Advertisement

Journal of Comparative Physiology A

, Volume 200, Issue 9, pp 799–809 | Cite as

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task

  • Yuki Kinoshita
  • Daiki Ogata
  • Yoshiaki Watanabe
  • Hiroshi Riquimaroux
  • Tetsuo Ohta
  • Shizuko HiryuEmail author
Original Paper

Abstract

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°–100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat’s pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.

Keywords

Acoustical glints Fluttering moths Pulse direction 

Abbreviations

CF

Constant frequency

CF2

Constant frequency component with a second harmonic

FM

Frequency modulated

iFM

Initial frequency modulated

PI

Pulse interval

TF

Terminal frequency

tFM

Terminal frequency modulated

Notes

Acknowledgments

We thank Dr. Takuma Takanashi and Dr. Ryo Nakano for their valuable support. We also thank Nobutaka Urano for assistance in capturing bats in the field. This work was partly supported by a Grant-in-Aid for Young Scientists (A) (Grant No. 70449510) from the Japan Society for the Promotion of Science (JSPS). These experiments complied with the Principles of Animal Care, publication no. 86-23, revised 1985, of the National Institutes of Health, and with current Japanese laws. All experiments were approved by the Animal Experiment Committee at Doshisha University.

References

  1. Corcoran AJ, Barber JR, Conner WE (2009) Tiger moth jams bat sonar. Science 325:325–327PubMedCrossRefGoogle Scholar
  2. Fenton MB, Fullard JH (1979) The influence of moth hearing on bat echolocation strategies. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 132:77–86Google Scholar
  3. Fujioka E, Aihara I, Watanabe S, Hosokawa Y, Kasai R, Hiryu S, Simmons JA, Riquimaroux H, Watanabe Y Rapid shifts of sonar attention to multiple prey items by foraging echolocating bats (under review)Google Scholar
  4. 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
  5. 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
  6. Kober R, Schnitzler H-U (1990) Information in sonar echoes of fluttering insects available for echolocating bats. J Acoust Soc Am 87:882–896CrossRefGoogle Scholar
  7. Lancaster WC, Keating AW, Henson OW Jr (1992) Ultrasonic vocalizations of flying bats monitored by radiotelemetry. J Exp Biol 173:43–58PubMedGoogle Scholar
  8. Lancaster WC, Henson OW Jr, Keating AW (1995) Respiratory muscle activity in relation to vocalization in flying bats. J Exp Biol 198:175–191PubMedGoogle Scholar
  9. Link A, Marimuthu G, Neuweiler G (1986) Movement as a specific stimulus for prey catching behaviour in rhinolophid and hipposiderid bats. J Comp Physiol A 159:403–413CrossRefGoogle Scholar
  10. Mantani S, Hiryu S, Fujioka E, Matsuta N, Riquimaroux H, Watanabe Y (2012) Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 198:741–751PubMedGoogle Scholar
  11. Matsuta N, Hiryu S, Fujioka E, Yamada Y, Riquimaroux H, Watanabe Y (2013) Adaptive beam-width control of echolocation sounds by CF-FM bats, Rhinolophus ferrumequinum nippon, during prey-capture flight. J Exp Biol 216:1210–1218PubMedCrossRefGoogle Scholar
  12. Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51:570–581CrossRefGoogle Scholar
  13. Neuweiler G, Metzner W, Heilmann U, Rubsamen R, Eckrich M, Costa HH (1987) Foraging behavior and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behav Ecol Sociobiol 20:53–67CrossRefGoogle Scholar
  14. Novick A (1963) Pulse duration in the echolocation of insects by the bats, Pteronotus. Ergebnisse Biol 26:21–26Google Scholar
  15. Sano A (2006) Impact of predation by a cave-dwelling bat, Rhinolophus ferrumequinum, on the diapausing population of a troglophilic moth, Goniocraspidum preyeri. Ecol Res 21:321–324CrossRefGoogle Scholar
  16. Schnitzler HU, Denzinger A (2011) Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals. J Comp Physiol A 197:541–559CrossRefGoogle Scholar
  17. Schnitzler H-U, Flieger E (1983) Detection of oscillating target movements by echolocation. J Comp Physiol A 153:385–391CrossRefGoogle Scholar
  18. Schnitzler HU, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569CrossRefGoogle Scholar
  19. Schnitzler HU, Ostwald J (1983) Adaptations for the detection of fluttering insects by echolocation in Horseshoe bats. In: Ewert JP, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 801–827CrossRefGoogle Scholar
  20. Schnitzler HU, Hackbath H, Heilmann U, Herbert H (1985) Echolocation behavior of rufous horseshoe bats hunting for insects in the flycatcher-style. J Comp Physiol A 157:39–46CrossRefGoogle Scholar
  21. Schuller G (1984) Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol A 155:121–128CrossRefGoogle Scholar
  22. Surlykke A, Filskov M (1999) Auditory relationships to size in noctuid moths: bigger is better. Naturwissenschaften 86:238–241CrossRefGoogle Scholar
  23. Suthers RA, Thomas SP, Suthers BJ (1972) Respiration, wing-beat and ultrasonic pulse emission in an echo-locating bat. J Exp Biol 56:37–48Google Scholar
  24. 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
  25. Trappe M, Schnitzler HU (1982) Doppler-shift compensation in insect-catching horseshoe bats. Naturwissenschaften 69:193–194CrossRefGoogle Scholar
  26. Vogler B, Neuweiler G (1983) Echolocation in the noctule (Nyctalus noctula) and horseshoe bat (Rhinolophus ferrumequinum). J Comp Physiol A 152:421–432CrossRefGoogle Scholar
  27. von der Emde G, Menne D (1989) Discrimination of insect wingbeat-frequencies by the bat Rhinolophus ferrumequinum. J Comp Physiol A 164:663–671CrossRefGoogle Scholar
  28. von der Emde G, Schnitzler HU (1990) Classification of insects by echolocating greater horseshoe bats. J Comp Physiol A 167:423–430CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Yuki Kinoshita
    • 1
  • Daiki Ogata
    • 1
  • Yoshiaki Watanabe
    • 2
  • Hiroshi Riquimaroux
    • 2
  • Tetsuo Ohta
    • 1
  • Shizuko Hiryu
    • 2
    Email author
  1. 1.Faculty of Life and Medical SciencesDoshisha UniversityKyotanabeJapan
  2. 2.Faculty of Life and Medical Sciences, Neurosensing and Bionavigation Research CenterDoshisha UniversityKyotanabeJapan

Personalised recommendations