Letter | Published:

Fossil evidence of the avian vocal organ from the Mesozoic

Nature volume 538, pages 502505 (27 October 2016) | Download Citation

Abstract

From complex songs to simple honks, birds produce sounds using a unique vocal organ called the syrinx1,2. Located close to the heart at the tracheobronchial junction, vocal folds or membranes attached to modified mineralized rings vibrate to produce sound1,2,3,4,5,6,7. Syringeal components were not thought to commonly enter the fossil record6, and the few reported fossilized parts of the syrinx are geologically young8,9,10,11 (from the Pleistocene and Holocene (approximately 2.5 million years ago to the present)). The only known older syrinx is an Eocene specimen that was not described or illustrated12. Data on the relationship between soft tissue structures and syringeal three-dimensional geometry are also exceptionally limited5. Here we describe the first remains, to our knowledge, of a fossil syrinx from the Mesozoic Era, which are preserved in three dimensions in a specimen from the Late Cretaceous (approximately 66 to 69 million years ago) of Antarctica. With both cranial and postcranial remains, the new Vegavis iaai specimen is the most complete to be recovered from a part of the radiation of living birds (Aves). Enhanced-contrast X-ray computed tomography (CT) of syrinx structure in twelve extant non-passerine birds, as well as CT imaging of the Vegavis and Eocene syrinxes, informs both the reconstruction of ancestral states in birds and properties of the vocal organ in the extinct species. Fused rings in Vegavis form a well-mineralized pessulus, a derived neognath bird feature, proposed to anchor enlarged vocal folds or labia5. Left-right bronchial asymmetry, as seen in Vegavis, is only known in extant birds with two sets of vocal fold sound sources. The new data show the fossilization potential of the avian vocal organ and beg the question why these remains have not been found in other dinosaurs. The lack of other Mesozoic tracheobronchial remains, and the poorly mineralized condition in archosaurian taxa without a syrinx, may indicate that a complex syrinx was a late arising feature in the evolution of birds, well after the origin of flight and respiratory innovations.

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References

  1. 1.

    A Manual of the Anatomy of Vertebrate Animals (Appleton, 1872)

  2. 2.

    The Structure and Classification of Birds (Longmans, Green & Co, 1898)

  3. 3.

    Das Prinzip der Stimmbildung in der Wirbeltierreihe und beim Menschen (Akademische Verlagsgesellschaft, 1967)

  4. 4.

    The morphology of the syrinx in passerine birds. Bulletin of the Peabody Museum of Natural History Vol. 37 (Yale University, 1971)

  5. 5.

    Functional anatomy of the syrinxin Form and Function in Birds (eds & ) 4, 105–192. (Academic Press, 1989)

  6. 6.

    Birdsong and Evolution in Nature’s Music. The Science of Birdsong (eds and ) 296–317 (Elsevier, 2004)

  7. 7.

    & A new mechanism of sound generation in songbirds. Proc. Natl Acad. Sci. USA 94, 14787–14791 (1997)

  8. 8.

    A Pleistocene avifauna from Rock Spring, Florida. Wilson Bull. 71, 183–187 (1959)

  9. 9.

    & Descriptions of thirty-two new species of birds from the Hawaiian Islands: Part I. non-passeriformes. Ornithol. Monogr. 45, 38–42 (1991)

  10. 10.

    & The Lost World of the Moa: Prehistoric Life of New Zealand. (Indiana Univ. Press, 2002)

  11. 11.

    , , , & A new Mesembriornithinae (Aves, Phorusrhacidae) provides new insights into the phylogeny and sensory capabilities of terror birds. J. Vert. Paleont. 35, e912656 (2015)

  12. 12.

    & Presbyornis and the origin of the Anseriformes (Aves: Charadriomorphae). Smithson. Contrib. Zool. 323, 1–24 (1980)

  13. 13.

    Voices of the past: a review of Paleozoic and Mesozoic animal sounds. Hist. Biol. 20, 255–287 (2008)

  14. 14.

    Acoustic analyses of potential vocalization in lambeosaurine dinosaurs (Reptilia: Ornithischia). Paleobiology 7, 252–261 (1981)

  15. 15.

    Nasal cavity homologies and cranial crest function in lambeosaurine dinosaurs. Paleobiology 32, 109–125 (2006)

  16. 16.

    Communication and human uniqueness in The Evolution of Social Communication in Primates 219–227 (Springer, 2014)

  17. 17.

    et al. A bony connection signals laryngeal echolocation in bats. Nature 463, 939–942 (2010)

  18. 18.

    , , , & Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433, 305–308 (2005)

  19. 19.

    et al. Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. J. Anat. 228, 889–909 (2016)

  20. 20.

    et al. The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ. BMC Biol. 11, 1 (2013)

  21. 21.

    & Integrative physiology of fundamental frequency control in birds. J. Physiol. (Paris) 107, 230–242 (2013)

  22. 22.

    & The peculiar syrinx of Rhea Americana (Greater Rhea, Palaeognathae). Vertebr. Zool. 63, 321–327 (2013)

  23. 23.

    Tracheal anatomy of the Anatidae and its taxonomic significance. Wildfowl 12, 58–69 (1961)

  24. 24.

    Comparative behavior and relationships of the eiders. Condor 66, 113–129 (1964)

  25. 25.

    , , , & Coos, booms, and hoots: the evolution of closed-mouth vocal behavior in birds. Evolution 70, 1734–1746 (2016)

  26. 26.

    A new raptor-like bird from the Lower Eocene of North America and Europe. Senckenbergiana lethaea 80, 59–65 (2000)

  27. 27.

    , , & Combined phylogenetic analysis of a new North American fossil species confirms widespread Eocene distribution for stem rollers (Aves, Coracii). Zool. J. Linn. Soc. 157, 586–611 (2009)

  28. 28.

    et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014)

  29. 29.

    , , & Evolutionary origins of the avian brain. Nature 501, 93–96 (2013)

  30. 30.

    & Evolution in the social brain. Science 317, 1344–1347 (2007)

Download references

Acknowledgements

This project was funded by the Gordon and Betty Moore Foundation (grant GBMF4498; J.A.C., T.R. and F.G.), as well as the National Science Foundation (OPP ANT-1141820, OPP 0927341 and EAR 1355292; J.A.C.), C. Burke and the Agencia Nacional de Promoción Científica y Técnica (PICT 2010-066; F.E.N). The Instituto Antártico Argentino (IAA), G. M. Robles, W. J. Zinsmeister and especially C. A. Rinaldi, E. B. Olivero, and the Fuerza Aérea Argentina provided key support for fieldwork in 1993.

Author information

Affiliations

  1. Department of Geological Sciences, University of Texas at Austin, Austin, Texas 78756, USA

    • Julia A. Clarke
    •  & Zhiheng Li
  2. Museum of Texas Tech University, Box 43191, Lubbock, Texas 79409, USA

    • Sankar Chatterjee
  3. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China

    • Zhiheng Li
  4. Department of Physiology, Midwestern University, 19555 N 59th Avenue, Glendale, Arizona 85308, USA

    • Tobias Riede
  5. Conicet — Laboratorio de Anatomía Comparada y Evolución de los Vertebrados, Museo Argentino de Ciencias Naturales, Av. Ángel Gallardo 470, C1405DJR Buenos Aires, Argentina

    • Federico Agnolin
    • , Marcelo P. Isasi
    •  & Fernando E. Novas
  6. Fundación de Historia Natural “Félix de Azara”, Universidad Maimónides, Hidalgo 775, C1405BDB Buenos Aires, Argentina

    • Federico Agnolin
  7. Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah 84112, USA

    • Franz Goller
  8. Laboratorio de Geologia Andina, CADIC-Conicet, B.Houssay 200, CP V9410CAB Ushuaia, Tierra del Fuego, Argentina

    • Daniel R. Martinioni
  9. Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, CP C1405DJR Buenos Aires, Argentina

    • Francisco J. Mussel

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Contributions

D.R.M. and F.J.M. collected the fossil specimen and contributed geological data. M.P.I. and S.C. contributed to the fossil specimen preparation and study. T.R., F.G., Z.L. and J.A.C. designed the study of the syrinx and collected primary data. Z.L. designed the enhanced contrast CT protocol and collected extant CT data. J.A.C. discovered the fossil syrinx remains and designed the project with F.E.N., S.C., T.R. and F.G. J.A.C., Z.L., F.A., F.E.N., T.R., F.G. and S.C. conducted morphological study of the specimen.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Julia A. Clarke.

Reviewer Information

Nature thanks P. O’Connor and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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    This file contains Supplementary Methods, Supplementary Tables 1-4 and additional references.

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https://doi.org/10.1038/nature19852

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