Journal of Comparative Physiology A

, Volume 198, Issue 9, pp 683–693

Convergence of reference frequencies by multiple CF–FM bats (Rhinolophus ferrumequinum nippon) during paired flights evaluated with onboard microphones

  • Yuto Furusawa
  • Shizuko Hiryu
  • Kohta I. Kobayasi
  • Hiroshi Riquimaroux
Original Paper

Abstract

The constant frequency component of the second harmonic (CF2) of echolocation sounds in Rhinolophus ferrumequinum nippon were measured using onboard telemetry microphones while the bats exhibited Doppler-shift compensation during flights with conspecifics. (1) The CF2 frequency of pulses emitted by individual bats at rest (Frest) showed a long-term gradual decline by 0.22 kHz on average over a period of 3 months. The mean neighboring Frest (interindividual differences in Frest between neighboring bats when the bats were arranged in ascending order according to Frest) ranged from 0.08 to 0.11 kHz among 18 bats in a laboratory colony. (2) The standard deviation of observed echo CF2 (reference frequency) for bats during paired flights ranged from 50 to 90 Hz, which was not significantly different from that during single flights. This finding suggests that during paired flights, bats exhibit Doppler-shift compensation with the same accuracy as when they fly alone. (3) In 60 % (n = 29) of the cases, the difference in the reference frequency between two bats during paired flights significantly decreased compared to when the bats flew alone. However, only 15 % of the cases (n = 7) showed a significant increase during paired flights. The difference in frequency between two bats did not increase even when the reference frequencies of the individuals were not statistically different during single flights.

Keywords

Jamming avoidance Reference frequency Resting frequency Doppler-shift compensation 

Abbreviations

BF

Best frequency

CF

Constant frequency

CF2

Constant frequency of the second harmonic component

DSC

Doppler-shift compensation

DSCF

Doppler-shifted constant frequency

FM

Frequency modulated

Frest

Resting frequency

IC

Inferior colliculus

IPI

Interpulse interval

JAR

Jamming avoidance response

TF

Terminal frequency

References

  1. Bartonicka T, Rehak Z, Gaisler J (2007) Can pipistrelles, Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus pygmaeus (Leach, 1825), foraging in a group, change parameters of their signals? J Zool 272:194–201CrossRefGoogle Scholar
  2. Bates ME, Stamper S, Simmons JA (2007) Jamming avoidance response of big brown bats in target detection. J Exp Biol 211:106–113CrossRefGoogle Scholar
  3. Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B 265:227–233CrossRefGoogle Scholar
  4. Bullock TH, Hamstra RH, Scheich H (1972a) The jamming avoidance response of high frequency electric fish. I. General features. J Comp Physiol A 77:1–22CrossRefGoogle Scholar
  5. Bullock TH, Hamstra RH, Scheich H (1972b) The jamming avoidance response of high frequency electric fish. II. Quantitative aspects. J Comp Physiol A 77:23–48CrossRefGoogle Scholar
  6. Chiu C, Xian W, Moss CF (2008) Flying in silence: echolocating bats cease vocalizing to avoid sonar jamming. Proc Natl Acad Sci USA 105:13116–13121PubMedCrossRefGoogle Scholar
  7. Chiu C, Xian W, Moss CF (2009) Adaptive echolocation behavior in bats for the analysis of auditory scenes. J Exp Biol 212:1392–1404PubMedCrossRefGoogle Scholar
  8. Esser KH (1994) Audio-vocal learning in a non-human mammal: the lesser spear-nosed bat Phyllostomus discolor. NeuroReport 5:1718–1720PubMedCrossRefGoogle Scholar
  9. 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
  10. Ghose K, Moss CF (2003) The sonar beam pattern of a flying bat as it tracks tethered insects. J Acoust Soc Am 114:1120–1131PubMedCrossRefGoogle Scholar
  11. Gillam EH, Ulanovsky N, McCracken GF (2007) Rapid jamming avoidance in biosonar. Proc R Soc Lond B 274:651–660CrossRefGoogle Scholar
  12. Griffin DR (1958) Listening in the dark. Yale University Press, New HavenGoogle Scholar
  13. Guillen A, Juste BJ, Ibáńez C (2000) Variation in the frequency of the echolocation calls of Hipposideros ruber in the Gulf of Guinea: an exploration of the adaptive meaning of the constant frequency value in rhinolophoid CF bats. J Evol Biol 13:70–80CrossRefGoogle Scholar
  14. Gustafson Y, Schnitzler HU (1979) Echolocation and obstacle avoidance in the hipposiderid bat Asellia tridens. J Comp Physiol A 131:161–167CrossRefGoogle Scholar
  15. Habersetzer J (1981) Adaptive echolocation in the bat Rhinopoma hardwickei. J Comp Physiol A 144:559–566CrossRefGoogle Scholar
  16. Habersetzer J, Schuller G, Neuweiler G (1984) Foraging behavior and Doppler shift compensation in echolocating hipposiderid bats, Hipposideros bicolor and Hipposideros speoris. J Comp Physiol 155:559–567CrossRefGoogle Scholar
  17. 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
  18. 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
  19. 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
  20. Hiryu S, Shiori Y, Hosokawa T, Riquimaroux H, Watanabe Y (2008) On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude. J Comp Physiol A 194:841–851CrossRefGoogle Scholar
  21. 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
  22. 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
  23. Ibáńez C, Juste J, Lopez-Wilchis R, Nunez-Garduno A (2004) Habitat variation and jamming avoidance in echolocation calls of the sac-winged bat (Balantiopteryx plicata). J Mammal 85:38–42CrossRefGoogle Scholar
  24. Jones G (1999) Scaling of echolocation call parameters in bats. J Exp Biol 202:3359–3367PubMedGoogle Scholar
  25. Jones G, Ransome RD (1993) Echolocation calls of bats are influenced by maternal effects and change over a lifetime. Proc R Soc Lond B 252:125–128CrossRefGoogle Scholar
  26. Jones G, Gordon T, Nightingale J (1992) Sex and age differences in the echolocation calls of the lesser horseshoe bats, Rhinolophu hipposideros. Mammalia 56:189–193Google Scholar
  27. Jones G, Morton M, Hughesand PM, Buden RM (1993) Echolocation, flight morphology and foraging strategies of some West African hipposiderid bats. J Zool Lond 230:385–400CrossRefGoogle Scholar
  28. Jones G, Sripathi K, Waters DA, Marimuthu G (1994) Individual variation in the echolocation calls of three sympatric Indian hipposiderid bats, and an experimental attempt to jam bat echolocation. Folia Zool 43:347–361Google Scholar
  29. Kazial KA, Burnett SC, Masters WM (2001) Individual and group variation in echolocation calls of big brown bats, Eptesicus fuscus (Chiroptera: Vespertilionidae). J Mammal 82:339–351CrossRefGoogle Scholar
  30. Knörnschild M, Nagy M, Metz M, Mayer F, Helversen OV (2010) Complex vocal imitation during ontogeny in a bat. Biol Lett 6:156–159PubMedCrossRefGoogle Scholar
  31. Masters WM, Jacobs SC, Simmons JA (1991) The structure of echolocation sounds used by the big brown bat Eptesicus fuscus: some consequences for echo processing. J Acoust Soc Am 89:1402–1413CrossRefGoogle Scholar
  32. Masters WM, Raver KAS, Kazial KA (1995) Sonar signals of big brown bats, Eptesicus fuscus, contain information about individual identity, age and family affiliation. Anim Behav 50:1243–1260CrossRefGoogle Scholar
  33. Miller LA, Degn HJ (1981) The acoustic behavior of four species of vespertilionid bats studied in the field. J Comp Physiol A 142:67–74CrossRefGoogle Scholar
  34. Necknig V, Zahn A (2011) Between-species jamming avoidance in Pipistrelles? J Comp Physiol A 197:469–473CrossRefGoogle Scholar
  35. Obrist MK (1995) Flexible bat echolocation: the influence of individual, habitat and conspecifics on sonar signal design. Behav Echol Sociobiol 36:207–219CrossRefGoogle Scholar
  36. 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
  37. Pye JD (1972) Bimodal distribution of constant frequencies in some hipposiderid bats (Mammalia: Hipposideridae). J Zool 66:323–335Google Scholar
  38. Riquimaroux H, Watanabe Y (2000) Characteristics of bat sonar sounds recorded by a telemetry system and a fixed ground microphone. In: Seventh western pacific regional acoustics conference (WESTPRACVII), pp 233–238Google Scholar
  39. Riquimaroux H, Gaioni SJ, Suga N (1991) Cortical computational maps control auditory perception. Science 251:565–568PubMedCrossRefGoogle Scholar
  40. Riquimaroux H, Gaioni SJ, Suga N (1992) Inactivation of the DSCF area of the auditory cortex with muscimol disrupts frequency discrimination in the mustached bat. J Neurophysiol 68:1613–1623PubMedGoogle Scholar
  41. Riquimaroux H, Watanabe Y, Lin LK (2002) Measurement of biosonar sounds of Taiwanese leaf-nosed bat by an on-board telemetry system: consistency of frequency components. Trans Tech Comm Psychol Physiol Acoust 32:271–276Google Scholar
  42. 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
  43. Schuller G (1980) Hearing characteristics and Doppler shift compensation in South Indian CF–FM bat. J Comp Physiol A 139:349–356CrossRefGoogle Scholar
  44. 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
  45. Simmons JA (1974) Response of the Doppler echolocation system in the bat, Rhinolophus ferrumequinum. J Acoust Soc Am 56:672–682PubMedCrossRefGoogle Scholar
  46. Simmons JA (2005) Big brown bats and June beetles: multiple pursuit strategies in a seasonal acoustic predator–prey system. Acoust Res Lett Online 6:238–242CrossRefGoogle Scholar
  47. Suga N (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Gall WE, Cowan WM, Edelman GM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 315–373Google Scholar
  48. 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
  49. Surlykke A, Moss CF (2000) Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am 108:2419–2429PubMedCrossRefGoogle Scholar
  50. 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
  51. Ulanovsky N, Fenton MB, Tsoar A, Korine C (2004) Dynamics of jamming avoidance in echolocating bats. Proc R Soc Lond B 271:1467–1475CrossRefGoogle Scholar
  52. Watanabe A, Takeda K (1963) The change of discharge frequency by A.C. stimulus in a weakly electric fish. J Exp Biol 40:57–66Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Yuto Furusawa
    • 1
  • Shizuko Hiryu
    • 1
  • Kohta I. Kobayasi
    • 1
  • Hiroshi Riquimaroux
    • 1
  1. 1.Faculty of Life and Medical Sciences, Neurosensing Bionavigation Research CenterDoshisha UniversityKyotanabeJapan

Personalised recommendations