Journal of Comparative Physiology A

, Volume 192, Issue 5, pp 535–550 | Cite as

Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum

  • Jie Ma
  • Kohta Kobayasi
  • Shuyi Zhang
  • Walter MetznerEmail author
Original Paper


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.


Vocalization Social calls Echolocation Song Chiroptera 



Arched frequency modulated


Long noise burst


Short noise burst


Constant frequency


Complex constant frequency


Downward frequency modulated


Frequency modulated


Long constant frequency


Noise burst


Rippled frequency modulated


Short constant frequency


Sinusoidal frequency modulated


True constant frequency (echolocation pulse)


Upward frequency modulated



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.


  1. Aldridge HDJN, Obrist M, Merriam HG, Fenton MB (1990) Roosting vocalizations and foraging by the African bat Nycteris thebaica. J Mamm 71:242–246CrossRefGoogle Scholar
  2. Andrews MM, Andrews PT (2003) Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterol 5:221–234Google Scholar
  3. Balcombe JP (1990) Vocal recognition of pups by mother Mexican free-tailed bats Tadarida brasiliensis mexicana. Anim Behav 39:960–966CrossRefGoogle Scholar
  4. Balcombe JP, McCracken GF (1992) Vocal recognition in Mexican free-tailed bats do pups recognize mothers? Anim Behav 43:79–88CrossRefGoogle Scholar
  5. Barclay RMR (1982) Interindividual use of echolocation calls: eavesdropping by bats. Behav Ecol Sociobiol 10:271–275CrossRefGoogle Scholar
  6. Barlow KE, Jones G (1997) Function of pipistrelle social calls: field data and a playback experiment. Anim Behav 53:991–999CrossRefGoogle Scholar
  7. Behr O, Helversen Ov (2004) Bat serenades—complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol 56:106–115CrossRefGoogle Scholar
  8. Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B Biol Sci 265:227–233CrossRefGoogle Scholar
  9. Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732CrossRefPubMedGoogle Scholar
  10. Broughton WP (1963) Glossary. In: Burnel RG (ed) Acoustic behavior of animals. Elsevier, Boston, 883 ppGoogle Scholar
  11. Brown P (1976) Vocal communication in the Pallid Bat, Antrozous pallidus. Z Tierpsychol 41:34–54PubMedGoogle Scholar
  12. Davidson SM, Wilkinson GS (2002) Geographic and individual variation in vocalizations by male Saccopteryx bilineata (Chiroptera: Emballonuridae). J Mamm 83:526–535CrossRefGoogle Scholar
  13. Davison ML (1983) Multidimensional scaling. Wiley, New YorkGoogle Scholar
  14. Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Ann Rev Neurosci 22:567–631CrossRefPubMedGoogle Scholar
  15. Fenton MB (1977) Variations in the social calls of little brown bats (Myotis lucifugus). Can J Zool 55:1151–1157Google Scholar
  16. Fenton MB (1985) Communication in the Chiroptera. Indiana University Press, BloomingtonGoogle Scholar
  17. Fenton MB (1994) Assessing signal variability and reliability: ‘To thine ownself be true’. Anim Behav 47:757–764CrossRefGoogle Scholar
  18. 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 16:1974–1986CrossRefPubMedGoogle Scholar
  19. Heller KG, Helversen OV (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80:178–186Google Scholar
  20. Helversen OV, Helversen DV (1994) The advertisement call of the lesser noctule bat (Nyctalus leisleri). Folia Zool 43:331–338Google Scholar
  21. 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 913–916Google Scholar
  22. Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386CrossRefPubMedGoogle Scholar
  23. 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 225:71–84Google Scholar
  24. 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 43:347–362Google Scholar
  25. 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 96:1229–1254CrossRefPubMedGoogle Scholar
  26. Kingston T, Rossiter SJ (2004) Harmonic-hopping in Wallacea’s bats. Nature 429:654–657CrossRefPubMedGoogle Scholar
  27. Kolb A (1977) Wie erkennen sich Mutter und Junges des Mausohrs, Myotis myotis, bei der Rückkehr vom Jagdflug wieder? Z Tierpsychol 44:423–431PubMedGoogle Scholar
  28. Kroodsma DE (1977) A re-evaluation of song development in the song sparrow. Anim Behav 25:390–399CrossRefPubMedGoogle Scholar
  29. Lundberg K, Gerell R (1986) Territorial advertisement and mate attraction in the bat, Pipistrellus pipistrellus. Ethology 71:115–124CrossRefGoogle Scholar
  30. Ma T-S, French B, Pollak GD (2004) The advertisement and territorial calls of Mexican free-tailed bats. Bat Res News 45:WIN 4.238Google Scholar
  31. 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
  32. Matsumura S (1979) Mother–infant communication in a horseshoe bat (Rhinolophus ferrumequinum nippon): development of vocalization. J Mamm 60:76–84CrossRefGoogle Scholar
  33. Matsumura S (1981) Mother–infant communication in a horseshoe bay (Rhinolophus ferrumequinum nippon): vocal communication in three-week-old infants. J Mamm 62:20–28CrossRefGoogle Scholar
  34. 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 939–945Google Scholar
  35. Moss CF, Sinha SR (2003) Neurobiology of echolocation in bats. Curr Opin Neurobiol 13:751–758CrossRefPubMedGoogle Scholar
  36. Neuweiler G (2003) Evolutionary aspects of bat echolocation. J Comp Physiol A 189:245–256Google Scholar
  37. Neuweiler G, Schmidt S (1993) Audition in echolocating bats. Curr Opin Neurobiol 3:563–569CrossRefPubMedGoogle Scholar
  38. 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 20:53–67CrossRefGoogle Scholar
  39. Obrist M (1995) Flexible bat echolocation: the influence of individual, habitat, and conspecifics on sonar signal design. Behav Ecol Sociobiol 36:207–219CrossRefGoogle Scholar
  40. Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. J Zool Lond 261:21–33CrossRefGoogle Scholar
  41. Pye JD (1972) Bimodal distribution of constant frequencies in some Hipposiderid bats (Mammalia: Hipposideridae). J Zool Lond 166:323–335CrossRefGoogle Scholar
  42. 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 267:545–551CrossRefPubMedGoogle Scholar
  43. Rossiter SJ, Ransome RD, Faulkes CG, Le Comber SC, Jones G (2005) Mate fidelity and intra-lineage polygyny in greater horseshoe bats. Nature 437:408–411CrossRefPubMedGoogle Scholar
  44. 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 67:1005–1014CrossRefGoogle Scholar
  45. Russo D, Jones G (1999) The social calls of Kuhl’s pipistrelles Pipistrellus kuhlii (Kuhl, 1819): structure and variation (Chiroptera: Vespertilionidae). J Zool Lond 249:476–481CrossRefGoogle Scholar
  46. Schnitzler H-U, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569CrossRefGoogle Scholar
  47. Smotherman MS, Zhang S, Metzner W (2003) A neural basis for auditory feedback control of vocal pitch. J Neurosci 23:1464–1477PubMedGoogle Scholar
  48. 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)Google Scholar
  49. Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783–794CrossRefPubMedGoogle 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 101:2347–2364CrossRefPubMedGoogle Scholar
  51. Wilkinson GS, Wenrick-Boughman J (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Jie Ma
    • 1
  • Kohta Kobayasi
    • 1
  • Shuyi Zhang
    • 2
  • Walter Metzner
    • 1
    • 3
    Email author
  1. 1.Department of Physiological ScienceUCLA Los AngelesUSA
  2. 2.Institute of ZoologyChinese Academy of SciencesBeijingChina
  3. 3.Brain Research InstituteUCLALos AngelesUSA

Personalised recommendations