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Learn it now, sing it later? Field and laboratory studies on song repertoire acquisition and song use in nightingales

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Abstract

In many bird species, song changes with age. The mechanisms that account for such changes are only partially understood. Common nightingales Luscinia megarhynchos change the size and composition of their repertoire between their first and second breeding season. To inquire into mechanisms involved in such changes, we compared the singing of 1-year-old and older free-living nightingales. Older males have more song types in common than have 1-year olds. Certain song types frequently sung by older birds did not (or only rarely) occur in the repertoire of yearlings (‘mature’ song types). We conducted learning experiments with hand-reared nightingales to address reasons for the lack of mature song types. The acquisition success of mature songs was as good as that of control songs (commonly sung by both age groups). However, the analysis of song type use revealed that all yearlings sang common song types more often than mature types. This indicates that the absence of certain song types in the repertoires of free-living yearlings cannot be accounted for by learning and/or motor constraints during song learning. Moreover, our results suggest that in communication networks, animals may restrict the actual use of their signal repertoire to a certain subset depending on the context.

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References

  • Arriaga G, Jarvis ED (2013) Mouse vocal communication system: are ultrasounds learned or innate? Brain Lang 124:96–116

    Article  PubMed  Google Scholar 

  • Arriaga G, Zhou EP, Jarvis ED (2012) Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One 7(10):e46610. doi:10.1371/journal.pone.0046610

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Baker MC, Cunningham MA (1985) The biology of bird-song dialects. Behav Brain Sci 8:85–100. doi:10.1017/S0140525X00019750

    Article  Google Scholar 

  • Ballentine B (2009) The ability to perform physically challenging songs predicts age and size in male swamp sparrows, Melospiza georgiana. Anim Behav 77:973–978

    Article  Google Scholar 

  • Baptista LF, Schuchmann KL (1990) Song learning in the Anna hummingbird. Ethology 84:15–26

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Berg KS, Delgado S, Cortopassi KA, Beissinger SR, Bradbury JW (2012) Vertical transmission of learned signatures in a wild parrot. P Roy Soc B-Biol Sci 279:585–59

    Article  Google Scholar 

  • Bernard DJ, Eens M, Ball GF (1996) Age- and behavior-related variation in volumes of song control nuclei in male European starlings. J Neurobiol 30:329–339

    Article  PubMed  CAS  Google Scholar 

  • Bolhuis JJ, Okanoya K, Scharff C (2010) Twitter evolution: converging mechanisms in birdsong and human speech. Nat Rev Neurosci 11:747–759

    Article  PubMed  CAS  Google Scholar 

  • Botero CA, Rossman RJ, Caro LM, Stenzler LM, Lovette IJ, de Kort SR, Vehrencamp SL (2009) Syllable type consistency is related to age, social status and reproductive success in the tropical mockingbird. Anim Behav 77:701–706

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Brainard MS, Doupe AJ (2013) Translating birdsong: songbirds as a model for basic and applied medical research. Annu Rev Neurosci 36:489–517

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Brumm H (2004) The impact of environmental noise on song amplitude in a territorial bird. J Anim Ecol 73:434–440

    Article  Google Scholar 

  • Chaiken M, Bohner J, Marler P (1994) Repertoire turnover and the timing of song acquisition in European starlings. Behaviour 128:25–39

    Article  Google Scholar 

  • Cucco M, Malacarne G (2000) Delayed maturation in passerine birds: an examination of plumage effects and some indications of a related effect in song. Ethol Ecol Evol 12:291–308

    Article  Google Scholar 

  • De Kort SR, Eldermire ERB, Valderrama S, Botero CA, Vehrencamp SL (2009) Trill consistency is an age-related assessment signal in banded wrens. P Roy Soc B-Biol Sci 276:2315–2321

    Article  Google Scholar 

  • Eriksen A, Lampe HM, Slagsvold T (2009) Interspecific cross-fostering affects song acquisition but not mate choice in pied flycatchers, Ficedula hypoleuca. Anim Behav 78:857–863

    Article  Google Scholar 

  • Eriksen A, Slagsvold T, Lampe HM (2011) Vocal plasticity—are pied flycatchers, Ficedula hypoleuca, open-ended learners? Ethology 117:188–189

    Article  Google Scholar 

  • Faraway JJ (2006) Extending linear models with R: generalized linear, mixed effects and nonparametric regression models. Chapman & Hall, London, Boca Raton

    Google Scholar 

  • Geberzahn N, Hultsch H (2003) Long-time storage of song types in birds: evidence from interactive playbacks. P Roy Soc B-Biol Sci 270:1085–1090

    Article  Google Scholar 

  • Glutz von Blotzheim UN, Bauer KM. (1988) Handbuch der Vögel Mitteleuropas, Bd. 11. Aula, Wiesbaden

  • Hammerschmidt K, Reisinger E, Westekemper K, Ehrenreich L, Strenzke N, Fischer J (2012) Mice do not require auditory input for the normal development of their ultrasonic vocalizations. BMC Neurosci 13:40. doi:10.1186/1471-2202-13-40

    Article  PubMed  PubMed Central  Google Scholar 

  • Hultsch H, Kopp ML (1989) Early auditory learning and song improvisation in nightingales. Anim Behav 37:510–512

    Article  Google Scholar 

  • Hultsch H, Todt D (1981) Repertoire sharing and song-post distance in nightingales (Luscinia megarhynchos B.). Behav Ecol Sociobiol 8:183–188

    Article  Google Scholar 

  • Hultsch H, Todt D (1989) Memorization and reproduction of songs in nightingales (Luscinia megarhynchos): evidence for package formation. J Comp Physiol A 165:197–203

    Article  Google Scholar 

  • Hultsch H, Todt D (2008) Comparative aspects of song learning. In: Zeigler HP, Marler P (eds) Neuroscience of birdsong. Cambridge University Press, Cambridge, pp 204–216

    Google Scholar 

  • Janik VM, Slater PJB (1997) Vocal learning in mammals. Adv Study Behav 26:59–99

    Article  Google Scholar 

  • Jarvis ED, Ribeiro S, Vielliard J, da Silva ML, Ventura D, Mello CV (2000) Behaviorally-driven gene expression reveals hummingbird brain song nuclei. Nature 406:628–632

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kiefer S, Spiess A, Kipper S, Mundry R, Sommer C, Hultsch H, Todt D (2006) First year common nightingales (Luscinia megarhynchos) have smaller repertoire sizes than older males. Ethology 112:1217–1224

    Article  Google Scholar 

  • Kiefer S, Sommer C, Scharff C, Kipper S, Mundry R (2009) Tuning towards tomorrow? Common nightingales Luscinia megarhynchos change and increase their song repertoires from the first to the second breeding season. J Avian Biol 40:231–236

    Article  Google Scholar 

  • Kiefer S, Sommer C, Scharff C, Kipper S (2010) Singing the popular songs? Nightingales share more song types with their breeding population in their second season than in their first. Ethology 116:619–626

    Google Scholar 

  • Kiefer S, Scharff C, Kipper S (2011) Does age matter in song bird vocal interactions? Results from interactive playback experiments. Front Zool 8:1–8

    Article  Google Scholar 

  • Kipper S, Kiefer S (2010) Age-related changes in bird’s singing styles: on fresh tunes and fading voices? Adv Study Behav 41:77–118

    Article  Google Scholar 

  • Kipper S, Mundry R, Hultsch H, Todt D (2004) Long-term persistence of song performance rules in nightingales (Luscinia megarhynchos): a longitudinal field study on repertoire size and composition. Behaviour 141:371–390

    Article  Google Scholar 

  • Kipper S, Mundry R, Sommer C, Hultsch H, Todt D (2006) Song repertoire size is correlated with body measures and arrival date in common nightingales, Luscinia megarhynchos. Anim Behav 71:211–217

    Article  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Knörnschild M, Nagy M, Metz M, Mayer F, von Helversen O (2012) Learned vocal group signatures in the polygynous bat Saccopteryx bilineata. Anim Behav 84:761–769

    Article  Google Scholar 

  • Logue DM, Forstmeier W (2008) Constrained performance in a communication network: implications for the function of song type matching and for the evolution of multiple ornaments. Am Nat 172:34–41

    Article  PubMed  Google Scholar 

  • MacDougall-Shackleton SA, Ball GF, Edmonds E, Sul R, Hahn TP (2005) Age- and sex-related variation in song-control regions in Cassin’s finches, Carpodacus cassinii. Brain Behav Evol 65:262–267

    Article  PubMed  Google Scholar 

  • Mundry R, Sommer C (2007) Ein neues Gefiedermerkmal zur Altersbestimmung bei Nachtigallen (Luscinia megarhynchos), a new pattern of feather colouration for age determination in common nightingales. Limicola 21:131–139

    Google Scholar 

  • Nemeth E, Kempenaers B, Matessi G, Brumm H (2012) Rock sparrow song reflects age and reproductive success. PLoS One 7:e43259. doi:10.1371/journal.pone.0043259

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nottebohm F, Nottebohm ME, Crane L (1986) Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav Neural Biol 46:445–471

    Article  PubMed  CAS  Google Scholar 

  • O’ Loghlen AL, Rothstein SI (2012) Delayed vocal ontogeny in songbirds: a laboratory study validates a model for delayed development derived from field studies. J Ethol 30:369–378

    Article  Google Scholar 

  • Osiejuk TS, Losak K, Dale S (2007) Cautious response of inexperienced birds to conventional signal of stronger threat. J Avian Biol 38:644–649

    Article  Google Scholar 

  • Pepperberg M (1999) The Alex Studies. Harvard University Press, Cambridge, Mass

    Google Scholar 

  • Podos D, Lahti C, Moseley DL (2009) Vocal performance and sensorimotor learning in songbirds. Adv Study Behav 40:159–195

    Article  Google Scholar 

  • Poesel A, Nelson DA (2012) Delayed song maturation and territorial aggression in a song bird. Biol Lett 8:369–371

    Article  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Ralls K, Fiorelli P, Gish S (1985) Vocalizations and vocal mimicry in captive harbor seals, Phoca vitulina. Canad Zool 63:1050–1056

    Article  Google Scholar 

  • Rohwer S (1978) Passerine subadult plumages and the deceptive acquisition of resources: test of a critical assumption. Condor 80:173–179

    Article  Google Scholar 

  • Sanvito S, Galimberti F, Miller EH (2007) Observational evidences of vocal learning in southern elephant seals: a longitudinal study. Ethology 113:137–146

    Article  Google Scholar 

  • Scharff C, Adam I (2013) Neurogenetics of birdsong. Curr Opin Neurobiol 23:29–36

    Article  PubMed  CAS  Google Scholar 

  • Scharff C, Petri J (2011) Evo-devo, deep homology and FoxP2: implications for the evolution of speech and language. P Roy Soc B-Biol Sci 366:2124–2140

    Google Scholar 

  • Searcy WA, Yasukawa K (1996) Song and female choice. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithacla & London, pp 454–473

    Google Scholar 

  • Sprau P, Roth T, Amrhein V, Naguib M (2013) The predictive value of trill performance in a large repertoire songbird, the nightingale Luscinia megarhynchos. J Avian Biol 44:001–008

    Article  Google Scholar 

  • Svensson L (1992) Identification guide to European Passerines. British Trust for Ornithology, Thetford

    Google Scholar 

  • Tchernichovski O, Nottebohm F, Ho CE, Bijan P, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167–1176

    Article  PubMed  Google Scholar 

  • Todt D (1975) Social learning of vocal patterns and modes of their application in Grey Parrots (Psittacus erithacus). Z Tierpsych 39:178–188

    Article  Google Scholar 

  • Todt D, Geberzahn N (2003) Age-dependent effects of song exposure: song crystallization sets a boundary between fast and delayed vocal imitation. Anim Behav 65:971–979

    Article  Google Scholar 

  • Todt D, Hultsch H, Heike D (1979) Conditions affecting song acquisition in nightingales (Luscinia megarhynchos L.). Z Tierpsych 51:23–35

    Google Scholar 

  • Weiss M, Kiefer S, Kipper S (2012) Buzzwords in females’ ears? The use of buzz songs in the communication of nightingales (Luscinia megarhynchos). PLoS One 7:e45057

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Weiss M, Hultsch H, Adam I, Scharff C, Kipper S (2014) The use of network analysis to study complex animal communication systems: a study on nightingale song. P Roy Soc B-Biol Sci 281:20140460

    Article  Google Scholar 

  • Wilbrecht L, Williams H, Gangadhar N, Nottebohm F (2006) High levels of new neuron addition persist when the sensitive period for song learning is experimentally prolonged. J Neurosci 26:9135–9141

    Article  PubMed  CAS  Google Scholar 

  • Wistel-Wozniak A, Hultsch H (1993) Konstante und altersabhängig veränderte Gesangsmerkmale bei handaufgezogenen Nachtigallen. Verh Dtsch Zool Ges 86:281

    Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgments

The study was conducted with permission of the Senatsverwaltung für Stadtentwicklung und Umweltschutz, Berlin. Keeping of nightingales was permitted by the Landesamt für Gesundheit und Soziales, Berlin. The study would not have been possible without the invaluable contribution of Christina Sommer and Roger Mundry, who determined age and banded the birds. We would also like to thank Jan Engler, Kim Geraldine Mortega, Philipp Sprau, Christoph Teufel, Tina Teutscher and Michael Weiss for their assistance in bird netting and/or obtaining recordings, and Monica Carlson, Kim Geraldine Mortega, Heike Posern and Joana Schulz for their help in hand-rearing and tutoring the birds. We are thankful to Arpik Nshdejan for sexing the birds and Michael Weiss for statistical advice.

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Correspondence to S. Kiefer.

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Communicated by: Sven Thatje

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Kiefer, S., Scharff, C., Hultsch, H. et al. Learn it now, sing it later? Field and laboratory studies on song repertoire acquisition and song use in nightingales. Naturwissenschaften 101, 955–963 (2014). https://doi.org/10.1007/s00114-014-1236-5

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  • DOI: https://doi.org/10.1007/s00114-014-1236-5

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