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Difference between the vocalizations of two sister species of pigeons explained in dynamical terms

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Abstract

Vocal communication is an unique example, where the nonlinear nature of the periphery can give rise to complex sounds even when driven by simple neural instructions. In this work we studied the case of two close-related bird species, Patagioenas maculosa and Patagioenas picazuro, whose vocalizations differ only in the timbre. The temporal modulation of the fundamental frequency is similar in both cases, differing only in the existence of sidebands around the fundamental frequency in the P. maculosa. We tested the hypothesis that the qualitative difference between these vocalizations lies in the nonlinear nature of the syrinx. In particular, we propose that the roughness of maculosa’s vocalizations is due to an asymmetry between the right and left vibratory membranes, whose nonlinear dynamics generate the sound. To test the hypothesis, we generated a biomechanical model for vocal production with an asymmetric parameter Q with which we can control the level of asymmetry between these membranes. Using this model we generated synthetic vocalizations with the principal acoustic features of both species. In addition, we confirmed the anatomical predictions by making post mortem inspection of the syrinxes, showing that the species with tonal song (picazuro) has a more symmetrical pair of membranes compared to maculosa.

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References

  • Amador A, Goller F, Mindlin GB (2008) Frequency modulation during song in a suboscine does not require vocal muscles. J Neurophysiol 99(5):2383–2389

    Article  PubMed  Google Scholar 

  • Baptista LP (1996) Nature and its nurturing in avian vocal development. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, pp 39–60

    Google Scholar 

  • Baptista LF, Trail PW (1992) The role of song in the evolution of passerine diversity. Syst Biol 41(2):242–247

    Article  Google Scholar 

  • Baptista LF, Trail PW, Horblit HM (1997) Family Columbidae (pigeons and doves). In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world, vol 4. Lynx Edicions, Barcelona, pp 60–243

  • Beckers GJL, ten Cate C (2006) Nonlinear phenomena and song evolution in Streptopelia doves. Acta Zool Sinica 52:482–485

    Google Scholar 

  • Beckers GJL, Suthers RA, ten Cate C (2003) Mechanisms of frequency and amplitude modulation in ringdove song. J Exp Biol 206(11):1833–1843

    Article  PubMed  Google Scholar 

  • Boersma P (2002) Praat, a system for doing phonetics by computer. Glot Int 5(9/10):341–345

    Google Scholar 

  • Chiel HJ, Beer RD (1997) The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci 20(12):553–557

    Article  CAS  PubMed  Google Scholar 

  • de Kort SR, ten Cate C (2001) Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Anim Behav 61(1):239–247

    Article  PubMed  Google Scholar 

  • de Kort SR, ten Cate C (2004) Repeated decrease in vocal repertoire size in Streptopelia doves. Anim Behav 67(3):549–557

    Article  Google Scholar 

  • de Kort SR, den Hartog PM, ten Cate C (2002) Diverge or merge? The effect of sympatric occurrence on the territorial vocalizations of the vinaceous dove Streptopelia vinacea and the ringnecked dove S. capicola. J Avian 33(2):150–158

    Article  Google Scholar 

  • den Hartog PM, Slabbekoorn H, ten Cate C (2008) Male territorial vocalizations and responses are decoupled in an avian hybrid zone. Philos Trans R Soc Lond B 363(1505):2879–2889

    Article  Google Scholar 

  • Edwards SV, Kingan SB, Calkins JD, Balakrishnan CN, Jennings WB, Swanson WJ, Sorenson MD (2005) Speciation in birds: genes, geography, and sexual selection. Proc Natl Acad Sci USA 102(1):6550–6557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elemans CP, Larsen ON, Hoffmann MR, van Leeuwen JL (2003) Quantitative modeling of the biomechanics of the avian syrinx. Anim Biol 53(2):183–193

    Article  Google Scholar 

  • Elemans CP, Zaccarelli R, Herzel H (2008) Biomechanics and control of vocalization in a non-songbird. J R Soc Interface 5(24):691–703

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibbs D, Barnes E, Cox J (2001) Pigeons and doves: a guide to the pigeons and doves of the world. Yale University Press, New Haven

    Google Scholar 

  • Goller F, Larsen ON (1997) In situ biomechanics of the syrinx and sound generation in pigeons. J Exp Biol 200(16):2165–2176

    CAS  PubMed  Google Scholar 

  • Goodwin D (1964) Some calls and displays of the Picazuro Pigeon. Condor 66(5):418–422

    Article  Google Scholar 

  • Goodwin D (1983) Pigeons and doves of the world. British Museum of Natural History, London

    Google Scholar 

  • Gray AP (1958) Bird hybrids. Commonwealth Agricultural Bureaux, Bucks

    Google Scholar 

  • Guckenheimer J, Holmes P (1983) Nonlinear oscillations, dynamical systems, and bifurcations of vector fields, vol 42. Springer Science & Business Media, New York

    Book  Google Scholar 

  • Ishizaka K, Flanagan JL (1972) Synthesis of voiced sounds from a two mass model of the vocal cords. Bell Syst Tech J 51(6):1233–1268

    Article  Google Scholar 

  • Johnson KP, Weckstein JD (2011) The Central American land bridge as an engine of diversification in New World doves. J Biogeogr 38(6):1069–1076

    Article  Google Scholar 

  • Lade BI, Thorpe WH (1964) Dove songs as innately coded patterns of specific behaviour. Nature 202:366–368

    Article  Google Scholar 

  • Lapiedra O, Sol D, Carranza S, Beaulieu JM (2013) Behavioural changes and the adaptive diversification of pigeons and doves. Proc R Soc Lond B Biol Sci 280(1755):20122893

    Article  Google Scholar 

  • Larsen ON, Goller F (1999) Role of syringeal vibrations in bird vocalizations. Proc R Soc Lond B Biol Sci 266(1429):1609–1615

    Article  Google Scholar 

  • López-Lanús B (2009) Bird sounds from southern South America. Audiornis Producciones, Buenos Aires

    Google Scholar 

  • Lucero JC, Koenig LL (2005) Phonation thresholds as a function of laryngeal size in a two-mass model of the vocal folds. J Acoust Soc Am 118(5):2798–2801

    Article  PubMed  Google Scholar 

  • Lucero JC, Schoentgen J, Haas J, Luizard P, Pelorson X (2015) Self-entrainment of the right and left vocal fold oscillators. J Acoust Soc 137(4):2036–2046

    Article  Google Scholar 

  • Mahler B, Tubaro PL (2001) Relationship between song characters and morphology in New World pigeons. Biol J Linn Soc 74(4):533–539

    Article  Google Scholar 

  • Mandiwana-Neudani TG, Kopuchian C, Louw G, Crowe TM (2011) A study of gross morphological and histological syringeal features of true francolins (Galliformes: Francolinus, Scleroptila, Peliperdix and Dendroperdix spp.) and spurfowls (Pternistis spp.) in a phylogenetic context. Ostrich 82(2):115–127

    Article  Google Scholar 

  • McCarthy EM (2006) Handbook of avian hybrids of the world. Oxford University Press, Oxford

    Google Scholar 

  • Milstein PLS, Wolff SW (1987) The oversimplification of our ‘francolins’. S Afr J Wildl Res 1:58–65

    Google Scholar 

  • Mindlin GB, Laje R (2005) The physics of birdsong. Springer, Berlin

    Google Scholar 

  • Nottebohm F (1970) Ontogeny of bird song. Science 167(3920):950–956

    Article  CAS  PubMed  Google Scholar 

  • Nottebohm F, Nottebohm ME (1971) Vocalizations and breeding behaviour of surgically deafened ringdoves (Streptopeliarisoria). Anim Behav 19(2):313–327

    Article  CAS  PubMed  Google Scholar 

  • Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1996) Numerical recipes in C, vol 2. Cambridge University Press, Cambridge

    Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675

    Article  CAS  PubMed  Google Scholar 

  • Sitt JD, Amador A, Goller F, Mindlin GB (2008) Dynamical origin of spectrally rich vocalizations in birdsong. Phys Rev E 78(1):011905

    Article  CAS  Google Scholar 

  • Slabbekoorn H, Smith TB (2002) Bird song, ecology and speciation. Philos T Roy Soc B 357(1420):493–503

    Article  Google Scholar 

  • Slabbekoorn H, ten Cate C (1998) Perceptual tuning to frequency characteristics of territorial signals in collared doves. Anim Behav 56(4):847–857

    Article  PubMed  Google Scholar 

  • Slabbekoorn H, de Kort S, ten Cate C (1999) Comparative analysis of perch-coo vocalizations in Streptopelia doves. Auk 116(3):737–748

    Article  Google Scholar 

  • Straneck R (1990a) Canto de las aves pampeanas II. Lola (Literature of Latin America), Buenos Aires

    Google Scholar 

  • Straneck R (1990b) Canto de las Aves de las Serranías Centrales. Lola (Literature of Latin America), Buenos Aires

    Google Scholar 

  • Suthers RA, Narins PM, Lin WY, Schnitzler HU, Denzinger A, Xu CH, Feng AS (2006) Voices of the dead: complex nonlinear vocal signals from the larynx of an ultrasonic frog. J Exp Biol 209(24):4984–4993

    Article  PubMed  Google Scholar 

  • Titze IR (1988) The physics of small-amplitude oscillation of the vocal folds. J Acoust Soc Am 83(4):1536–1552

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Administración de Parques Nacionales and Fauna Authorities from Entre Ríos Province (Argentina), for authorizing permits for this study; the staff and rangers from Quebrada del Condorito National Park (Argentina), Darío Lijtmaer, Natalia Trujillo Arias, Diego Masson and Luciano Calderón for assistance in field work; and Adrián Di Giacomo, Natalia García, Priscila Hanisch and Belén Bukowski for help in taking care of the animals in captivity. We also thank Mr. Ramón Moller Jensen and El Potrero SA (Argentina) for allowing the fieldwork with pigeon specimens in the Natural Reserve. We are especially thankful with Fabián Gabelli for his advice and assistance with fieldwork and animal management. Yolanda Davies helped with captures, animal care, preparation and conservation of the specimens in the Ornithology Collection of the National Museum of Natural Science.

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Authors and Affiliations

  1. Department of Physics, FCEN, University of Buenos Aires and IFIBA, CONICET, Buenos Aires, Argentina

    R. Gogui Alonso, Ana Amador, Maria de los Angeles Suarez & Gabriel B. Mindlin

  2. División Ornitología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (MACN - CONICET), Avenida Ángel Gallardo 470, C1405DJR, Buenos Aires, Argentina

    Cecilia Kopuchian & Pablo L. Tubaro

  3. Laboratorio de Biología de la Conservación, Centro de Ecología Aplicada del Litoral (CECOAL - CONICET), Ruta Provincial 5, Km 2.5, CEP 3400, Corrientes, Argentina

    Cecilia Kopuchian

Authors
  1. R. Gogui Alonso
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  2. Cecilia Kopuchian
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  3. Ana Amador
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  4. Maria de los Angeles Suarez
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  5. Pablo L. Tubaro
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  6. Gabriel B. Mindlin
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Corresponding author

Correspondence to R. Gogui Alonso.

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The authors declare no competing or financial interests.

Funding

This work describes research partially funded by National Council of Scientific and Technical Research (CONICET), National Agency of Science and Technology (ANPCyT), University of Buenos Aires (UBA) and National Institute of Health through R01-DC-012859 and R01-DC-006876.

Ethical standard

All experiments on animals described above were performed in accordance with applicable national legislation and institutional guidelines for the care and use of animals.

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Alonso, R.G., Kopuchian, C., Amador, A. et al. Difference between the vocalizations of two sister species of pigeons explained in dynamical terms. J Comp Physiol A 202, 361–370 (2016). https://doi.org/10.1007/s00359-016-1082-3

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  • DOI: https://doi.org/10.1007/s00359-016-1082-3

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