Letter | Published:

A bony connection signals laryngeal echolocation in bats

Nature volume 463, pages 939942 (18 February 2010) | Download Citation

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & Auditory scene analysis by echolocation in bats. J. Acoust. Soc. Am. 110, 2207–2226 (2001)

  2. 2.

    Listening in the Dark (Yale Univ. Press, 1958)

  3. 3.

    & The evolution of echolocation in bats. Trends Ecol. Evol. 21, 149–156 (2006)

  4. 4.

    & Echolocation signals and pinnae movement in the fruit bat Rousettus aegyptiacus. Acta Chiropt. 7, 83–90 (2005)

  5. 5.

    , & eds. Echolocation in Bats and Dolphins (Univ. Chicago Press, 2004)

  6. 6.

    , , & Primitive early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–821 (2008)

  7. 7.

    , , & Why do shrews twitter? Communication or simple echo-based orientation. Biol. Lett. 5, 593–596 (2009)

  8. 8.

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

  9. 9.

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

  10. 10.

    , , & Signal strength, timing and self-deafening; the evolution of echolocation in bats. Paleobiology 21, 229–242 (1995)

  11. 11.

    & Echolocation by insect-eating bats. Bioscience 51, 557–569 (2001)

  12. 12.

    & 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)

  13. 13.

    & 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)

  14. 14.

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

  15. 15.

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

  16. 16.

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

  17. 17.

    , & Lehrbuch der Anatomie der Haustiere, Band I: Bewegungsaparat (Paul Parey, 1954)

  18. 18.

    & 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)

  19. 19.

    , , & Molecules consolidate the placental mammal tree. Trends Ecol. Evol. 19, 430–438 (2004)

  20. 20.

    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)

  21. 21.

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

  22. 22.

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

  23. 23.

    & Coordinated activities of middle-ear in echolocating bats. Science 191, 950–952 (1976)

  24. 24.

    , & 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)

  25. 25.

    , & Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J. Morphol. 228, 223–285 (1996)

  26. 26.

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

  27. 27.

    & No cost to echolocation for bats in flight. Nature 350, 421–423 (1991)

  28. 28.

    , , , & The direct examination of three-dimensional bone architecture in vitro by computed tomography. J. Bone Miner. Res. 4, 3–11 (1989)

  29. 29.

    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)

  30. 30.

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

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

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, Medical University of Vienna, Division of Human Health, 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. Search for Nina Veselka in:

  2. Search for David D. McErlain in:

  3. Search for David W. Holdsworth in:

  4. Search for Judith L. Eger in:

  5. Search for Rethy K. Chhem in:

  6. Search for Matthew J. Mason in:

  7. Search for Kirsty L. Brain in:

  8. Search for Paul A. Faure in:

  9. Search for M. Brock Fenton in:

Corresponding author

Correspondence to M. Brock Fenton.

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

Supplementary information

PDF files

  1. 1.

    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

Videos

  1. 1.

    Supplementary Movie 1

    This movie shows the arrangement of the hyoid apparatus in the common vampire bat Desmodus rotundus, a laryngeal echolocator.

  2. 2.

    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.

  3. 3.

    Supplementary Movie 3

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

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature08737

Further reading

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.