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Ultrasonic frogs show hyperacute phonotaxis to female courtship calls

Abstract

Sound communication plays a vital role in frog reproduction1,2, in which vocal advertisement is generally the domain of males. Females are typically silent, but in a few anuran species they can produce a feeble reciprocal call3 or rapping sounds4 during courtship. Males of concave-eared torrent frogs (Odorrana tormota) have demonstrated ultrasonic communication capacity5. Although females of O. tormota have an unusually well-developed vocal production system6, it is unclear whether or not they produce calls or are only passive partners in a communication system dominated by males. Here we show that before ovulation, gravid females of O. tormota emit calls that are distinct from males’ advertisement calls, having higher fundamental frequencies and harmonics and shorter call duration. In the field and in a quiet, darkened indoor arena, these female calls evoke vocalizations and extraordinarily precise positive phonotaxis (a localization error of <1°), rivalling that of vertebrates with the highest localization acuity (barn owls7,8, dolphins, elephants and humans9). The localization accuracy of O. tormota is remarkable in light of their small head size (interaural distance of <1 cm), and suggests an additional selective advantage of high-frequency hearing beyond the ability to avoid masking by low-frequency background noise5.

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Figure 1: Female’s courtship call and male’s evoked vocal responses.
Figure 2: Males' phonotactic responses to a female’s courtship call.

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References

  1. Capranica, R. R. The Evoked Vocal Response of the Bullfrog: A Study of Communication by Sound (Research Monograph 33, MIT, Cambridge, Massachusetts, 1965)

    Google Scholar 

  2. Glaw, F. & Vences, M. A Fieldguide to the Amphibians and Reptiles of Madagascar 2nd edn (Vences & Glaw, Köln, Germany, 1994)

    Google Scholar 

  3. Roy, D. Communication signals and sexual selection in amphibians. Curr. Sci. 72, 923–927 (1997)

    Google Scholar 

  4. Tobias, M. L., Viswanathan, S. & Kelley, D. B. Rapping, a female receptive call, initiates male/female duets in the South African clawed frog. Proc. Natl Acad. Sci. USA 95, 1870–1875 (1998)

    Article  ADS  CAS  Google Scholar 

  5. Feng, A. S. et al. Ultrasonic communication in frogs. Nature 440, 333–336 (2006)

    Article  ADS  CAS  Google Scholar 

  6. Suthers, R. A. et al. Voices of the dead: Complex nonlinear vocal signals from the larynx of an ultrasonic frog. J. Exp. Biol. 209, 4984–4993 (2006)

    Article  Google Scholar 

  7. Knudsen, E. I., Blasdel, G. G. & Konishi, M. Sound localization by the barn owl (Tyto alba) measured with search coil technique. J. Comp. Physiol. A 133, 1–11 (1979)

    Article  Google Scholar 

  8. Bala, A. D. S., Spitzer, M. W. & Takahashi, T. T. Prediction of auditory spatial acuity from neural images on the owl’s auditory space map. Nature 424, 771–774 (2003)

    Article  ADS  CAS  Google Scholar 

  9. Heffner, R. S. & Masterton, R. B. in Comparative Perception Vol. I, Basic Mechanisms (eds Berkley, M. A. & Stebbins, W. C.) 285–314 (John Wiley & Sons, New York, 1990)

    Google Scholar 

  10. Cai, H.-X., Che, J., Pang, J.-F., Zhao, E.-M. & Zhang, Y.-P. Paraphyly of Chinese Amolops (Anura, Ranidae) and phylogenetic position of the rare Chinese frog, Amolops tormotus . Zootaxa 1531, 49–55 (2007)

    Article  Google Scholar 

  11. Narins, P. M. et al. Old world frog and bird vocalizations contain prominent ultrasonic harmonics. J. Acoust. Soc. Am. 115, 910–913 (2004)

    Article  ADS  Google Scholar 

  12. Feng, A. S., Narins, P. M. & Xu, C. H. Vocal acrobatics in a Chinese frog, Amolops tormotus . Naturwissenschaften 89, 352–356 (2002)

    Article  ADS  CAS  Google Scholar 

  13. Narins, P. M. & Smith, S. L. Clinal variation in anuran advertisement calls: Basis for acoustic isolation? Behav. Ecol. Sociobiol. 19, 135–141 (1986)

    Article  Google Scholar 

  14. Marquez, R. Female choice in the midwife toads (Alytes obstetricans and A. cisternasii). Behaviour 132, 151–161 (1995)

    Article  Google Scholar 

  15. McClelland, B. E., Wilczynski, W. & Ryan, M. J. Correlations between call characteristics and morphology in male cricket frogs (Acris crepitans). J. Exp. Biol. 199, 1907–1919 (1996)

    CAS  Google Scholar 

  16. Gerhardt, H. C. & Huber, F. Acoustic Communication in Insects and Anurans (Univ. Chicago Press, Chicago, 2002)

    Google Scholar 

  17. Narins, P. M., Feng, A. S., Fay, R. R. & Popper, A. N. Hearing and Sound Communication in Amphibians (Springer, New York, 2007)

    Google Scholar 

  18. Duellman, W. E. & Trueb, L. Biology of Amphibians (McGraw-Hill, New York, 1986)

    Google Scholar 

  19. Roy, D., Borah, B. & Sarma, A. Analysis and significance of female reciprocal call in frogs. Curr. Sci. 69, 265–270 (1995)

    Google Scholar 

  20. Kelley, D. B. & Tobias, M. L. in The Design of Animal Communication (eds Konishi, M. & Hauser, M.) 9–35 (MIT Press, Cambridge, Massachusetts, 1999)

    Google Scholar 

  21. Emerson, S. B. & Boyd, S. K. Mating vocalizations of female frogs: Control and evolutionary mechanisms. Brain Behav. Evol. 53, 187–197 (1999)

    Article  CAS  Google Scholar 

  22. Kelley, D. B. Vocal communication in frogs. Curr. Opin. Neurobiol. 14, 751–757 (2004)

    Article  CAS  Google Scholar 

  23. Rand, A. S. Is the canary singing? Froglog 48, 3 (2001)

    Google Scholar 

  24. Christensen-Dalsgaard, J. in Sound Source Localization (eds Popper, A. N. & Fay, R. R.) 67–123 (Springer, New York, 2005)

    Book  Google Scholar 

  25. Siemers, B. M. & Schnitzler, H.-U. Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429, 657–661 (2004)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Sciences Foundation of China (J.-X.S.), the National Institute on Deafness and Other Communication Disorders (A.S.F. and P.M.N.), the UCLA Academic Senate and the Paul S. Veneklasen Research Foundation (P.M.N.), and the National Science Foundation (A.S.F.).

Author Contributions J.-X.S., A.S.F. and P.M.N. were responsible for project planning. All authors (except P.M.N.) conducted the behavioural experiments, J.-X.S. and Z.-M.X. analysed the behavioural data and video recordings, and J.-X.S. and A.S.F. analysed the acoustic data. All authors contributed to writing the manuscript.

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Correspondence to Jun-Xian Shen.

Supplementary information

Supplementary Audio 1

The file contains Supplementary Audio 1 with phonotactic behaviour of males of Odorrana tormota in response to female courtship calls. In response to female courtship calls (FCs), males of O. tormota produced four types of vocal responses and displayed phonotactic movement toward the loudspeaker. (WMV 1552 kb)

Supplementary Audio 2

The file contains Supplementary Audio 2 with males of Odorrana tormota show hyperacute phonotaxis to female courtship calls. Upon hearing a female courtship call, a male of O. tormota usually oriented his body toward the loudspeaker – this was followed by a long-distance hop (range: 30 - 75 cm) toward the loudspeaker. The precision of the long-distance hops was remarkable, and the male soon reached the center of the diaphragm of the loudspeaker. (WMV 1208 kb)

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Shen, JX., Feng, A., Xu, ZM. et al. Ultrasonic frogs show hyperacute phonotaxis to female courtship calls. Nature 453, 914–916 (2008). https://doi.org/10.1038/nature06719

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