Trade-offs in the production of animal vocal sequences: insights from the structure of wild chimpanzee pant hoots

BackgroundVocal sequences - utterances consisting of calls produced in close succession - are common phenomena in animal communication. While many studies have explored the adaptive benefits of producing such sequences, very little is known about how the costs and constraints involved in their production affect their form. Here, we investigated this issue in the chimpanzee (Pan troglodytes schweinfurthii) pant hoot, a long and structurally complex vocal sequence comprising four acoustically distinct phases – introduction, build-up, climax and let-down.ResultsWe found that in each of these phases, and for the sequence as a whole, there was a negative relationship between the number of calls produced and their average duration. There was also a negative relationship between the total duration of some adjacent phases. Significant relationships between the fundamental frequency of calls and their number or duration were found for some phases of the sequence, but the direction of these relationships differed between particular phases.ConclusionsThese results indicate that there are trade-offs in terms of signal duration at two levels in pant-hoot production: between call number and duration, and between the relative durations of successive phases. These trade-offs are likely to reflect biomechanical constraints on vocal sequence production. Phase-specific trade-offs also appear to occur between fundamental frequency and call number or duration, potentially reflecting that different phases of the sequence are associated with distinct types of information, linked in different ways to call pitch. Overall, this study highlights the important role of costs and constraints in shaping the temporal and acoustic structure of animal vocal sequences.

[1]  J. Mitani,et al.  Chorusing and Call Convergence in Chimpanzees: Tests of Three Hypotheses , 1998 .

[2]  Colin A. Chapman,et al.  Fission‐Fusion Dynamics , 2008, Current Anthropology.

[3]  R. Wiley,et al.  Physical constraints on acoustic communication in the atmosphere: Implications for the evolution of animal vocalizations , 1978, Behavioral Ecology and Sociobiology.

[4]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[5]  Franz Goller,et al.  Respiratory patterns and oxygen consumption in singing zebra finches , 2003, Journal of Experimental Biology.

[6]  A. K. Hill,et al.  Sexual Selection on Human Voices , 2014 .

[7]  Zarin P. Machanda,et al.  Pant hoot chorusing and social bonds in male chimpanzees , 2013, Animal Behaviour.

[8]  P. Marler,et al.  Individuality in a long-range vocalization of wild chimpanzees. , 2010, Zeitschrift fur Tierpsychologie.

[9]  D. Reby,et al.  Context-Related Variation in the Vocal Growling Behaviour of the Domestic Dog (Canis familiaris) , 2009 .

[10]  James M. Fattu,et al.  Subglottic pressure and the control of phonation by the echolocating bat,Eptesicus , 1981, Journal of comparative physiology.

[11]  W. F. Twaddell,et al.  Die Architektonik des deutschen Wortschatzes , 1954 .

[12]  Gertraud Fenk-Oczlon,et al.  Menzerath’s Law and the Constant Flow of Linguistic Information , 1993 .

[13]  P. Lieberman,et al.  Determination of the rate of change of fundamental frequency with respect to subglottal air pressure during sustained phonation. , 1969, The Journal of the Acoustical Society of America.

[14]  William J. Smith,et al.  The Behavior of Communicating: An Ethological Approach , 1980 .

[15]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[16]  Ramon Ferrer-i-Cancho,et al.  Acoustic sequences in non‐human animals: a tutorial review and prospectus , 2016, Biological reviews of the Cambridge Philosophical Society.

[17]  Douglas A. Nelson,et al.  Segregation of information in a complex acoustic signal: individual and dialect identity in white-crowned sparrow song , 2007, Animal Behaviour.

[18]  Katie E. Slocombe,et al.  Social and ecological correlates of long-distance pant hoot calls in male chimpanzees , 2014, Behavioral Ecology and Sociobiology.

[19]  Ramon Ferrer-i-Cancho,et al.  Gelada vocal sequences follow Menzerath’s linguistic law , 2016, Proceedings of the National Academy of Sciences.

[20]  D. Reby,et al.  Oestrous red deer hinds prefer male roars with higher fundamental frequencies , 2010, Proceedings of the Royal Society B: Biological Sciences.

[21]  Robin C. Dunkin,et al.  The metabolic cost of communicative sound production in bottlenose dolphins (Tursiops truncatus) , 2013, Journal of Experimental Biology.

[22]  Ingo R. Titze,et al.  A Cervid Vocal Fold Model Suggests Greater Glottal Efficiency in Calling at High Frequencies , 2010, PLoS Comput. Biol..

[23]  Julie Gros-Louis,et al.  Selection for acoustic individuality within the vocal repertoire of wild chimpanzees , 1996, International Journal of Primatology.

[24]  EFFECT OF ANDROGENS ON STRUCTURE AND RATE OF CROWING IN THE JAPANESE QUAIL(COTURNIX JAPONICA) , 2000 .

[25]  J. Mitani,et al.  Contexts and social correlates of long-distance calling by male chimpanzees , 1993, Animal Behaviour.

[26]  Antje Engelhardt,et al.  Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating , 2011, Animal Behaviour.

[27]  Tobias Riede,et al.  Nonlinear acoustics in pant hoots of common chimpanzees (Pan troglodytes): Frequency jumps, subharmonics, biphonation, and deterministic chaos , 2004, American journal of primatology.

[28]  F Goller,et al.  The metabolic cost of birdsong production. , 2001, The Journal of experimental biology.

[29]  Drew Rendall,et al.  Contextual variation in chimpanzee pant hoots and its implications for referential communication , 2005, Animal Behaviour.

[30]  K. Slocombe,et al.  The relationship between testosterone and long-distance calling in wild male chimpanzees , 2016, Behavioral Ecology and Sociobiology.

[31]  Tomasz S. Osiejuk,et al.  What makes a ‘local song’ in a population of ortolan buntings without a common dialect? , 2007, Animal Behaviour.

[32]  E. H. Haimoff Convergence in the duetting of monogamous Old World primates , 1986 .

[33]  I R Titze,et al.  On the relation between subglottal pressure and fundamental frequency in phonation. , 1989, The Journal of the Acoustical Society of America.

[34]  M. Ryan,et al.  The Adaptive Significance of a Complex Vocal Repertoire in a Neotropical Frog , 2010 .

[35]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[36]  P. Waser,et al.  Experimental Studies of Primate Vocalization: Specializations for Long-distance Propagation , 2010 .

[37]  D. Rendall,et al.  The meaning and function of grunt variants in baboons , 1999, Animal Behaviour.

[38]  Charles F. Hockett,et al.  A mathematical theory of communication , 1948, MOCO.

[39]  D. Barr,et al.  Random effects structure for confirmatory hypothesis testing: Keep it maximal. , 2013, Journal of memory and language.

[40]  Klaus Zuberbühler,et al.  Sequential information in a great ape utterance , 2016, Scientific Reports.

[41]  K. Hammerschmidt,et al.  Cues to Androgens and Quality in Male Gibbon Songs , 2013, PloS one.

[42]  David Lusseau,et al.  Compression as a Universal Principle of Animal Behavior , 2013, Cogn. Sci..

[43]  Philippe Schlenker,et al.  What Do Monkey Calls Mean? , 2016, Trends in Cognitive Sciences.

[44]  G. Isabirye-Basuta,et al.  The Chimpanzees of Budongo Forest: Ecology, Behaviour and Conservation , 2007 .

[45]  A. MØller,et al.  Song correlates with social context, testosterone and body condition in male barn swallows , 1997, Animal Behaviour.

[46]  Kate E. Jones,et al.  The Functions of Laryngeal Air Sacs in Primates: A New Hypothesis , 2002, Folia Primatologica.

[47]  S. Semple,et al.  Perception of female reproductive state from vocal cues in a mammal species , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  Kimberly A. Pollard,et al.  Evolving communicative complexity: insights from rodents and beyond , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[49]  P. Slater,et al.  Bird Song: Biological Themes and Variations , 1995 .

[50]  Klaus Zuberbühler,et al.  Chimpanzees modify recruitment screams as a function of audience composition , 2007, Proceedings of the National Academy of Sciences.

[51]  Katie E. Slocombe,et al.  The acoustic structure of chimpanzee pant-hooting facilitates chorusing , 2013, Behavioral Ecology and Sociobiology.

[52]  Klaus Zuberbühler,et al.  Chimpanzees communicate to two different audiences during aggressive interactions , 2015, Animal Behaviour.

[53]  Simon W. Townsend,et al.  Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System , 2015, PLoS biology.

[54]  A. Harcourt The Chimpanzees of Gombe. Patterns of Behavior, Jane Goodall. Belknap Press of Harvard University Press, Cambridge, Massachussets (1986), xii, +671. Price $30 , 1988 .

[55]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[56]  Steven M. Phelps,et al.  Androgens modulate song effort and aggression in Neotropical singing mice , 2011, Hormones and Behavior.

[57]  A. MacLarnon,et al.  The evolution of human speech: the role of enhanced breathing control. , 1999, American journal of physical anthropology.

[58]  D. Reby,et al.  The contribution of source–filter theory to mammal vocal communication research , 2010 .

[59]  R. Seyfarth,et al.  Baboon loud calls advertise male quality: acoustic features and their relation to rank, age, and exhaustion , 2004, Behavioral Ecology and Sociobiology.

[60]  H. Schielzeth,et al.  Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse , 2010, Behavioral Ecology and Sociobiology.

[61]  H. Geisser,et al.  Singing and mating success in water pipits: one specific song element makes all the difference , 1998, Animal Behaviour.

[62]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[63]  E. Geffen,et al.  Complex call in male rock hyrax (Procavia capensis): a multi-information distributing channel , 2009, Behavioral Ecology and Sociobiology.

[64]  Klaus Zuberbühler,et al.  Language evolution: Semantic combinations in primate calls , 2006, Nature.

[65]  Tobias Riede,et al.  Nonlinear acoustics in the pant hoots of common chimpanzees (Pan troglodytes): vocalizing at the edge. , 2007, The Journal of the Acoustical Society of America.

[66]  J. Mitani Sexual selection and adult male orangutan long calls , 1985, Animal Behaviour.