Animal Cognition

, Volume 16, Issue 6, pp 945–959

Perception of individuality in bat vocal communication: discrimination between, or recognition of, interaction partners?

  • Hanna B. Kastein
  • Rebecca Winter
  • A. K. Vinoth Kumar
  • Sripathi Kandula
  • Sabine Schmidt
Original Paper

Abstract

Different cognitive processes underlying voice identity perception in humans may have precursors in mammals. A perception of vocal signatures may govern individualised interactions in bats, which comprise species living in complex social structures and are nocturnal, fast-moving mammals. This paper investigates to what extent bats recognise, and discriminate between, individual voices and discusses acoustic features relevant for accomplishing these tasks. In spontaneous presentation and habituation–dishabituation experiments, we investigated how Megaderma lyra perceives and evaluates stimuli consisting of contact call series with individual-specific signatures from either social partners or unknown individuals. Spontaneous presentations of contact call stimuli from social partners or unknown individuals elicited strong, but comparable reactions. In the habituation–dishabituation experiments, bats dishabituated significantly to any new stimulus. However, reactions were less pronounced to a novel stimulus from the bat used for habituation than to stimuli from other bats, irrespective of familiarity, which provides evidence for identity discrimination. A model separately assessing the dissimilarity of stimuli in syllable frequencies, syllable durations and inter-call intervals relative to learned memory templates accounted for the behaviour of the bats. With respect to identity recognition, the spontaneous presentation experiments were not conclusive. However, the habituation–dishabituation experiments suggested that the bats recognised voices of social partners as the reaction to a re-habituation stimulus differed after a dishabituation stimulus from a social partner and an unknown bat.

Keywords

Bats Vocal communication Individual recognition Individual discrimination Social call perception Habituation–dishabituation paradigm 

Supplementary material

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Supplementary material 1_NOV (MP3 293 kb)
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Supplementary material 2_SP1 (MP3 293 kb)
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Supplementary material 3_SP2 (MP3 293 kb)
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Supplementary material 4_UNK (MP3 293 kb)
10071_2013_628_MOESM5_ESM.pdf (16 kb)
Supplementary material 5 (PDF 16 kb)
10071_2013_628_MOESM6_ESM.pdf (490 kb)
Supplementary material 6 (PDF 491 kb)

References

  1. Arnold BD, Wilkinson GS (2011) Individual specific contact calls of pallid bats (Antrozous pallidus) attract conspecifics at roosting sites. Behav Ecol Sociobiol 65:1581–1593CrossRefGoogle Scholar
  2. Balcombe JP (1990) Vocal recognition of pups by mother Mexican free-tailed bats, Tadarida brasiliensis mexicana. Anim Behav 39:960–966CrossRefGoogle Scholar
  3. Belin P, Fecteau S, Bédard C (2004) Thinking the voice: neural correlates of voice perception. Trends Cogn Sci 8:129–135CrossRefPubMedGoogle Scholar
  4. Belin P, Bestelmeyer PEG, Latinus M, Watson R (2011) Understanding voice perception. Br J Psychol 102:711–725CrossRefPubMedGoogle Scholar
  5. Blumstein DT, Daniel JC (2004) Yellow-bellied marmots discriminate between the alarm calls of individuals and are more responsive to calls from juveniles. Anim Behav 68:1257–1265CrossRefGoogle Scholar
  6. Bohn KM, Wilkinson GS, Moss CF (2007) Discrimination of infant isolation calls by female greater spear-nosed bats, Phyllostomus hastatus. Anim Behav 73:423–432CrossRefPubMedGoogle Scholar
  7. Bortz J, Lienert GA, Boehnke K (2000) Verteilungsfreie Methoden in der Biostatistik. Springer, Heidelberg, p 50CrossRefGoogle Scholar
  8. Boughman JW (1997) Greater spear-nosed bats give group-distinctive calls. Behav Ecol Sociobiol 40:61–70CrossRefGoogle Scholar
  9. Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732CrossRefPubMedGoogle Scholar
  10. Carter GG, Skowronski MD, Faure PA, Fenton B (2008) Antiphonal calling allows individual discrimination in white-winged vampire bats. Anim Behav 76:1343–1355CrossRefGoogle Scholar
  11. Charlton BD, Ellis WAH, McKinnon AJ, Brumm J, Nilsson K, Fitch WT (2011) Perception of male caller identity in koalas (Phascolarctos cinereus): acoustic analysis and playback experiments. PLoS One 6:e20329. doi:10.1371/journal.pone.0020329 CrossRefPubMedGoogle Scholar
  12. Charrier I, Mathevon N, Jouventin P (2002) How does a fur seal mother recognize the voice of her pup? An experimental study of Arctocephalus tropicalis. J Exp Biol 205:603–612PubMedGoogle Scholar
  13. Charrier I, Mathevon N, Jouventin P (2003) Fur seal mothers memorize subsequent versions of developing pups’ calls: adaptation to long-term recognition or evolutionary by-product? Biol J Linn Soc 80:305–312CrossRefGoogle Scholar
  14. Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–367CrossRefGoogle Scholar
  15. Cheney DL, Seyfarth RM (1982) Recognition of individuals within and between groups of free-ranging vervet monkeys. Am Zool 22:519–529Google Scholar
  16. Cheney DL, Seyfarth RM (1988) Assessment of meaning and the detection of unreliable signals by vervet monkeys. Anim Behav 36:477–486CrossRefGoogle Scholar
  17. Cheney DL, Seyfarth RM (1999) Recognition of other individuals’ social relationships by female baboons. Anim Behav 58:67–75CrossRefPubMedGoogle Scholar
  18. De Fanis E, Jones G (1995) The role of odour in the discrimination of conspecifics by pipistrelle bats. Anim Behav 49:835–839CrossRefGoogle Scholar
  19. Dörrie M, Schmidt S, Suba M, Sripathi K (2001) Contact calls of the bat Megaderma lyra: a comparison between an Indian and a Sri Lankan population. Diploma thesis, University of Veterinary Medicine Hannover FoundationGoogle Scholar
  20. Eaton JW, Bateman D, Hauberg S (2008) GNU Octave Manual Version 3. Network Theory LimitedGoogle Scholar
  21. Ehret G (1990) Categorical perception of sound signals: facts and hypotheses from animal studies. In: Harnad S (ed) Categorical perception. The groundwork of cognition. Cambridge University Press, Cambridge, pp 301–331Google Scholar
  22. Ehret G (2013) Sound communication in house mice: emotions in their voices and ears? In: Altenmüller E, Schmidt S, Zimmermann E (eds) From sounds in non-human mammals to speech and music in man. Oxford University Press, Oxford, pp 63–74CrossRefGoogle Scholar
  23. Eimas PD, Siqueland ER, Jusczyk P, Vigorito J (1971) Speech perception in infants. Science 171:303–306CrossRefPubMedGoogle Scholar
  24. Esser K-H, Schmidt U (1989) Mother–infant communication in the lesser spear-nosed bat Phyllostomus discolor (Chiroptera, Phyllostomidae)—evidence for acoustic learning. Ethology 82:156–168CrossRefGoogle Scholar
  25. Fenton MB (1994) Assessing signal variability and reliability: ‘to thine ownself be true’. Anim Behav 47:757–764CrossRefGoogle Scholar
  26. Fitch WT (2006) Production of vocalizations in mammals. In: Brown K (ed) Encyclopedia of language and linguistics, vol 10, 2nd edn. Elsevier, Oxford, pp 115–121Google Scholar
  27. Fitch WT (2010) The evolution of language. Cambridge University Press, Cambridge, pp 315–324CrossRefGoogle Scholar
  28. Frommolt K-H, Goltsman ME, Macdonald DW (2003) Barking foxes, Alopex lagopus: field experiments in individual recognition in a territorial mammal. Anim Behav 65:509–518CrossRefGoogle Scholar
  29. Gainotti G (2011) What the study of voice recognition in normal subjects and brain-damaged patients tells us about models of familiar people recognition. Neuropsychologia 49:2273–2282CrossRefPubMedGoogle Scholar
  30. Goymann W, Leippert D, Hofer H (2000) Sexual segregation, roosting, and social behaviour in a free-ranging colony of Indian false vampires (Megaderma lyra). Z Säugetierk 65:138–148Google Scholar
  31. Hare JF (1998) Juvenile Richardson’s ground squirrels, Spermophilus richardsonii, discriminate among individual alarm callers. Anim Behav 55:451–460CrossRefPubMedGoogle Scholar
  32. Holekamp KE, Boydston EE, Szykman M, Graham I, Nutt KJ, Birch S, Piskiel A, Singh M (1999) Vocal recognition in the spotted hyena and its possible implications regarding the evolution of intelligence. Anim Behav 58:383–395CrossRefPubMedGoogle Scholar
  33. Insley SJ (2001) Mother-offspring vocal recognition in northern fur seals is mutual but asymmetrical. Anim Behav 61:129–137CrossRefPubMedGoogle Scholar
  34. Janik VM, Sayigh LS, Wells RS (2006) Signature whistle shape conveys identity information to bottlenose dolphins. Proc Natl Acad Sci USA 103:8293–8297CrossRefPubMedGoogle Scholar
  35. Janßen S, Schmidt S (2009) Evidence for a perception of prosodic cues in bat communication: contact call classification by Megaderma lyra. J Comp Physiol A 195:663–672CrossRefGoogle Scholar
  36. Kazial KA, Kenny TL, Burnett SC (2008) Little brown bats (Myotis lucifugus) recognize individual identity of conspecifics using sonar calls. Ethology 114:469–478CrossRefGoogle Scholar
  37. Knörnschild M, von Helversen O (2008) Nonmutual vocal mother-pup recognition in the greater sac-winged bat. Anim Behav 76:1001–1009CrossRefGoogle Scholar
  38. Kreiman J, Sidtis D (2011) Foundations of voice studies. An interdisciplinary approach to voice production and perception. Wiley-Blackwell, BostonCrossRefGoogle Scholar
  39. Krumbholz K, Schmidt S (1999) Perception of complex tones and its analogy to echo spectral analysis in the bat, Megaderma lyra. J Acoust Soc Am 105:898–911CrossRefPubMedGoogle Scholar
  40. Kulzer E (2005) Chiroptera. In: Fischer MS, Schliemann H (eds) Handbuch der Zoologie, vol. 3, Biologie. W de Gruyter, Berlin, pp 175–176Google Scholar
  41. Lampe JF, Andre J (2012) Cross-modal recognition of human individuals in domestic horses (Equus caballus). Anim Cogn 15:623–630CrossRefPubMedGoogle Scholar
  42. Latinus M, Crabbe F, Belin P (2011) Learning-induced changes in the cerebral processing of voice identity. Cereb Cortex 21:2820–2828CrossRefPubMedGoogle Scholar
  43. Lemasson A, Boutin A, Boivin S, Blois-Heulin C, Hausberger M (2009) Horse (Equus caballus) whinnies: a source of social information. Anim Cogn 12:693–704CrossRefPubMedGoogle Scholar
  44. McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103–1109CrossRefPubMedGoogle Scholar
  45. McCulloch S, Boness DJ (2000) Mother-pup vocal recognition in the grey seal (Halichoerus grypus) of Sable Island, Nova Scotia, Canada. J Zool 251:449–455Google Scholar
  46. Miller CT, Bee MA (2012) Receiver psychology turns 20: is it time for a broader approach? Anim Behav 83:331–343CrossRefPubMedGoogle Scholar
  47. Müller CA, Manser MB (2008) Mutual recognition of pups and providers in the cooperatively breeding banded mongoose. Anim Behav 75:1683–1692CrossRefGoogle Scholar
  48. Neuner F, Schweinberger SR (2000) Neuropsychological impairments in the recognition of faces, voices, and personal names. Brain Cogn 44:342–366CrossRefPubMedGoogle Scholar
  49. Neuweiler G (1990) Auditory adaptations for prey capture in echolocating bats. Physiol Rev 70:615–641PubMedGoogle Scholar
  50. Neuweiler G (2000) The biology of bats. Oxford University Press, Oxford, pp 192–206Google Scholar
  51. Petkov CI, Kayser C, Steudel T, Whittingstall K, Augath M, Lohothetis NK (2008) A voice region in the monkey brain. Nat Neurosci 11:367–374CrossRefPubMedGoogle Scholar
  52. Pitcher BJ, Harcourt RG, Charrier I (2010) The memory remains: long-term vocal recognition in Australian sea lions. Anim Cogn 13:771–776CrossRefPubMedGoogle Scholar
  53. Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Natl Acad Sci USA 106:947–951CrossRefPubMedGoogle Scholar
  54. Reby D, Charlton BD (2012) Attention grabbing in red deer sexual calls. Anim Cogn 15:265–270CrossRefPubMedGoogle Scholar
  55. Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015CrossRefGoogle Scholar
  56. Rendall D, Notman H, Owren MJ (2009) Asymmetries in the individual distinctiveness and maternal recognition of infant contact calls and distress screams in baboons. J Acoust Soc Am 125:1792–1805CrossRefPubMedGoogle Scholar
  57. Sayigh LS, Tyack PL, Wells RS, Solow AR, Scott MD, Irvine AB (1998) Individual recognition in wild bottlenose dolphins: a field test using playback experiments. Anim Behav 57:41–50CrossRefGoogle Scholar
  58. Schmidt S (2013) Beyond echolocation: emotional acoustic communication in bats. In: Altenmüller E, Schmidt S, Zimmermann E (eds) From sounds in non-human mammals to speech and music in man. Oxford University Press, Oxford, pp 92–104CrossRefGoogle Scholar
  59. Schnitzler HU, Moss C, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394CrossRefGoogle Scholar
  60. Searby A, Jouventin P (2003) Mother-lamb acoustic recognition in sheep: a frequency coding. Proc R Soc Lond B 270:1765–1771CrossRefGoogle Scholar
  61. Sidtis D, Kreiman J (2012) In the beginning was the familiar voice: personally familiar voices in the evolutionary and contemporary biology of communication. Integr Psychol Behav 46:146–159CrossRefGoogle Scholar
  62. Siegel S (1985) Nichtparametrische statistische Methoden. Fachbuchhandlung für Psychologie Verlagsabteilung, Eschborn bei Frankfurt am Main, 2nd edn, p 85Google Scholar
  63. Siemers BM, Kerth G (2006) Do echolocation calls of wild colony-living Bechstein’s bats (Myotis bechsteinii) provide individual-specific signatures? Behav Ecol Sociobiol 59:443–454CrossRefGoogle Scholar
  64. Sliwa J, Duhamel J-R, Pascalis O, Wirth S (2011) Spontaneous voice-face identity matching by rhesus monkeys for familiar conspecifics and humans. Proc Natl Acad Sci USA 108:1735–1740CrossRefPubMedGoogle Scholar
  65. Snowdon CT, Cleveland J (1980) Individual recognition of contact calls by Pygmy marmosets. Anim Behav 28:717–727CrossRefGoogle Scholar
  66. Sproul C, Palleroni A, Hauser MD (2006) Cottontop tamarin, Saguinus oedipus, alarm calls contain sufficient information for recognition of individual identity. Anim Behav 72:1379–1385CrossRefGoogle Scholar
  67. Terrazas A, Serafin N, Hernández H, Nowak R, Poindron P (2003) Early recognition of newborn goat kids by their mother: II. Auditory recognition and evidence of an individual acoustic signature in the neonate. Dev Psychobiol 43:311–320CrossRefPubMedGoogle Scholar
  68. Thomson DE, Fenton MB, Barclay RMR (1985) The role of infant isolation calls in mother-infant reunions in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae). Can J Zool 63:1982–1988CrossRefGoogle Scholar
  69. Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537CrossRefPubMedGoogle Scholar
  70. Townsend SW, Hollén LI, Manser MB (2010) Meerkat close calls encode group-specific signatures, but receivers fail to discriminate. Anim Behav 80:133–138CrossRefGoogle Scholar
  71. Townsend SW, Allen C, Manser MB (2012) A simple test of vocal individual recognition in wild meerkats. Biol Lett 8:179–182CrossRefPubMedGoogle Scholar
  72. Tripovich JS, Charrier I, Rogers TL, Canfield R, Arnould JPY (2008) Acoustic features involved in the neighbour-stranger vocal recognition process in male Australian fur seals. Behav Process 79:74–80CrossRefGoogle Scholar
  73. Van Lancker DR, Canter GJ (1982) Impairment of voice and face recognition in patients with hemispheric damage. Brain Cogn 1:185–195CrossRefPubMedGoogle Scholar
  74. Van Lancker DR, Kreiman J (1987) Voice discrimination and recognition are separate abilities. Neuropsychologia 25:829–834CrossRefPubMedGoogle Scholar
  75. Van Lancker DR, Cummings JL, Kreiman J, Dobkin BH (1988) Phonagnosia: a dissociation between familiar and unfamiliar voices. Cortex 24:195–209CrossRefPubMedGoogle Scholar
  76. Voigt-Heucke SL, Taborsky M, Dechmann DKN (2010) A dual function of echolocation: bats use echolocation calls to identify familiar and unfamiliar individuals. Anim Behav 80:59–67CrossRefGoogle Scholar
  77. Yovel Y, Melcon ML, Franz MO, Denzinger A, Schnitzler HU (2009) The voice of bats: how greater mouse-eared bats recognize individuals based on their echolocation calls. PLoS Comput Biol 5:e1000400CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Hanna B. Kastein
    • 1
  • Rebecca Winter
    • 1
  • A. K. Vinoth Kumar
    • 2
  • Sripathi Kandula
    • 2
  • Sabine Schmidt
    • 1
  1. 1.Institute of ZoologyUniversity of Veterinary Medicine Hannover FoundationHannoverGermany
  2. 2.School of Biological SciencesMadurai Kamaraj UniversityMaduraiIndia

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