Journal of Comparative Physiology A

, Volume 194, Issue 9, pp 841–851 | Cite as

On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude

  • Shizuko Hiryu
  • Yu Shiori
  • Tatsuro Hosokawa
  • Hiroshi Riquimaroux
  • Yoshiaki Watanabe
Original Paper

Abstract

To understand complex sensory–motor behavior related to object perception by echolocating bats, precise measurements are needed for echoes that bats actually listen to during flight. Recordings of echolocation broadcasts were made from flying bats with a miniature light-weight microphone and radio transmitter (Telemike) set at the position of the bat’s ears and carried during flights to a landing point on a wall. Telemike recordings confirm that flying horseshoe bats (Rhinolophus ferrumequinum nippon) adjust the frequency of their sonar broadcasts to compensate for echo Doppler shifts. Returning constant frequency echoes were maintained at the bat’s reference frequency ±83 Hz during flight, indicating that the bats compensated for frequency changes with an accuracy equivalent to that at rest. The flying bats simultaneously compensate for increases in echo amplitude as target range becomes shorter. Flying bats thus receive echoes with both stabilized frequencies and stabilized amplitudes. Although it is widely understood that Doppler-shift frequency compensation facilitates detection of fluttering insects, approaches to a landing do not involve fluttering objects. Combined frequency and amplitude compensation may instead be for optimization of successive frequency modulated echoes for target range estimation to control approach and landing.

Keywords

Doppler-shift compensation Echo-intensity compensation Rhinolophus ferrumequinum nippon CF–FM bats 

Abbreviations

BF

Best frequency

CF

Constant frequency

CM

Cochlear microphonic

DSC

Doppler-shift compensation

FM

Frequency modulated

IPI

Interpulse interval

RF

Resting frequency

References

  1. Au WWL, Benoit-Bird KJ (2003) Automatic gain control in the echolocation system of dolphins. Nature 423:861–863PubMedCrossRefGoogle Scholar
  2. Boonman A, Jones G (2002) Intensity control during target approach in echolocating bats; stereotypical sensory–motor behaviour in Daubenton’s bats, Myotis daubentonii. J Exp Biol 205:2865–2874PubMedGoogle Scholar
  3. Edamatsu H, Suga N (1993) Differences in response properties of neurons between two delay-tuned areas in the auditory cortex of the mustached bat. J Neurophysiol 69:1700–1712PubMedGoogle Scholar
  4. Gaioni SJ, Riquimaroux H, Suga N (1990) Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. J Neurophysiol 64:1801–1817PubMedGoogle Scholar
  5. Griffin DR (1958) Listening in the dark. Yale University Press, New HavenGoogle Scholar
  6. Gustafson Y, Schnitzler HU (1979) Echolocation and obstacle avoidance in the hipposiderid bat Assellia tridens. J Comp Physiol A 131:161–167CrossRefGoogle Scholar
  7. Hartley DJ, Campbell KA, Suthers RA (1989) The acoustic behavior of the fish-catching bat, Noctilio leporinus, during pre-capture. J Acoust Soc Am 86:8–27CrossRefGoogle Scholar
  8. Henson OW Jr, Pollak GD, Kobler JB, Henson MM, Goldman LJ (1982) Cochlear microphonic potentials elicited by biosonar signals in flying bats, Pteronotus p. parnellii. Hear Res 7:127–147PubMedCrossRefGoogle Scholar
  9. Henson OW Jr, Bishop AL, Keating AW, Kobler JB, Henson MM, Wilson BS, Hansen R (1987) Bisonar imaging of insects by Pteronotus p. parnellii, the mustached bat. Nat Geor Res 3:82–101Google Scholar
  10. Henson OW, Koplas PA, Keating AW, Huffman RF, Henson MM (1990) Cochlear resonance in the mustached bat: behavioral adaptations. Hear Res 50:259–273PubMedCrossRefGoogle Scholar
  11. Hiryu S, Katsura K, Lin LK, Riquimaroux H, Watanabe Y (2005) Doppler-shift compensation in the Taiwanese leaf-nosed bat (Hipposideros terasensis) recorded with a telemetry microphone system during flight. J Acoust Soc Am 118:3927–3933PubMedCrossRefGoogle Scholar
  12. Hiryu S, Katsura K, Nagato T, Yamazaki H, Lin LK, Watanabe Y, Riquimaroux H (2006) Intra-individual variation in the vocalized frequency of the Taiwanese leaf-nosed bat, Hipposideros terasensis, influenced by conspecific colony members. J Comp Physiol A 192:807–815CrossRefGoogle Scholar
  13. Hiryu S, Hagino T, Riquimaroux H, Watanabe Y (2007) Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone. J Acoust Soc Am 121:1749–1757PubMedCrossRefGoogle Scholar
  14. Huffman RF, Henson OW Jr (1993a) Labile cochlear tuning in the mustached bat. I. Concomitant shifts in biosonar emission frequency. J Comp Physiol A 171:725–734PubMedCrossRefGoogle Scholar
  15. Huffman RF, Henson OW Jr (1993b) Labile cochlear tuning in the mustached bat. II. Concomitant shifts in neural tuning. J Comp Physiol A 171:735–748PubMedCrossRefGoogle Scholar
  16. Jen PH, Kamada T (1982) Analysis of orientation signals emitted by the CF–FM bat, Pteronotus p. parnellii and the FM bat, Eptesicus fuscus during avoidance of moving and stationary obstacles. J Comp Physiol A 148:389–398CrossRefGoogle Scholar
  17. Kick SA, Simmons JA (1984) Automatic gain control in the bat’s sonar receiver and the neuroethology of echolocation. J Neurosci 4:2725–2737PubMedGoogle Scholar
  18. Kobler JB, Wilson BS, Henson OW Jr, Bishop AL (1985) Echo intensity compensation by echolocating bats. Hear Res 20:99–108PubMedCrossRefGoogle Scholar
  19. Lancaster WC, Keating AW, Henson OW Jr (1992) Ultrasonic vocalizations of flying bats monitored by radiotelemetry. J Exp Biol 173:43–58PubMedGoogle Scholar
  20. Li S, Wang D, Wang K, Akamatsu T (2006) Sonar gain control in echolocating finless porpoises (Neophocaena phocaenoides) in an open water. J Acoust Soc Am 120(4):1803–1806PubMedCrossRefGoogle Scholar
  21. Metzner W (1993) An audio-vocal interface in echolocating horseshoe bats. J Neurosci 13:1899–1915PubMedGoogle Scholar
  22. Metzner W, Zhang S, Smotherman M (2002) Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency. J Exp Biol 205:1607–1616PubMedGoogle Scholar
  23. Moss CF, Surlykke A (2001) Auditory scene analysis by echolocation in bats. J Acoust Soc Am 110:2207–2226PubMedCrossRefGoogle Scholar
  24. Neumann I, Schuller G (1991) Spectral and temporal gating mechanisms enhance the clutter rejection in the echolocating bat, Rhinolophus rouxi. J Comp Physiol A 169:109–116PubMedCrossRefGoogle Scholar
  25. Neuweiler G (1970) Neurophysilogische Untersuchungen zum Echoortungssystem der groben Hufeisennase Rhinolophus ferrum equinum Schreber, 1774. Z Vergl Physiol 67:273–306CrossRefGoogle Scholar
  26. Neuweiler G (2000) The biology of bats. Oxford University Press, New YorkGoogle Scholar
  27. Ostwald J (1984) Tonotopical organization and pure tone response characteristics of single units in the auditory cortex of the greater horseshoe bat. J Comp Physiol A 155:821–834CrossRefGoogle Scholar
  28. Riquimaroux H, Watanabe Y (2000) Characteristics of bat sonar sounds recorded by a telemetry system and a fixed ground microphone. Seventh Western Pacific Regional Acoustics Conference (WESTPRACVII):233–238Google Scholar
  29. Riquimaroux H, Gaioni SJ, Suga N (1991) Cortical computational maps control auditory perception. Science 251:565–568PubMedCrossRefGoogle Scholar
  30. Schnitzler HU (1968) Die Ultraschallortungslaute der Hufeisen-Fledermäuse (Chiroptera-Rhinolophidae) in verschiedenen Orientierungssituationen [The ultrasonic sounds of horseshoe bats (Chiroptera-Rhinolophidae) in different orientation situations]. Z Vergl Physiol 57:376–408CrossRefGoogle Scholar
  31. Schnitzler HU, Henson OW Jr (1980) Performance of airborne animal sonar system, I. Microchiroptera. In: Busnel R-G, James FF (eds) Animal sonar systems. Plenum Press, New York, pp 109–181Google Scholar
  32. Schuller G, Beuter K, Schnitzler HU (1974) Response to frequency shifted artificial echoes in the bat Rhinolophus ferrumequinum. J Comp Physiol A 89:275–286CrossRefGoogle Scholar
  33. Simmons JA (1974) Response of the Doppler echolocation system in the bat, Rhinolophus ferrumequinum. J Acoust Soc Am 56:672–682PubMedCrossRefGoogle Scholar
  34. Smotherman M, Metzner W (2003) Fine control of call frequency by horseshoe bats. J Comp Physiol A 189:435–446CrossRefGoogle Scholar
  35. Suga N (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 315–373Google Scholar
  36. Suga N, Jen PH (1976) Disproportionate tonotopic representation for processing CF–FM sonar signals in the mustache bat auditory cortex. Science 194:542–544PubMedCrossRefGoogle Scholar
  37. Suga N, Niwa H, Taniguchi I, Margoliash D (1987) The personalized auditory cortex of the mustached bat: adaptation for echolocation. J Neurophysiol 58:643–654PubMedGoogle Scholar
  38. Taniguchi I (1985) Echolocation sounds and hearing of the greater Japanese horseshoe bat (Rhinolophus ferrumequinum nippon). J Comp Physiol A 156:185–188CrossRefGoogle Scholar
  39. Thomas JA, Moss CF, Vater M (2003) Echolocation in bats and dolphins. University of Chicago Press, ChicagoGoogle Scholar
  40. Tian B, Schnitzler HU (1997) Echolocation signals of the greater horseshoe bat (Rhinolophus ferrumequinum) in transfer flight and during landing. J Acoust Soc Am 101:2347–2364PubMedCrossRefGoogle Scholar
  41. Vogler B, Neuweiler G (1983) Echolocation in the noctule (Nyctalus noctula) and horseshoe bat (Rhinolophus ferrumequinum). J Comp Physiol A 152:421–432CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Shizuko Hiryu
    • 1
    • 3
  • Yu Shiori
    • 1
  • Tatsuro Hosokawa
    • 1
  • Hiroshi Riquimaroux
    • 1
    • 2
    • 3
  • Yoshiaki Watanabe
    • 1
    • 2
    • 3
  1. 1.Faculty of EngineeringDoshisha UniversityKyotanabeJapan
  2. 2.Bio-navigation Research CenterDoshisha UniversityKyotanabeJapan
  3. 3.Faculty of Life and Medical SciencesDoshisha UniversityKyotanabeJapan

Personalised recommendations