Journal of Comparative Physiology A

, Volume 197, Issue 5, pp 475–490

Complex echo classification by echo-locating bats: a review

  • Yossi Yovel
  • Matthias O. Franz
  • Peter Stilz
  • Hans-Ulrich Schnitzler
Review

Abstract

Echo-locating bats constantly emit ultrasonic pulses and analyze the returning echoes to detect, localize, and classify objects in their surroundings. Echo classification is essential for bats’ everyday life; for instance, it enables bats to use acoustical landmarks for navigation and to recognize food sources from other objects. Most of the research of echo based object classification in echo-locating bats was done in the context of simple artificial objects. These objects might represent prey, flower, or fruit and are characterized by simple echoes with a single up to several reflectors. Bats, however, must also be able to use echoes that return from complex structures such as plants or other types of background. Such echoes are characterized by superpositions of many reflections that can only be described using a stochastic statistical approach. Scientists have only lately started to address the issue of complex echo classification by echo-locating bats. Some behavioral evidence showing that bats can classify complex echoes has been accumulated and several hypotheses have been suggested as to how they do so. Here, we present a first review of this data. We raise some hypotheses regarding possible interpretations of the data and point out necessary future directions that should be pursued.

Keywords

Echolocation Classification Bat Statistics Behavior 

References

  1. Altes RA (1976) Sonar for generalized target description and its similarity to animal echolocation systems. J Acoust Soc Am 105:59–97Google Scholar
  2. Au WWL (1993) The sonar of Dolphins. Springer, New YorkGoogle Scholar
  3. Boonman A, Ostwald J (2007) A modeling approach to explain pulse design in bats. Biol Cybern 97:159–172Google Scholar
  4. Boonman AM, Parsons S, Jones G (2003) The influence of flight speed on the ranging performance of bats using frequency modulated echolocation pulses. J Acoust Soc Am 113:617–628PubMedCrossRefGoogle Scholar
  5. Borina F, Firzlaff U, Schuller G, Wiegrebe L (2008) Representation of echo roughness and its relationship to amplitude-modulation processing in the bat auditory midbrain. Eur J Neurosci 27:2724–2732PubMedCrossRefGoogle Scholar
  6. Bradbury JW (1970) Target discrimination by the echolocating Bat Vampyrum Spectrum. J Exp Zool 173:23–46PubMedCrossRefGoogle Scholar
  7. Firzlaff U, Schörnich S, Hoffmann S, Schuller G, Wiegrebe L (2006) A neural correlate of stochastic echo imaging. J Neurosci 26:785–791PubMedCrossRefGoogle Scholar
  8. Firzlaff U, Schuchmann M, Grunwald JE, Schuller G, Wiegrebe L (2007) Object-oriented echo perception and cortical representation in echolocating bats. PLoS Biol 5:e100PubMedCrossRefGoogle Scholar
  9. Fritz J, Shamma S, Elhiliali M, Klein D (2003) Rapid task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci 6:1216–1223PubMedCrossRefGoogle Scholar
  10. Griffin DR (1958) Listening in the dark. Yale University Press, New HavenGoogle Scholar
  11. Griffin DR (1967) Discriminative echolocation by bats in animal sonar systems biology and bionics. In: Busnel RG (ed) Laboratoire de Physiologie Acoustique. Jouyen-Josas, France, pp 273–300Google Scholar
  12. Griffin DR, Friend JH, Webster FA (1965) Target discrimination by the echolocation of bats. J Exp Zool 158:155–168PubMedCrossRefGoogle Scholar
  13. Grothe B, Covey E, Casseday JH (2001) Medial superior olive of the big brown bat: neuronal responses to pure tones, amplitude modulations, and pulse trains. J Neurophysiol 86:2219–2230PubMedGoogle Scholar
  14. Grunwald JE, Schornich S, Wiegrebe L (2004) Classification of natural textures in echolocation. Proc Natl Acad Sci USA 101:5670–5674PubMedCrossRefGoogle Scholar
  15. Habersetzer J, Vogler B (1983) Discrimination of surface-structured targets by the echolocating bat Myotis myotis during flight. J Comp Physiol A 152:275–282CrossRefGoogle Scholar
  16. Holderied MW, von Helversen O (2006) ‘Binaural echo disparity’ as a potential indicator of object orientation and cue for object recognition in echolocating nectar- feeding bats. J Exp Biol 209:3457–3468PubMedCrossRefGoogle Scholar
  17. Holderied MW, Jones G, von Helversen O (2006) Flight and echolocation behaviour of whiskered bats commuting along a hedgerow: range-dependent sonar signal design, Doppler tolerance and evidence for ‘acoustic focussing’. J Exp Biol 209:1816–1826PubMedCrossRefGoogle Scholar
  18. Kalko EKV, Condon MA (1998) Olfaction and fruit display: how bats find fruit of flagellichorous cucurbits. Funct Ecol 12:364–372CrossRefGoogle Scholar
  19. 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
  20. Konstantinov AI, Akhmarova NI (1968) Discrimination of targets by echolocation in Myotis oxygnathus. J Biol Sci Moscow Univ 4:22–28Google Scholar
  21. Levin E, Yom-Tov Y, Barnea A (2009) Frequent summer nuptial flights of ants provide a primary food source for bats. Naturwissenschaften 96:477–483PubMedCrossRefGoogle Scholar
  22. Matsuo I, Kunugiyama K, Yano M (2004) An echolocation model for range discrimination of multiple closely spaced objects: transformation of spectrogram into the reflected intensity distribution. J Acoust Soc Am 115:920–928PubMedCrossRefGoogle Scholar
  23. McDermott JH, Oxenham AJ, Simoncelli E (2009) Sound texture synthesis via filter statistics. Workshop on applications of signal processing to audio and acoustics. Mohonk, NYGoogle Scholar
  24. McKerrow P, Harper N (2001) Plant acoustic density profile model of CTFM. Ultrasonic sensing IEEE sensors J, pp 245–255Google Scholar
  25. Mogdans J, Schnitzler H-U, Ostwald J (1993) Discrimination of two-wavefront echoes by the big brown bat, Eptesicus fuscus: behavioral experiments and receiver simulations. J Comp Physiol A 172:309–323PubMedCrossRefGoogle Scholar
  26. Moss CF, Schnitzler H-U (1995) Behavioral studies of auditory information processing. Springer, BerlinGoogle Scholar
  27. Moss CF, Surlykke A (2001) Auditory scene analysis in echolocating in bats. J Acoust Soc Am 110:2207–2226PubMedCrossRefGoogle Scholar
  28. Müller R (2003) A computational theory for the classification of natural biosonar targets based on a spike code. Comput Neural Syst 14:595–612CrossRefGoogle Scholar
  29. Müller R, Kuc R (2000) Foliage echoes: a probe into the ecological acoustics of bat echolocation. J Acoust Soc Am 108:836–845PubMedCrossRefGoogle Scholar
  30. Ostwald J, Schnitzler H-U, Schuller G (1998) Target discrimination and target classification in echolocating bats. Plenum Press, New YorkGoogle Scholar
  31. Palmer AR, Russell IJ (1986) Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells. Hear Res 24:1–15PubMedCrossRefGoogle Scholar
  32. Patterson RD (1994) The sound of a sinusoid: spectralmodels. J Acoust Soc Am 96:1409–1418CrossRefGoogle Scholar
  33. Peremans H, Hallam J (1998) The spectrogram correlation and transformation receiver, revisited. J Acoust Soc Am 104:1101–1110PubMedCrossRefGoogle Scholar
  34. Pye JD (1980) Echolocation signals and echoes in air. In: Busnel RG, Fish JF (eds) Animal sonar systems. Plenum Press, New York, pp 309–353Google Scholar
  35. Saillant PA, Simmons JA, Dear SP, McMullen TA (1993) A computational model of echo processing and acoustic imaging in frequency-modulated echolocating bats: the spectrogram correlation and transformation receiver. J Acoust Soc Am 94:2691–2712PubMedCrossRefGoogle Scholar
  36. Sanderson MI, Simmons JA (2000) Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats. J Neurophysiol 83(4):1840–1855Google Scholar
  37. Sanderson MI, Neretti N, Simmons JA (2003) Evaluation of an auditory model for echo delay accuracy in wideband biosonar. J Acoust Soc Am 114:1648–1659PubMedCrossRefGoogle Scholar
  38. Schmidt S (1988) Evidence for a spectral basis of texture perception in bat sonar. Nature 331:617–619PubMedCrossRefGoogle Scholar
  39. Schmidt S (1992) Perception of structured phantom targets in the echolocating bat, Megaderma lyra. J Acoust Soc Am 91:2203–2223PubMedCrossRefGoogle Scholar
  40. Schmidt S, Hanke S, Pillat J (2000) The role of echolocation in the hunting of terrestrial prey—new evidence for an underestimated strategy in the gleaning bat Megaderma lyra. J Comp Physiol A 186:975–988PubMedCrossRefGoogle Scholar
  41. Schnitzler H-U, Henson OW (1980) Performance of aiborne animal sonar systems: I. Microchiroptera. Plenum Press, New YorkGoogle Scholar
  42. Schnitzler H-U, Menne D, Kober R, Heblich D (1983) The acoustical image of fluttering insects in echolocating bats. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology: roots and growing points, pp 235–250Google Scholar
  43. Schnitzler H-U, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evolut 18:386–394CrossRefGoogle Scholar
  44. Schörnich S, Wiegrebe L (2008) Phase sensitivity in bat sonar revisited. J Comp Physiol A 194:61–67CrossRefGoogle Scholar
  45. 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 155:121–128CrossRefGoogle Scholar
  46. Simmons JA, Chen L (1989) The acoustic basis for target discrimination by FM echolocating bats. J Acoust Soc Am 86:1333–1350PubMedCrossRefGoogle Scholar
  47. Simmons JA, Vernon JA (1971) Echolocation: discrimination of targets by the bat, Eptesicus fuscus. J Exp Zool 176:315–328PubMedCrossRefGoogle Scholar
  48. Simmons JA, Lavender WA, Lavender BA, Doroshow CA, Kiefer SW, Livingston R, Scallet AC, Crowley DE (1974) Target structure and echo spectral discrimination by echolocating bats. Science 186:1130–1132PubMedCrossRefGoogle Scholar
  49. Simmons JA, Ferragamo M, Moss CF, Stevenson SB, Altes RA (1990a) Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: the shape of target images in echolocation. J Comp Physiol A 167:589–616PubMedCrossRefGoogle Scholar
  50. Simmons JA, Moss CF, Ferragamo M (1990b) Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus. J Comp Physiol A 166:449–470PubMedGoogle Scholar
  51. Simon R, Holderied MW, von Helversen O (2006) Size discrimination of hollow hemispheres by echolocation in a nectar feeding bat. J Exp Biol 209:3599–3609PubMedCrossRefGoogle Scholar
  52. Skolnik Ml (2001) Introduction to RADAR systems. Mcgraw-Hill, New YorkGoogle Scholar
  53. Smith DR, Patterson RD, Turner R, Kawahara H, Irino T (2005) The processing and perception of size information in speech sounds. J Acoust Soc Am 117:305–318PubMedCrossRefGoogle Scholar
  54. Stilz P (2004) Akustische untersuchungen zur echoortung bei fledermauesen. Tier Phisiologie. University of Tuebingen. http://www.biosonarlab.uni-tuebingen.de/public/diss-stilz/diss.pdf
  55. Sum YW, Menne D (1988) Discrimination of fluttering targets by the FM-bat Pipistrellus stenopterus? J Comp Physiol A 163:349–354CrossRefGoogle Scholar
  56. Thies W, Kalko EKV, Schnitzler H-U (1998) The roles of echolocation and olfaction in two neotropical fruit-eating bats, Carollia perpiscillata and C. castanea, feeding on piper. Behav Ecol Sociobiol 42:397–409CrossRefGoogle Scholar
  57. Ulanovsky N, Moss CF (2008) What the bat’s voice tells the bat’s brain. Proc Natl Acad Sci USA 105:8491–8498PubMedCrossRefGoogle Scholar
  58. von Helversen D (2004) Object classification by echolocation in nectar feeding bats: size-independent generalization of shape. J Comp Physiol A 190:515–521CrossRefGoogle Scholar
  59. von Helversen D, von Helversen O (2003) Object recognition by echolocation: a nectar-feeding bat exploiting the flowers of a rain forest vine. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:327–336Google Scholar
  60. von Stebut B, Schmidt S (2001) Frequency discrimination threshold at search call frequencies in the echolocating bat Eptesicus fuscus. J Comp Physiol A 187:287–291CrossRefGoogle Scholar
  61. Webster FA, Brazier OG (1965) Experimental studies on target detection, evaluation and interception by echolocating bats. Springfield, VAGoogle Scholar
  62. Weissenbacher P, Wiegrebe L (2003) Classification of virtual objects in the echolocating bat Megaderma lyra. Behav Neurosci 117:833–839PubMedCrossRefGoogle Scholar
  63. Weissenbacher P, Wiegrebe L, Kössl M (2002) The effect of preceding sonar emission on temporal integration in the bat Megaderma lyra. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188(2):147–155Google Scholar
  64. Wiegrebe L (2008) An autocorrelation model of bat sonar. Biol Cybern 98:587–595PubMedCrossRefGoogle Scholar
  65. Yovel Y, Franz MO, Stilz P, Schnitzler HU (2008) Plant classification from bat-like echolocation signals. PLoS Comput Biol 4:e1000032PubMedCrossRefGoogle Scholar
  66. Yovel Y, Stilz P, Franz MO, Boonman A, Schnitzler H-U (2009) What a plant sounds like: the statistics of vegetation echoes as received by echolocating bats. PLoS Comput Biol 5:e1000429PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Yossi Yovel
    • 1
    • 3
  • Matthias O. Franz
    • 2
  • Peter Stilz
    • 3
  • Hans-Ulrich Schnitzler
    • 3
  1. 1.Department of NeurobiologyWeizmann Institute of ScienceRehovotIsrael
  2. 2.Faculty of InformaticsUniversity of Applied SciencesConstanceGermany
  3. 3.Animal Physiology, Institute of NeurobiologyUniversity of TuebingenTuebingenGermany

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