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Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum

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Abstract

Whereas echolocation in horseshoe bats is well studied, virtually nothing is known about characteristics and function of their communication calls. Therefore, the communication calls produced by a group of captive adult greater horseshoe bats were recorded during various social interactions in a free-flight facility. Analysis revealed that this species exhibited an amazingly rich repertoire of vocalizations varying in numerous spectro-temporal aspects. Calls were classified into 17 syllable types (ten simple syllables and seven composites). Syllables were combined into six types of simple phrases and four combination phrases. The majority of syllables had durations of more than 100 ms with multiple harmonics and fundamental frequencies usually above 20 kHz, although some of them were also audible to humans. Preliminary behavioral observations indicated that many calls were emitted during direct interaction with and in response to social calls from conspecifics without requiring physical contact. Some echolocation-like vocalizations also appeared to clearly serve a communication role. These results not only shed light upon a so far widely neglected aspect of horseshoe bat vocalizations, but also provide the basis for future studies on the neural control of the production of communicative vocalizations in contrast to the production of echolocation pulse sequences.

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Abbreviations

AFM:

Arched frequency modulated

BNBl:

Long noise burst

BNBs:

Short noise burst

CF:

Constant frequency

CCF:

Complex constant frequency

DFM:

Downward frequency modulated

FM:

Frequency modulated

LCF:

Long constant frequency

NB:

Noise burst

RFM:

Rippled frequency modulated

SCF:

Short constant frequency

SFM:

Sinusoidal frequency modulated

TCF:

True constant frequency (echolocation pulse)

UFM:

Upward frequency modulated

References

  • Aldridge HDJN, Obrist M, Merriam HG, Fenton MB (1990) Roosting vocalizations and foraging by the African bat Nycteris thebaica. J Mamm 71:242–246

    Article  Google Scholar 

  • Andrews MM, Andrews PT (2003) Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterol 5:221–234

    Google Scholar 

  • Balcombe JP (1990) Vocal recognition of pups by mother Mexican free-tailed bats Tadarida brasiliensis mexicana. Anim Behav 39:960–966

    Article  Google Scholar 

  • Balcombe JP, McCracken GF (1992) Vocal recognition in Mexican free-tailed bats do pups recognize mothers? Anim Behav 43:79–88

    Article  Google Scholar 

  • Barclay RMR (1982) Interindividual use of echolocation calls: eavesdropping by bats. Behav Ecol Sociobiol 10:271–275

    Article  Google Scholar 

  • Barlow KE, Jones G (1997) Function of pipistrelle social calls: field data and a playback experiment. Anim Behav 53:991–999

    Article  Google Scholar 

  • Behr O, Helversen Ov (2004) Bat serenades—complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol 56:106–115

    Article  Google Scholar 

  • Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B Biol Sci 265:227–233

    Article  CAS  Google Scholar 

  • Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732

    Article  PubMed  Google Scholar 

  • Broughton WP (1963) Glossary. In: Burnel RG (ed) Acoustic behavior of animals. Elsevier, Boston, 883 pp

    Google Scholar 

  • Brown P (1976) Vocal communication in the Pallid Bat, Antrozous pallidus. Z Tierpsychol 41:34–54

    PubMed  CAS  Google Scholar 

  • Davidson SM, Wilkinson GS (2002) Geographic and individual variation in vocalizations by male Saccopteryx bilineata (Chiroptera: Emballonuridae). J Mamm 83:526–535

    Article  Google Scholar 

  • Davison ML (1983) Multidimensional scaling. Wiley, New York

    Google Scholar 

  • Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Ann Rev Neurosci 22:567–631

    Article  PubMed  CAS  Google Scholar 

  • Fenton MB (1977) Variations in the social calls of little brown bats (Myotis lucifugus). Can J Zool 55:1151–1157

    Google Scholar 

  • Fenton MB (1985) Communication in the Chiroptera. Indiana University Press, Bloomington

    Google Scholar 

  • Fenton MB (1994) Assessing signal variability and reliability: ‘To thine ownself be true’. Anim Behav 47:757–764

    Article  Google Scholar 

  • Fenzl T, Schuller G (2002) Periaqueductal gray and the region of the paralemniscal area have different functions in the control of vocalization in the neotropical bat, Phyllostomus discolor. Eur J Neurosci 16:1974–1986

    Article  PubMed  CAS  Google Scholar 

  • Heller KG, Helversen OV (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80:178–186

    Google Scholar 

  • Helversen OV, Helversen DV (1994) The advertisement call of the lesser noctule bat (Nyctalus leisleri). Folia Zool 43:331–338

    Google Scholar 

  • Henson OWJ, Henson MM, Kobler JB, Pollak GD (1980) The constant frequency component of the biosonar signals of the bat Pteronotus parnellii. In: Busnell R-G, Fish JF (eds) Animal sonar systems. Plenum Press, New York, pp 913–916

    Google Scholar 

  • Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386

    Article  PubMed  CAS  Google Scholar 

  • Jones G, Hughes PM, Rayner JMV (1991) The development of vocalizations in Pipistrellus pipistrellus (Chiroptera, Vespertilionidae) during post-natal growth and the maintenance of individual vocal signatures. J Zool Lond 225:71–84

    Google Scholar 

  • 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 43:347–362

    Google Scholar 

  • Kanwal JS, Matsumura S, Ohlemiller K, Suga N (1994) Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J Acoust Soc Am 96:1229–1254

    Article  PubMed  CAS  Google Scholar 

  • Kingston T, Rossiter SJ (2004) Harmonic-hopping in Wallacea’s bats. Nature 429:654–657

    Article  PubMed  CAS  Google Scholar 

  • Kolb A (1977) Wie erkennen sich Mutter und Junges des Mausohrs, Myotis myotis, bei der Rückkehr vom Jagdflug wieder? Z Tierpsychol 44:423–431

    PubMed  CAS  Google Scholar 

  • Kroodsma DE (1977) A re-evaluation of song development in the song sparrow. Anim Behav 25:390–399

    Article  PubMed  CAS  Google Scholar 

  • Lundberg K, Gerell R (1986) Territorial advertisement and mate attraction in the bat, Pipistrellus pipistrellus. Ethology 71:115–124

    Article  Google Scholar 

  • Ma T-S, French B, Pollak GD (2004) The advertisement and territorial calls of Mexican free-tailed bats. Bat Res News 45:WIN 4.238

    Google Scholar 

  • 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 50:1243–1260

    Article  Google Scholar 

  • Matsumura S (1979) Mother–infant communication in a horseshoe bat (Rhinolophus ferrumequinum nippon): development of vocalization. J Mamm 60:76–84

    Article  Google Scholar 

  • Matsumura S (1981) Mother–infant communication in a horseshoe bay (Rhinolophus ferrumequinum nippon): vocal communication in three-week-old infants. J Mamm 62:20–28

    Article  Google Scholar 

  • Möhres FP (1967) Communicative characters of sonar signals in bats. In: Busnel RG (ed) Animal sonar systems: biology and bionics. INRA-CNRS, Jouy-en-Josas, pp 939–945

    Google Scholar 

  • Moss CF, Sinha SR (2003) Neurobiology of echolocation in bats. Curr Opin Neurobiol 13:751–758

    Article  PubMed  CAS  Google Scholar 

  • Neuweiler G (2003) Evolutionary aspects of bat echolocation. J Comp Physiol A 189:245–256

    CAS  Google Scholar 

  • Neuweiler G, Schmidt S (1993) Audition in echolocating bats. Curr Opin Neurobiol 3:563–569

    Article  PubMed  CAS  Google Scholar 

  • Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH (1987) Foraging behaviour and echolocation in the rufous horseshoe bats, Rhinolophus rouxi, of Sri Lanka. Behav Ecol Sociobiol 20:53–67

    Article  Google Scholar 

  • Obrist M (1995) Flexible bat echolocation: the influence of individual, habitat, and conspecifics on sonar signal design. Behav Ecol Sociobiol 36:207–219

    Article  Google Scholar 

  • Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. J Zool Lond 261:21–33

    Article  Google Scholar 

  • Pye JD (1972) Bimodal distribution of constant frequencies in some Hipposiderid bats (Mammalia: Hipposideridae). J Zool Lond 166:323–335

    Article  Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD, Barratt EM (2000) Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proc Biol Sci 267:545–551

    Article  PubMed  CAS  Google Scholar 

  • Rossiter SJ, Ransome RD, Faulkes CG, Le Comber SC, Jones G (2005) Mate fidelity and intra-lineage polygyny in greater horseshoe bats. Nature 437:408–411

    Article  PubMed  CAS  Google Scholar 

  • Russ JM, Jones G, Mackie IJ, Racey PA (2004) Interspecific responses to distress calls in bats (Chiroptera: Vespertilionidae): a function for convergence in call design? Anim Behav 67:1005–1014

    Article  Google Scholar 

  • Russo D, Jones G (1999) The social calls of Kuhl’s pipistrelles Pipistrellus kuhlii (Kuhl, 1819): structure and variation (Chiroptera: Vespertilionidae). J Zool Lond 249:476–481

    Article  Google Scholar 

  • Schnitzler H-U, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569

    Article  Google Scholar 

  • Smotherman MS, Zhang S, Metzner W (2003) A neural basis for auditory feedback control of vocal pitch. J Neurosci 23:1464–1477

    PubMed  CAS  Google Scholar 

  • Smotherman M, Kobayasi K, Ma J, Zhang S, Metzner W (2006) A mechanism for vocal-respiratory coupling in the mammalian parabrachial nucleus. J Neurosci (in revision)

  • Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783–794

    Article  PubMed  CAS  Google Scholar 

  • Tian B, Schnitzler HU (1997) Echolocation signals of the greater horseshoe bat (Rhinolophus ferrumequinum) in transfer flight and during landing. J Acoust Soc Am 101:2347–2364

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson GS, Wenrick-Boughman J (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from NIH to WM (DC005400) and the National Science Foundation of China to SZ (30025007). We are particularly grateful to the Chinese Forestry Department for issuing the export permits and to Bing Liang, Jinshuo Zhang, and Zhanhui Tang for help with collecting the bats in China.

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Correspondence to Walter Metzner.

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Ma, J., Kobayasi, K., Zhang, S. et al. Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum . J Comp Physiol A 192, 535–550 (2006). https://doi.org/10.1007/s00359-006-0094-9

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  • DOI: https://doi.org/10.1007/s00359-006-0094-9

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