The high-output singing displays of a lekking bat encode information on body size and individual identity

Abstract

A growing body of research suggests that songs are an important part of the courtship behavior of many bat species, however there is little information on the basic characteristics of these vocalizations, or how they may function as a courtship signal. Lekking male lesser short-tailed bats (Mystacina tuberculata) appear to use vocal displays as a primary method for attracting mates, but it is unclear if these vocalizations constitute songs, and what characteristics females may use for mate selection. We recorded 16 lekking males and described the frequency and temporal properties of their vocalizations. We identified four notes (upsweeps, downsweeps, trills, and tones) that comprise courtship vocalizations, and males produced these notes either singly, or combined them linearly to form composite syllables. We classified 51 distinct syllable types (with an average of 29 types per male), with four (trills, upsweep-trills, trill-downsweeps, and upsweep-trill-downsweeps) comprising 69% of all syllables produced. The duration of trill-downsweeps scaled negatively with forearm length (a proxy for body size in bats), and all four main syllable types showed evidence of individuality. Based on the behavioral characteristics and contexts of these courtship vocalizations, we posit that this behavior constitutes singing. Furthermore, M. tuberculata potentially has one of the highest sustained song outputs yet described. Our results suggest the singing displays of M. tuberculata are signals that provide useful, honest cues of male characteristics and identity to females, and are as complex as the songs of many passerines.

Significance statement

Male courtship displays are predicted to honestly advertise aspects of male traits. Like many birds, some bat species produce songs to attract mates, but the characteristics of these songs are not well understood within the context of sexual selection. We demonstrate that the courtship vocalizations of Mystacina tuberculata – a species that likely relies on singing as its primary method of mate attraction – are a complex set of signals. Males have large syllable repertoires, encode four of their most-common syllables with individual signatures, and have one of the highest recorded song outputs for either birds or bats. Moreover, the length of one of the most commonly used syllable types is inversely related to male size, providing females the opportunity to appraise male size by auditory cues alone. Our work is part of a growing body of research demonstrating singing behavior in bats.

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References

  1. Bee MA, Kozich CE, Blackwell KJ, Gerhardt HC (2001) Individual variation in advertisement calls of territorial male green frogs, Rana clamitans: implications for individual discrimination. Ethology 107:65–84

    Article  Google Scholar 

  2. Beecher MD (1989) Signalling systems for individual recognition: an information theory approach. Anim Behav 38:248–261

    Article  Google Scholar 

  3. Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20:143–149

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  5. Behr O, von Helversen O, Heckel G, Nagy M, Voigt CC, Mayer F (2006) Territorial songs indicate male quality in the sac-winged bat Saccopteryx bilineata (Chiroptera, Emballonuridae). Behav Ecol 17:810–817

    Article  Google Scholar 

  6. Bohn KM, Schmidt-French B, Schwartz C, Smotherman M, Pollak GD (2009) Versatility and stereotypy of free-tailed bat songs. PLoS One 4:e6746

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Bohn K, Montiel-Reyes F, Salazar I (2016) The complex songs of two Molossid species. In: Ortega J (ed) Sociality in Bats. Springer, Switzerland, pp 143–160

    Google Scholar 

  8. Bradbury JW (1977) Lek mating behavior in the hammer-headed bat. Z Tierpsychol 45:225–255

    Article  Google Scholar 

  9. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates Inc., Sunderland, MA

    Google Scholar 

  10. Byers BE (2006) Extrapair paternity in chestnut-sided warblers is correlated with consistent vocal performance. Behav Ecol 18:130–136

    Article  Google Scholar 

  11. Carter GG, Riskin DK (2006) Mystacina tuberculata. Mamm Species 790:1–8

    Article  Google Scholar 

  12. Catchpole CK, Slater PJB (2003) Bird song: biological themes and variations. Cambridge University Press, Cambridge, UK

    Google Scholar 

  13. Charlton BD, Reby D (2016) The evolution of acoustic size exaggeration in terrestrial mammals. Nat Commun 7:12739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Charlton BD, Reby D, McComb K (2007) Female red deer prefer the roars of larger males. Biol Lett 3:382–385

    Article  PubMed  PubMed Central  Google Scholar 

  15. Charlton BD, Ellis WAH, Brumm J, Nilsson K, Fitch WT (2012) Female koalas prefer bellows in which lower formants indicate larger males. Anim Behav 84:1565–1571

    Article  Google Scholar 

  16. Christie PJ, Mennill DJ, Ratcliffe LM (2004) Pitch shifts and song structure indicate male quality in the dawn chorus of black-capped chickadees. Behav Ecol Sociobiol 55:341–348

    Article  Google Scholar 

  17. Collins S (2004) Vocal fighting and flirting: the functions of birdsong. In: Marler P, Slabbekoorn H (eds) Nature's music: the science of birdsong. Academic Press, New York, pp 39–79

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  19. Davidson SM, Wilkinson GS (2004) Function of male song in the greater white-lined bat, Saccopteryx bilineata. Anim Behav 67:883–891

    Article  Google Scholar 

  20. Eckenweber M, Knörnschild M (2013) Social influences on territorial signaling in male greater sac-winged bats. Behav Ecol Sociobiol 67:639–648

    Article  Google Scholar 

  21. Ellis JMS (2008) Decay of apparent individual distinctiveness in the begging calls of adult female white-throated magpie-jays. Condor 110:648–657

    Article  Google Scholar 

  22. ESRI (2012) ArcMap 10. Environmental Systems Research Institute, Redlands, CA

    Google Scholar 

  23. Ey E, Pfefferle D, Fischer J (2007) Do age-and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48:253–267

    Article  PubMed  CAS  Google Scholar 

  24. Fenton MB (2013) Questions, ideas and tools: lessons from bat echolocation. Anim Behav 85:869–879

    Article  Google Scholar 

  25. Galeotti P, Sacchi R, Rosa DP, Fasola M (2005) Female preference for fast-rate, high-pitched calls in Hermann's tortoises Testudo hermanni. Behav Ecol 16:301–308

    Article  Google Scholar 

  26. Gil D, Gahr M (2002) The honesty of bird song: multiple constraints for multiple traits. Trends Ecol Evol 17:133–141

    Article  Google Scholar 

  27. Godard R (1991) Long-term memory of individual neighbours in a migratory songbird. Nature 350:228–229

    Article  Google Scholar 

  28. Gray DA (1997) Female house crickets, Acheta domesticus, prefer the chirps of large males. Anim Behav 54:1553–1562

    Article  PubMed  CAS  Google Scholar 

  29. Höglund J, Alatalo RV (1995) Leks. Princeton University Press, Princeton

    Book  Google Scholar 

  30. Jahelková H, Horáček I, Bartonička T (2008) The advertisement song of Pipistrellus nathusii (Chiroptera, Vespertilionidae): a complex message containing acoustic signatures of individuals. Acta Chiropterol 10:103–126

    Article  Google Scholar 

  31. Jones G (1997) Differences in songflight calls and social calls between two phonic types of the vespertilionid bat Pipistrellus pipistrellus. J Zool 241:315–324

    Article  Google Scholar 

  32. Jones G, Siemers BM (2011) The communicative potential of bat echolocation pulses. J Comp Physiol 197:447–457

    Article  Google Scholar 

  33. Knörnschild M, Behr O, von Helversen O (2006) Babbling behavior in the sac-winged bat (Saccopteryx bilineata). Naturwissenschaften 93:451–454

    Article  PubMed  CAS  Google Scholar 

  34. Knörnschild M, Nagy M, Metz M, Mayer F, von Helversen O (2010) Complex vocal imitation during ontogeny in a bat. Biol Lett 6:156–159

    Article  PubMed  Google Scholar 

  35. Kroodsma D (2005) The singing life of birds: the art and science of listening to birdsong. Houghton Mifflin Harcourt, New York

    Google Scholar 

  36. Lardner B, bin Lakim M (2002) Animal communication: Tree-hole frogs exploit resonance effects. Nature 420:475–475

    Article  PubMed  CAS  Google Scholar 

  37. Linhart P, Fuchs R (2015) Song pitch indicates body size and correlates with males' response to playback in a songbird. Anim Behav 103:91–98

    Article  Google Scholar 

  38. Lloyd BD (2001) Advances in New Zealand mammalogy 1990–2000: short-tailed bats. J Roy Soc New Zeal 31:59–81

    Article  Google Scholar 

  39. Marler P (2004) Science and birdsong: the good old days. In: Marler P, Slabbekoorn H (eds) Nature's Music: the science of birdsong. Academic Press, New York, pp 1–38

    Google Scholar 

  40. Marler P, Slabbekoorn H (2004) Nature's music: the science of birdsong. Elsevier Academic Press, San Diego, California

    Google Scholar 

  41. McGregor PK, Krebs JR (1982) Mating and song sharing in the great tit. Nature 297:60–61

    Article  Google Scholar 

  42. Mennill DJ, Otter KA (2007) Status signaling and communication networks in chickadees: complex communication with a simple song. In: Otter KA (ed) Ecology and behavior of chickadees and titmice: an integrated approach. Oxford University Press, Oxford, pp 215–234

    Chapter  Google Scholar 

  43. Molles LE, Vehrencamp SL (1999) Repertoire size, repertoire overlap, and singing modes in the banded wren (Thryothorus pleurostictus). Auk 116:677–689

    Article  Google Scholar 

  44. Morton ES, Young K (1986) A previously undescribed method of song matching in a species with a single song “type”, the Kentucky warbler (Oporornis formosus). Ethology 73:334–342

    Article  Google Scholar 

  45. Mundry R, Sommer C (2007) Discriminant function analysis with nonindependent data: consequences and an alternative. Anim Behav 74:965–976

    Article  Google Scholar 

  46. Nordby JC, Campbell SE, Beecher MD (1999) Ecological correlates of song learning in song sparrows. Behav Ecol 10:287–297

    Article  Google Scholar 

  47. Nordby JC, Campbell SE, Burt JM, Beecher MD (2000) Social influences during song development in the song sparrow: a laboratory experiment simulating field conditions. Anim Behav 59:1187–1197

    Article  PubMed  CAS  Google Scholar 

  48. Patel R, Mulder RA, Cardoso GC (2010) What makes vocalisation frequency an unreliable signal of body size in birds? A study on black swans. Ethology 116:554–563

    Article  Google Scholar 

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

    Article  Google Scholar 

  50. Podos J, Huber SK, Taft B (2004) Bird song: the interface of evolution and mechanism. Annu Rev Ecol Evol S 35:55–87

    Article  Google Scholar 

  51. Poesel A, Kunc HP, Foerster K, Johnsen A, Kempenaers B (2006) Early birds are sexy: male age, dawn song and extrapair paternity in blue tits, Cyanistes (formerly Parus) caeruleus. Anim Behav 72:531–538

    Article  Google Scholar 

  52. Pollak GD, Casseday J (2012) The neural basis of echolocation in bats. Springer, Berlin

    Google Scholar 

  53. Puechmaille SJ, Borissov IM, Zsebok S, Allegrini B, Hizem M, Kuenzel S, Schuchmann M, Teeling EC, Siemers BM (2014) Female mate choice can drive the evolution of high frequency echolocation in bats: a case study with Rhinolophus mehelyi. PLoS One 9:e103452

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  55. Revelle W (2018) Psych: Procedures for Personality and Psychological Research, Northwestern University, Evanston, Illinois. https://www.CRAN.R-project.org/package=psychVersion=1.8.3

  56. Rice WR, Gaines SD (1994) ‘Heads I win, tails you lose’: testing directional alternative hypotheses in ecological and evolutionary research. TREE 9:236–237

    Google Scholar 

  57. Rivera-Gutierrez HF, Pinxten R, Eens M (2010) Multiple signals for multiple messages: great tit, Parus major, song signals age and survival. Anim Behav 80:451–459

    Article  Google Scholar 

  58. Russ JM, Racey PA (2007) Species-specificity and individual variation in the song of male Nathusius’ pipistrelles (Pipistrellus nathusii). Behav Ecol Sociobiol 61:669–677

    Article  Google Scholar 

  59. Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209:523–525

    Article  PubMed  CAS  Google Scholar 

  60. Sachteleben J, von Helversen O (2006) Songflight behaviour and mating system of the pipistrelle bat (Pipistrellus pipistrellus) in an urban habitat. Acta Chiropterol 8:391–401

    Article  Google Scholar 

  61. SAS Institute Inc. (2016) JMP Pro 13. Cary, NC: SAS Institute Inc.

  62. Schmidt S (2013) Beyond echolocation: emotional acoustic communication in bats. In: Altenmuller E, Schmidt S, Zimmermann E (eds) Evolution of emotional communication: from sounds in nonhuman mammals to speech and music in man. Oxford University Press, Oxford, pp 92–104

    Chapter  Google Scholar 

  63. Sell A, Bryant GA, Cosmides L, Tooby J, Sznycer D, von Rueden C, Krauss A, Gurven M (2010) Adaptations in humans for assessing physical strength from the voice. Proc R Soc Lond B 277:3509–3518

    Article  Google Scholar 

  64. Sibly RM, Nott HMR, Fletcher DJ (1990) Splitting behaviour into bouts. Anim Behav 39:63–69

    Article  Google Scholar 

  65. Smarsh GC, Smotherman M (2015) Singing away from home: Songs are used on foraging territories in the African megadermatid bat, Cardioderma cor. In: Proceeding of Meetings on Acoustics 25:010002. Acoustical Society of America, Jacksonville

  66. Smarsh GC, Smotherman M (2017) Behavioral response to conspecific songs on foraging territories of the heart-nosed bat. Behav Ecol Sociobiol 71:142

    Article  Google Scholar 

  67. Smotherman MS (2007) Sensory feedback control of mammalian vocalizations. Behav Brain Res 182:315–326

    Article  PubMed  PubMed Central  Google Scholar 

  68. Smotherman M, Knörnschild M, Smarsh G, Bohn K (2016) The origins and diversity of bat songs. J Comp Physiol A 202:535–554

    Article  Google Scholar 

  69. Sokal RR, Rohlf FJ (1995) Biometry: The principles and practice of statistics in biological research. W.H. Freeman and Co., New York

    Google Scholar 

  70. Spector DA (1992) Wood-warbler song systems. Curr Ornithol 9:199–238

    Article  Google Scholar 

  71. Toth CA, Parsons S (2013) Is lek breeding rare in bats? J Zool 291:3–11

    Article  Google Scholar 

  72. Toth CA, Cummings G, Dennis TE, Parsons S (2015a) Adoption of alternative habitats by a threatened, "obligate" deep-forest bat in a fragmented landscape. J Mammal 96:927–937

    Article  Google Scholar 

  73. Toth CA, Dennis TE, Pattemore DE, Parsons S (2015b) Females as mobile resources: communal roosts promote the adoption of lek breeding in a temperate bat. Behav Ecol 26:1156–1163

    Article  Google Scholar 

  74. Toth CA, Santure AW, Holwell GI, Pattemore DE, Parsons S (2018) Courtship behaviour and display-site sharing appears conditional on body size in a lekking bat. Anim Behav 136:13–19

    Article  Google Scholar 

  75. Vehrencamp SL (2000) Handicap, index, and conventional signal elements of bird song. In: Espmark Y, Amundsen T, Rosenqvist GO (eds) Animal signals. Tapir Academic Press, Trondheim, Norway, pp 277–300

    Google Scholar 

  76. Vignal C, Mathevon N, Mottin S (2004) Audience drives male songbird response to partner's voice. Nature 430:448–451

    Article  PubMed  CAS  Google Scholar 

  77. Vignal C, Mathevon N, Mottin S (2008) Mate recognition by female zebra finch: analysis of individuality in male call and first investigations on female decoding process. Behav Process 77:191–198

    Article  Google Scholar 

  78. Voigt CC, Behr O, Caspers B, von Helversen O, Knörnschild M, Mayer F, Nagy M (2008) Songs, scents, and senses: sexual selection in the greater sac-winged bat, Saccopteryx bilineata. J Mammal 89:1401–1410

    Article  Google Scholar 

  79. Wells KD (2010) The ecology and behavior of amphibians. University of Chicago Press, Chicago

    Google Scholar 

  80. Wildenthal JL (1965) Structure in primary song of the mockingbird (Mimus polyglottos). Auk 82:161–189

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to the New Zealand Department of Conservation – particularly T. Thurley and D. Smith – for assistance and support. We thank R. Germain for statistical advice, and three anonymous reviewers for their comments on previous versions of this manuscript.

Funding

Funding was provided by the Australasian Society for the Study of Animal Behaviour, the Australasian Bat Society, Bat Conservation International, and the University of Auckland.

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Correspondence to Cory A. Toth.

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The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The capture and marking of individuals was approved by both the University of Auckland Animal Ethics Committee (permit AEC#000920) and the New Zealand Department of Conservation (High Impact Research and Collection Permit WK-32184-RES).

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Communicated by M. Knoernschild

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Toth, C.A., Parsons, S. The high-output singing displays of a lekking bat encode information on body size and individual identity. Behav Ecol Sociobiol 72, 102 (2018). https://doi.org/10.1007/s00265-018-2496-4

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Keywords

  • Allometry
  • Chiroptera
  • Courtship
  • Lek breeding
  • Sexual selection
  • Song