Journal of Comparative Physiology A

, Volume 161, Issue 6, pp 899–913

Ontogenesis of the echolocation system in the rufous horseshoe bat,Rhinolophus rouxi (Audition and vocalization in early postnatal development)

  • Rudolf Rübsamen
Article

Summary

  1. 1.

    The development of vocalization and hearing was studied in Sri Lankan horseshoe bats (Rhinolophus rouxi) during the first postnatal month. The young bats were caught in a nursing colony of rhinolophids in which birth took place within a two week period.

     
  2. 2.

    The new-born bats emitted isolation calls through the mouth. At the beginning these calls consisted of pure tones with frequencies below 10 kHz (Fig. 1). During the first postnatal week the call frequency increased to about 15 kHz, and the fundamental was augmented by two to four harmonics. No evoked potentials to pure tone stimuli could be elicited in the inferior colliculus of this age group, i.e., auditory processing at the midbrain level was not demonstrable.

     
  3. 3.

    Evoked potentials were first recorded in the second week, broadly tuned to 15–45 kHz, with a maximum sensitivity between 15–25 kHz. In the course of the second week, however, higher frequencies up to 60 kHz became progressively incorporated into the audiogram (Fig. 3). The fundamental frequency of the multiharmonic isolation calls, emitted strictly through the mouth, increased to about 20 kHz.

     
  4. 4.

    In the bats' third postnatal week an increased hearing sensitivity (auditory filter) emerged, sharply tuned at frequencies between 57 and 60 kHz (Fig. 4e). The same individuals were also the first to emit long constant frequency echolocation calls through the nostrils (Fig. 4c). The energy of the calls was arranged in harmonic frequency bands with the second harmonic exactly tuned to the auditory filter. These young bats continued to emit isolation calls through the mouth, which were, however, not harmonically related to the echolocation calls (Fig. 4b, d).

     
  5. 5.

    During the fourth week, both the auditory filter and the matched echolocation pulses (the second harmonic) shifted towards higher frequencies (Fig. 5). During the fifth week the fundamental frequency of the calls was progressively attenuated, and both the second harmonic of the pulses and the auditory filter reached the frequency range typical for adult bats of 73–78 kHz (Fig. 6).

     
  6. 6.

    The development of audition and vocalization is discussed with regard to possible interactions of both subsystems, and their incorporation into the active orientation system of echolocation.

     

Abbreviations

CF

constant frequency

FM

frequency modulated

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References

  1. Aitkin LM, Moore DR (1975) Inferior colliculus II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat. J Neurophysiol 38:1208–1216Google Scholar
  2. Brown PE, Grinnell AD (1980) Echolocation ontogeny in bats. In: Busnel R-G, Fish JF (eds) Animal sonar systems. Plenum Press, New York, pp 355–377Google Scholar
  3. Brown PE, Grinnell AD, Harrison JB (1978) The development of hearing in the Pallid bat,Antrozous pallidus. J Comp Physiol 126:169–182Google Scholar
  4. Bruns V (1976) Peripheral auditory tuning for fine frequency analysis by the CF-FM bat,Rhinolophus ferrumequinum. I. Mechanical specializations of the cochlea. J Comp Physiol 106:77–86Google Scholar
  5. Clopton BM, Winfield JA (1976) Effect of early exposure to patterned sound on unit activity in rat inferior colliculus. J Neurophysiol 39:1081–1089Google Scholar
  6. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209Google Scholar
  7. Gould E (1971) Studies of maternal-infant communication and development of vocalizations in the batsMyotis andEptesicus. Commun Behav Biol 5:263–313Google Scholar
  8. Gould E (1975) Neonatal vocalization in bats of eight genera. J Mammal 56:15–29Google Scholar
  9. Gould E (1979) Neonatal vocalizations of ten species of Malaysian bats (Megachiroptera and Microchiroptera). Am Zool 19:481–491Google Scholar
  10. Grinnell AD, Hagiwara S (1972) Adaptations of auditory nervous system for echolocation (Studies in New Guinea bats). Z Vergl Physiol 76:41–81Google Scholar
  11. Habersetzer J, Marimuthu G (1986) Ontogeny of sounds in the echolocating batHipposideros speoris. J Comp Physiol A 158:147–257Google Scholar
  12. Harris DM, Dallos P (1984) Ontogenetic changes in frequency mapping of mammalian ear. Science 225:741–743Google Scholar
  13. Konstantinov AI (1973) Development of echolocation in bats in postnatal ontogenesis. Period Biol 75:13–19Google Scholar
  14. Kraus H-J, Aulbach-Kraus K (1981) Morphological changes in the cochlea of the mouse after the onset of hearing. Hearing Res 4:89–102Google Scholar
  15. Matsumura S (1979) Mother infant communication in a Horseshoe bat (Rhinolophus ferrumequinum nippon): Development of vocalization. J Mammal 60:76–84Google Scholar
  16. Mayr E (1974) Behavioural programs and evolutionary strategies. Am Sci 62:650–659Google Scholar
  17. Moore DR (1983) Development of inferior colliculus and binaural audition. In: Romand R (ed) Development of auditory and vestibular system. Academic Press, New York London, pp 121–160Google Scholar
  18. Neuweiler G (1970) Neurophysiologische Untersuchungen zum Echoortungssystem der Großen HufeisennaseRhinolophus ferrumequinum. Z Vergl Physiol 67:273–306Google Scholar
  19. Neuweiler G (1977) Recognition mechanisms in echolocation of bats. In: Bullock TH (ed) Life Sci Res Rep 5:111–125Google Scholar
  20. Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH (1987) Foraging behaviour in the rufous horseshoe bat,Rhinolophus rouxi, of Sri Lanka. Behav Ecol Sociobiol 20:53–67Google Scholar
  21. Pujol R, Hilding D (1973) Anatomy and physiology of the onset of auditory function. Acta Otolaryngol 76:1–10Google Scholar
  22. Relkin EM, Saunders JC (1980) Displacement of the malleus in neonatal gold hamster. Acta Otolaryngol 90:6–15Google Scholar
  23. Rubel EW, Lippe WR, Ryals BM (1984) Development of the place principle. Ann Otol Rhinol Laryngol 93:609–615Google Scholar
  24. Scheich H (1983) Sensorimotor interfacing. In: Ewert J-P, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Publishing Corporation, New York London, pp 7–14Google Scholar
  25. Schnitzler H-U (1968) Die Ultraschall-Ortungslaute der Hufeisenfledermäuse (Chiroptera, Rhinolophidae) in verschiedenen Orientierungssituationen. Z Vergl Physiol 57:376–408Google Scholar
  26. Schuller G, Pollak G (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating Greater Horseshoe bats: Evidence for an acoustic fovea. J Comp Physiol 132:47–54Google Scholar
  27. Schuller G, Rübsamen R (1981) Laryngeal nerve activity during pulse emission in the CF-FM bat,Rhinolophus ferrumequinum. I. Superior laryngeal nerve (external motor branch). J Comp Physiol 143:317–321Google Scholar
  28. Schuller G, Suga N (1976) Laryngeal mechanisms for the emission of CF-FM sounds in the Doppler-shift compensating bat,Rhinolophus ferrumequinum. J Comp Physiol 107:253–262Google Scholar
  29. Schuller G, Beuter K, Schnitzler H-U (1974) Response to frequency shifted artificial echoes in the batRhinolophus ferrumequinum. J Comp Physiol 89:275–286Google Scholar
  30. Sewell GD (1970) Ultrasonic communication in rodents. Nature 227:410Google Scholar
  31. Shnerson A, Pujol R (1983) Development: Anatomy, electrophysiology and behaviour. In: Willott JF (ed) The auditory psychobiology of the house mouse. Thomas, Springfield, Illinois, pp 395–426Google Scholar
  32. Shnerson A, Willot JF (1979) Development of inferior colliculus response properties in C57BL/6J mouse pubs. Exp Brain Res 37:373–386Google Scholar
  33. Vater M (1987) Lightmicroscopic observations on cochlear development in horseshoe bats. Animal sonar systems. Helsingör Symposium, Plenum Press, New York London (in press)Google Scholar
  34. Vater M, Feng AS, Betz M (1985) An HRP-study of the frequency-place map of the horseshoe bat cochlea: Morphological correlates of the sharp tuning to a narrow frequency band. J Comp Physiol A 157:671–686Google Scholar
  35. Wiesel TN, Hubel DH (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26:1003–1017Google Scholar
  36. Wiesel TN, Hubel DH (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 28:1115–1156Google Scholar
  37. Zippelius HM, Schleidt (1956) Ultraschall-Laute bei jungen Mäusen. Naturwissenschaften 43:502Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • Rudolf Rübsamen
    • 1
    • 2
  1. 1.Zoologisches Institut der Universität MünchenMünchen 2Federal Republic of Germany
  2. 2.Lehrstuhl für Allgemeine ZoologieRuhr-Universität Bochum ND6/30Bochum 1Federal Republic of Germany

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