Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A bony connection signals laryngeal echolocation in bats

Nature volume 463, pages 939–942 (2010)Cite this article

Subjects

Abstract

Echolocation is an active form of orientation in which animals emit sounds and then listen to reflected echoes of those sounds to form images of their surroundings in their brains1. Although echolocation is usually associated with bats, it is not characteristic of all bats2,3. Most echolocating bats produce signals in the larynx, but within one family of mainly non-echolocating species (Pteropodidae), a few species use echolocation sounds produced by tongue clicks4,5. Here we demonstrate, using data obtained from micro-computed tomography scans of 26 species (n = 35 fluid-preserved bats), that proximal articulation of the stylohyal bone (part of the mammalian hyoid apparatus) with the tympanic bone always distinguishes laryngeally echolocating bats from all other bats (that is, non-echolocating pteropodids and those that echolocate with tongue clicks). In laryngeally echolocating bats, the proximal end of the stylohyal bone directly articulates with the tympanic bone and is often fused with it. Previous research on the morphology of the stylohyal bone in the oldest known fossil bat (Onychonycteris finneyi) suggested that it did not echolocate6, but our findings suggest that O. finneyi may have used laryngeal echolocation because its stylohyal bones may have articulated with its tympanic bones. The present findings reopen basic questions about the timing and the origin of flight and echolocation in the early evolution of bats. Our data also provide an independent anatomical character by which to distinguish laryngeally echolocating bats from other bats.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Stylohyal and tympanic bones.
Figure 2: Orientation of stylohyal and tympanic bones in non-echolocating, tongue-click-echolocating and laryngeally echolocating bats.
Figure 3: The stylohyal bone in an Eocene bat.

References

  1. Moss, C. F. & Surlykke, A. Auditory scene analysis by echolocation in bats. J. Acoust. Soc. Am. 110, 2207–2226 (2001)

    Article  ADS  CAS  Google Scholar 

  2. Griffin, D. R. Listening in the Dark (Yale Univ. Press, 1958)

    Google Scholar 

  3. Jones, G. & Teeling, E. C. The evolution of echolocation in bats. Trends Ecol. Evol. 21, 149–156 (2006)

    Article  Google Scholar 

  4. Holland, R. A. & Waters, D. A. Echolocation signals and pinnae movement in the fruit bat Rousettus aegyptiacus . Acta Chiropt. 7, 83–90 (2005)

    Article  Google Scholar 

  5. Thomas, J. A., Moss, C. F. & Vater, M. A. eds. Echolocation in Bats and Dolphins (Univ. Chicago Press, 2004)

    Google Scholar 

  6. Simmons, N. B., Seymour, K. L., Habersetzer, J. & Gunnell, G. F. Primitive early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–821 (2008)

    Article  ADS  CAS  Google Scholar 

  7. Siemers, B. M., Schauermann, G., Turni, H. & von Merten, S. Why do shrews twitter? Communication or simple echo-based orientation. Biol. Lett. 5, 593–596 (2009)

    Article  Google Scholar 

  8. Gould, E. Wing-clapping sounds of Eonycteris spelaea (Pteropodidae) in Malaysia. J. Mamm. 69, 378–379 (1988)

    Article  Google Scholar 

  9. Holderied, M. W. et al. Echolocation call intensity in the aerial hawking bat Eptesicus bottae (Vespertilionidae) studied using stereo videogrammetry. J. Exp. Biol. 208, 1321–1327 (2005)

    Article  Google Scholar 

  10. Fenton, M. B., Audet, D., Obrist, M. K. & Rydell, J. Signal strength, timing and self-deafening; the evolution of echolocation in bats. Paleobiology 21, 229–242 (1995)

    Article  Google Scholar 

  11. Schnitzler, H.-U. & Kalko, E. K. V. Echolocation by insect-eating bats. Bioscience 51, 557–569 (2001)

    Article  Google Scholar 

  12. Simmons, N. B. & Geisler, J. H. Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull. Am. Mus. Nat. Hist. 235, 1–182 (1998)

    Google Scholar 

  13. Reidenberg, J. S. & Laitman, J. T. Anatomy of the hyoid apparatus in Odontoceti (toothed whales): specializations of their skeleton and musculature compared with those of terrestrial mammals. Anat. Rec. 240, 598–624 (1994)

    Article  CAS  Google Scholar 

  14. Sprague, J. M. The hyoid region of placental mammals with especial reference to the bats. Am. J. Anat. 72, 385–472 (1943)

    Article  Google Scholar 

  15. Sprague, J. M. A study of the hyoid apparatus of the Cricetinae. J. Mamm. 22, 296–310 (1941)

    Article  Google Scholar 

  16. Müller, R. A numerical study of the role of the tragus in the big brown bat. J. Acoust. Soc. Am. 116, 3701–3712 (2004)

    Article  ADS  Google Scholar 

  17. Nickel, R., Schummer, A. & Seiferle, E. Lehrbuch der Anatomie der Haustiere, Band I: Bewegungsaparat (Paul Parey, 1954)

    Google Scholar 

  18. Hoffmeister, R. G. & Hoffmeister, D. F. The hyoid in North American squirrels, Sciuridae, with remarks on associated musculature. An. Inst. Biol. Univ. Nac. Auton. Mex. Ser. Zool. 52, 219–234 (1991)

    Google Scholar 

  19. Springer, M. S., Stanhope, M. J., Madsen, O. & de Jong, W. W. Molecules consolidate the placental mammal tree. Trends Ecol. Evol. 19, 430–438 (2004)

    Article  Google Scholar 

  20. van der Klaauw, C. J. The auditory bulla in some fossil mammals with a general introduction to this region of the skull. Bull. Am. Mus. Nat. Hist. 62, 1–352 (1931)

    Google Scholar 

  21. Wible, J. R. On the cranial osteology of the Hispaniolan solenodon Solenodon paradoxus Brandt, 1833 (Mammalia, Lipotyphla, Solenodontidaea). Ann. Carnegie Mus. 77, 321–402 (2008)

    Article  Google Scholar 

  22. Teeling, E. C. Hear, hear: the convergent evolution of echolocation in bats? Trends Ecol. Evol. 24, 351–354 (2009)

    Article  Google Scholar 

  23. Jen, P. H. & Suga, N. Coordinated activities of middle-ear in echolocating bats. Science 191, 950–952 (1976)

    Article  ADS  CAS  Google Scholar 

  24. Suthers, R. A., Hartley, D. J. & Wenstrup, J. J. The acoustic role of tracheal chambers and nasal cavities in the production of sonar pulses by the horseshoe bat, Rhinolophus hildebrandti . J. Comp. Physiol. A 162, 799–813 (1988)

    Article  CAS  Google Scholar 

  25. Cranford, T. W., Amundein, M. & Norris, K. S. Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J. Morphol. 228, 223–285 (1996)

    Article  CAS  Google Scholar 

  26. Mason, M. J. Evolution of the middle ear apparatus in talpid moles. J. Morphol. 267, 678–695 (2006)

    Article  Google Scholar 

  27. Speakman, J. R. & Racey, P. A. No cost to echolocation for bats in flight. Nature 350, 421–423 (1991)

    Article  ADS  CAS  Google Scholar 

  28. Feldkamp, L. A., Goldstein, S. A., Parfitt, A. M., Jesion, G. & Kleerekoper, M. The direct examination of three-dimensional bone architecture in vitro by computed tomography. J. Bone Miner. Res. 4, 3–11 (1989)

    Article  CAS  Google Scholar 

  29. McErlain, D. D. et al. Study of subchondral bone adaptations in a rodent surgical model of OA using in vivo micro-computed tomography. Osteoarthritis Cartilage 16, 458–469 (2008)

    Article  CAS  Google Scholar 

  30. Habersetzer, J. & Storch, G. Cochlea size in extant Chiroptera and Middle Eocene microchiropterans from Messel. Naturwissenschaften 79, 462–466 (1992)

    Article  ADS  Google Scholar 

Download references

Acknowledgements

We thank B. Clare, E. Fraser, B. Galef, L. Jakobsen, D. S. Johnston, L. Lazure, J. McNeil, S. Peters, J. Ratcliffe, D. Riskin, K. Seymour, J. A. Simmons, N. Simmons, J. Szewczak and H. Thewissen for comments on earlier versions of the manuscript, and K. Seymour, who arranged access to the O. finneyi specimen. We are particularly grateful to S. I. Pollmann, who assisted in the preparation of the Supplementary Movies. Our research was supported by an Operating Grant from the Canadian Institutes of Health Research (CIHR MOP-89852), and by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada. The McMaster Bat Lab is also supported by grants from the Canada Foundation for Innovation and the Ontario Innovation Trust.

Author Contributions All authors made essential contributions and helped to write the paper. N.V. and D.D.M. are joint first authors; N.V. was responsible for compiling and analysing the scans and D.D.M. was responsible for making them. D.W.H. provided the facilities for scanning; J.L.E. provided specimens from the Royal Ontario Museum mammals collections; R.K.C. suggested the initial idea of conducting MCT scans of bats and discussed the protocol for matching inner-ear and laryngeal anatomy, M.J.M. and K.L.B. provided expertise about the basicranium and hyoid apparatus in general; P.A.F. provided expertise in echolocation and neurobiology; and M.B.F. provided knowledge of bats and echolocation, and led the writing of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology,,

    Nina Veselka & M. Brock Fenton

  2. Imaging Research Laboratories, Robarts Research Institute,,

    David D. McErlain & David W. Holdsworth

  3. Department of Medical Biophysics, University of Western Ontario, London, Ontario N6A 5B7, Canada,

    David D. McErlain

  4. Department of Surgery, Schulich School of Medicine and Dentistry, University of Western Ontario, London, Ontario N6A 5K8, Canada,

    David W. Holdsworth

  5. Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada,

    Judith L. Eger

  6. Department of Radiology, Division of Human Health, Medical University of Vienna, 1090 Vienna, Austria

    Rethy K. Chhem

  7. Division of Human Health, International Atomic Energy Agency, Wagramer Strasse 5, PO Box 200, 1400 Vienna, Austria,

    Rethy K. Chhem

  8. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK,

    Matthew J. Mason & Kirsty L. Brain

  9. Department of Psychology, Neuroscience and Behaviour, McMaster University, Hamilton, Ontario L8S 4K1, Canada,

    Paul A. Faure

Authors
  1. Nina Veselka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David D. McErlain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David W. Holdsworth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Judith L. Eger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rethy K. Chhem
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matthew J. Mason
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kirsty L. Brain
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paul A. Faure
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. Brock Fenton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Brock Fenton.

Additional information

Catalogue numbers for all specimens examined from the Royal Ontario Museum mammals collections are given in the Supplementary Information.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-3 with Legends, Supplementary Table 1, Supplementary Notes, Supplementary References, Supplementary list of Specimens and Legends for Supplementary Movies 1-3 (PDF 1386 kb)

Supplementary Movie 1

This movie shows the arrangement of the hyoid apparatus in the common vampire bat Desmodus rotundus, a laryngeal echolocator. (MP4 4831 kb)

Supplementary Movie 2

This movie shows the arrangement of the hyoid apparatus in the Egyptian fruit bat Rousettus aegyptiacus, a pteropodid that echolocates with tongue clicks. (MP4 4907 kb)

Supplementary Movie 3

This movie shows the arrangement of the hyoid apparatus in Blanford's fruit bat Sphaerias blanfordi, a non-echolocating pteropodid. (MP4 4794 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Veselka, N., McErlain, D., Holdsworth, D. et al. A bony connection signals laryngeal echolocation in bats. Nature 463, 939–942 (2010). https://doi.org/10.1038/nature08737

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08737

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing