung verwenden, besitzen ihre Muskeln eine Kombination aus langsam und schnell kontrahierenden Muskelfasertypen, die je nach Bedarf gezielt eingesetzt werden können. In einem bestimmten Muskel können langsame Muskelfasern isometrische Kontraktionen mit minimaler Ermüdung für die Haltung verantwortlich sein, während schnelle Fasern für schnelle und kraftvolle Fortbewegungen eingesetzt werden können. Im Gegensatz dazu werden die Vorderbeinmuskeln von Vögeln entweder für die gefaltete Haltung der Flügel oder zum Fliegen verwendet. Die Haltungsmuskeln der meisten Vögel sind vergleichsweise klein, bestehen ausschließlich aus langsamen Fasern und werden wahrscheinlich nicht beim Fliegen eingesetzt, aber bei hochfliegenden Vögeln funktionieren Muskeln mit langsamen Fasern isometrisch wie Haltungsmuskeln und halten die Flügel für längere Zeit ausgestreckt. In dieser Weise haben Vögel und Säugetiere für den Gebrauch ihrer Vorderbeine unterschiedliche Strategien und somit unterschiedliche Haltungsmuskeln entwickelt.

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Fig. 1

(modified from Gray 1968, and Homberger and Walker 2004)

Fig. 2

(modified from Evans and Christensen 1979)

Fig. 3
Fig. 4

(adapted from Meyers 1992a)

Fig. 5
Fig. 6

(b adapted from Fisher 1946 with permission)

Fig. 7

(adapted from Meyers 1993)

Fig. 8

(adapted from Meyers and Stakebake 2005)

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Notes

  1. Mammalian nomenclature from Nomina Anatomica Veterinaria (2017).

  2. Avian nomenclature from Vanden Berge and Zweers (1993).

  3. And is the source of a widely used slow myosin antibody (Shafiq et al. 1984).

  4. The lack of a functional explanation for its absence in this kingfisher is peculiar and should be investigated further.

  5. NAA 2nd edition does not describe any division of the M. pectoralis; thus I am proposing the nomenclature M. pectoralis superficialis and profundus for those species with the divided pectoralis muscle.

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Acknowledgements

I would like to thank Dr. Dominique G. Homberger, and Dr. Andrei Zinoviev for the invitation to participate in the 2018 International Ornithological Congress Symposium “Comparative aspects of avian morphology.” Dr. Dominique Homberger, Alexis Mathews, Chanel Ross, and two anonymous reviewers made valuable comments on the manuscript. Cindy Rehkemper and Beth Flint of the United States Fish and Wildlife Service (Hawaii) made the frigatebird specimen available. Chanel Ross performed the histochemical analysis of the frigatebird tissue. The ALD58 and F18 antibodies developed by D.A. Fischman and F.E. Stockdale, respectively, were obtained from the Developmental Studies Hybridoma Bank, created by the NICHD of the NIH and maintained at The University of Iowa, Department of Biology, Iowa City, IA 52242, USA. Weber State University and its Zoology Department provided funding for the research and travel to the 2018 International Ornithological Congress in Vancouver to present the keynote lecture.

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    Ron A. Meyers

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Meyers, R.A. Comparative anatomy of the postural mechanisms of the forelimbs of birds and mammals. J Ornithol 160, 869–882 (2019). https://doi.org/10.1007/s10336-019-01678-3

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