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
Andrews MM, Andrews PT (2003) Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterol 5:221–234
Balcombe JP (1990) Vocal recognition of pups by mother Mexican free-tailed bats Tadarida brasiliensis mexicana. Anim Behav 39:960–966
Balcombe JP, McCracken GF (1992) Vocal recognition in Mexican free-tailed bats do pups recognize mothers? Anim Behav 43:79–88
Barclay RMR (1982) Interindividual use of echolocation calls: eavesdropping by bats. Behav Ecol Sociobiol 10:271–275
Barlow KE, Jones G (1997) Function of pipistrelle social calls: field data and a playback experiment. Anim Behav 53:991–999
Behr O, Helversen Ov (2004) Bat serenades—complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol 56:106–115
Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B Biol Sci 265:227–233
Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732
Broughton WP (1963) Glossary. In: Burnel RG (ed) Acoustic behavior of animals. Elsevier, Boston, 883 pp
Brown P (1976) Vocal communication in the Pallid Bat, Antrozous pallidus. Z Tierpsychol 41:34–54
Davidson SM, Wilkinson GS (2002) Geographic and individual variation in vocalizations by male Saccopteryx bilineata (Chiroptera: Emballonuridae). J Mamm 83:526–535
Davison ML (1983) Multidimensional scaling. Wiley, New York
Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Ann Rev Neurosci 22:567–631
Fenton MB (1977) Variations in the social calls of little brown bats (Myotis lucifugus). Can J Zool 55:1151–1157
Fenton MB (1985) Communication in the Chiroptera. Indiana University Press, Bloomington
Fenton MB (1994) Assessing signal variability and reliability: ‘To thine ownself be true’. Anim Behav 47:757–764
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
Heller KG, Helversen OV (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80:178–186
Helversen OV, Helversen DV (1994) The advertisement call of the lesser noctule bat (Nyctalus leisleri). Folia Zool 43:331–338
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
Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386
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
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
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
Kingston T, Rossiter SJ (2004) Harmonic-hopping in Wallacea’s bats. Nature 429:654–657
Kolb A (1977) Wie erkennen sich Mutter und Junges des Mausohrs, Myotis myotis, bei der Rückkehr vom Jagdflug wieder? Z Tierpsychol 44:423–431
Kroodsma DE (1977) A re-evaluation of song development in the song sparrow. Anim Behav 25:390–399
Lundberg K, Gerell R (1986) Territorial advertisement and mate attraction in the bat, Pipistrellus pipistrellus. Ethology 71:115–124
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
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
Matsumura S (1979) Mother–infant communication in a horseshoe bat (Rhinolophus ferrumequinum nippon): development of vocalization. J Mamm 60:76–84
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
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
Moss CF, Sinha SR (2003) Neurobiology of echolocation in bats. Curr Opin Neurobiol 13:751–758
Neuweiler G (2003) Evolutionary aspects of bat echolocation. J Comp Physiol A 189:245–256
Neuweiler G, Schmidt S (1993) Audition in echolocating bats. Curr Opin Neurobiol 3:563–569
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
Obrist M (1995) Flexible bat echolocation: the influence of individual, habitat, and conspecifics on sonar signal design. Behav Ecol Sociobiol 36:207–219
Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. J Zool Lond 261:21–33
Pye JD (1972) Bimodal distribution of constant frequencies in some Hipposiderid bats (Mammalia: Hipposideridae). J Zool Lond 166:323–335
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
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
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
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
Schnitzler H-U, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569
Smotherman MS, Zhang S, Metzner W (2003) A neural basis for auditory feedback control of vocal pitch. J Neurosci 23:1464–1477
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
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
Wilkinson GS, Wenrick-Boughman J (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350
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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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