Acoustic structure and variation in mountain and western gorilla close calls: a syntactic approach

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


Our understanding of the functioning of a species’ vocal repertoire can be greatly improved by investigating acoustic variation and using objective classification schemes based on acoustic structure. Here we used a syntactic approach to investigate the acoustic structure of the gorilla close distance vocalizations (‘close calls’), which remain as yet little understood. We examined 2130 calls of 10 mountain gorillas (Gorilla beringei beringei) from Bwindi Impenetrable National Park, Uganda, and 5 western lowland gorillas (Gorilla gorilla gorilla) from Bai Hokou, Central African Republic. We segmented calls into units using distinct acoustic features and employed model-based cluster analyses to define the repertoire of unit types. We then examined how unit types were combined into calls. Lastly, we compared unit type use between age–sex classes and the two study groups. We found that the gorilla close calls consist of 5 intergraded acoustic unit types which were flexibly but yet non-randomly concatenated into 159 combinations. Our results are in line with previous quantitative acoustic analyses demonstrating a high degree of acoustic variation in a variety of animal vocal repertoires, particularly close distance vocalizations. Our findings add on to (1) the recent argument that the common practice of describing vocal repertoires as either discrete or graded may be of little value as such distinctions may be driven by human perception and non-quantitative descriptions of vocal repertoires, and (2) recent studies indicating that flexibility in close range social calls can come about through combinatorial systems, which previously have been studied primarily in long distance vocalizations. Furthermore, our study highlights differences in the vocal repertoire of western and mountain gorillas, as expected given differences in environment and social behaviour. Our results offer opportunities for further in-depth studies investigating the function of the gorilla close calls, which will contribute to a more comprehensive understanding of ape vocal communication in general.

Acoustic structure and variation in mountain and western gorilla close calls: a syntactic approach

in Behaviour



  • AbramsonA.S.LiskerL. (1970). Discrimination along the voicing continuum: cross-language tests. — In: Proceedings of the 6th International Congress on Phonetic Science Academiac Prague p. 569-573.

  • AltmannJ. (1974). Observational study of behavior: sampling methods. — Behaviour 49: 227-267.

  • ArnoldK.ZuberbühlerK. (2008). Meaningful call combinations in a non-human primate. — Curr. Biol. 18: 202-203.

  • ArnoldK.ZuberbühlerK. (2012). Call combinations in monkeys: compositional or idiomatic expressions?Brain Lang. 120: 303-309.

  • BaughA.T.AkreK.L.RyanM.J. (2008). Categorical perception of a natural multi-variate signal: mating call recognition in túngara frogs. — Proc. Natl. Acad. Sci. USA 105: 8985-8988.

  • BerwickR.C.OkanoyaK.BeckersG.J.L.BolhuisJ.J. (2011). Songs to syntax: the linguistics of birdsong. — Trends Cogn. Sci. 15: 113-121.

  • BlumsteinD.T.ArmitageK.B. (1997). Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. — Am. Nat. 150: 179-200.

  • BoinskiS. (1993). Vocal coordination of troop movement among white-faced capuchin monkeys Cebus capuchinus. — Am. J. Primatol. 30: 85-100.

  • BoinskiS.CampbellA.F. (1996). The huh vocalization of white-faced capuchins: a spacing call disguised as a food call?Ethology 102: 826-840.

  • BouchetH.Blois-HeulinC.PellierA.ZuberbühlerK.LemassonA. (2012). Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus). — J. Comp. Psychol. 126: 45-56.

  • BradburyJ.W.VehrencampS.L. (2011). Principles of animal communication. — Sinauer AssociatesSunderland, MA.

  • BradleyB.J.RobbinsM.M.WilliamsonE.A.SteklisH.D.SteklisN.G.EckhardtN.BoeschC.VigilantL. (2005). Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. — Proc. Natl. Acad. Sci. USA 102: 9418-9423.

  • CairnsS.J.SchwagerS.J. (1987). A comparison of association indices. — Anim. Behav. 35: 1454-1469.

  • CandiottiA.ZuberbühlerK.LemassonA. (2012). Context-related call combinations in female Diana monkeys. — Anim. Cogn. 15: 327-339.

  • CharltonB.D.EllisW.A.H.LarkinR.FitchW.T. (2012). Perception of size-related formant information in male koalas (Phascolarctos cinereus). — Anim. Cogn. 15: 999-1006.

  • CheneyD.L.SeyfarthR.M.SilkJ.B. (1995). The role of grunts in reconciling opponents and facilitating interactions among adult female baboons. — Anim. Behav. 50: 249-257.

  • ClarkeE.ReichardU.H.ZuberbühlerK. (2006). The syntax and meaning of wild gibbon songs. — PLoS ONE 1: e73.

  • ClayZ.ZuberbühlerK. (2011). Bonobos extract meaning from call sequences. — PLoS ONE 6: e18786.

  • ClevelandJ.SnowdonC.T. (1982). The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus). — Ethology 58: 231-270.

  • CrockfordC.BoeschC. (2005). Call combinations in wild chimpanzees. — Behaviour 142: 397-421.

  • CrockfordC.HerbigerI.VigilantL.BoeschC. (2004). Wild chimpanzees produce group-specific calls: a case for vocal learning?Ethology 110: 221-243.

  • CrockfordC.WittigR.M.MundryR.ZuberbühlerK. (2012). Wild chimpanzees inform ignorant group members of danger. — Curr. Biol. 22: 142-146.

  • DoranD.McNeilageA. (1998). Gorilla ecology and behaviour. — Evol. Anthropol. 6: 120-131.

  • EensM.PinxtenR.VerheyenR.F. (1989). Temporal and sequential organisation of song bouts in the starling. — Ardea 77: 75-86.

  • ElowsonA.M.SnowdonC.T. (1994). Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. — Anim. Behav. 47: 1267-1277.

  • FagenR.M.GoldmanR.N. (1977). Behavioural catalogue analysis methods. — Anim. Behav. 25: 261-274.

  • FischerJ. (1998). Barbary macaques categorize shrill barks into two call types. — Anim. Behav. 55: 799-807.

  • FischerJ.HammerschmidtK.TodtD. (1995). Factors affecting acoustic variation in Barbary-macaque (Macaca sylvanus) disturbance calls. — Ethology 101: 51-66.

  • FischerJ.NoserR.HammerschmidtK. (2013). Bioacoustic field research: a primer to acoustic analyses and playback experiments with primates. — Am. J. Primatol. 75: 643-663.

  • FosseyD. (1972). Vocalizations of the mountain gorilla (Gorilla gorilla beringei). — Anim. Behav. 20: 36-53.

  • FraleyC.RafteryA.MurphyT.B.ScruccaL. (2012). MClust version 4 for R: normal mixture modelling for model-based clustering classification and density estimation. — Available online at

  • FranzM.GollerF. (2002). Respiratory units of motor production and song imitation in the zebra finch. — J. Neurobiol. 51: 129-141.

  • FreebergT.M.DunbarR.I.M.OrdT.J. (2012). Social complexity as a proximate and ultimate factor in communicative complexity. — Phil. Trans. Roy. Soc. B 367: 1785-1801.

  • FuruiS. (1986). On the role of spectral transition for speech perception. — J. Acoust. Soc. Am. 80: 1016-1025.

  • GruberT.ZuberbühlerK. (2013). Vocal recruitment for joint travel in wilde chimpanzees. — PLoS ONE 8: e76073.

  • GustisonM.L.le RouxA.BergmanT.J. (2012). Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates. — Phil. Trans. Roy. Soc. B 367: 1847-1859.

  • HammerschmidtK. (1990). Individuelle Lautmuster bei Berberaffen (Macaca sylvanus): Ein Ansatz zum Verständnis ihrer vokalen Kommunikation. — Dissertation Freie Universität Berlin Berlin.

  • HammerschmidtK.FischerJ. (1998). The vocal repertoire of Barbary macaques: a quantitative analysis of a graded signal system. — Ethology 104: 203-216.

  • HarcourtA.H.StewartK.J. (1996). Function and meaning of wild gorilla ‘close’ calls 2. Correlations with rank and relatedness. — Behaviour 133: 827-845.

  • HarcourtA.H.StewartK.J. (2001). Vocal relationships of wild mountain gorillas. — In: Mountain gorillas. Three decades of research at Karisoke ( RobbinsM.M.SicotteP.StewartK.J. eds). Cambridge University PressLondon p.  241-262.

  • HarcourtA.H.StewartK.J.HarcourtD.E. (1986). Vocalizations and social relationships of wild gorillas: a preliminary analysis. — In: Current perspectives in primate social dynamics ( TaubD.M.KingF.A. eds). Van Nostrand ReinholdNew York, NY p.  346-356.

  • HarcourtA.H.StewartK.J.HauserM. (1993). Functions of wild gorilla ‘close calls’. I. Repertoire, context, and interspecific comparison. — Behaviour 124: 89-122.

  • HohmannG. (1989). Comparative study of vocal communication in two Asian leaf monkeys, Presbytis johnii and Presbytis entellus. — Folia Primatol. 52: 27-57.

  • JanikV.M.SayighL.S.WellsR.S. (2006). Signature whistle shape conveys identity information to bottlenose dolphins. — Proc. Natl. Acad. Sci. USA 103: 8293-8297.

  • JansenD.A.W.A.M.CantM.A.ManserM.B. (2012). Segmental concatenation of individual signatures and context cues in banded mongoose (Mungos mungo) close calls. — BMC Biol. 10: 97.

  • JiA.JohnsonM.T.WalshE.J.McGeeJ.ArmstrongD.L. (2013). Discrimination of individual tigers (Panthera tigris) from long distance roars. — J. Acoust. Soc. Am. 133: 1762-1769.

  • KeenanS.LemassonA.Klaus ZuberbühlerK. (2013). Graded or discrete? A quantitative analysis of Campbell’s monkey alarm calls. — Anim. Behav. 85: 109-118.

  • KuhlP.K.MillerJ.D. (1975). Speech perception by the chinchilla: voiced-voiceless distinction in alveolarplosive consonants. — Science 190: 69-72.

  • LemassonA.HausbergerM. (2011). Acoustic variability and social significance of calls in female Campbell’s monkeys (Cercopithecus campbelli campbelli). — J. Acoust. Soc. Am. 129: 3341-3352.

  • MaciejP.FischerJ.HammerschmidtK. (2011). Transmission characteristics of primate vocalizations: implications for acoustic analyses. — PLoS ONE 6: e23015.

  • ManserM.B. (2001). The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 2315-2324.

  • MarlerP. (2000). Origins of music and speech: insights from animals. — In: The origins of music ( WallinN.L.MerkerB.BrownS. eds). MIT PressCambridge, MA p.  31-48.

  • MasiS.CipollettaC.RobbinsM.M. (2009). Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory. — Am. J. Primatol. 71: 91-100.

  • MayB.MoodyD.B.StebbinsW.C. (1989). Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. — J. Acoust. Soc. Am. 85: 837-847.

  • McCombK.SempleS. (2005). Coevolution of vocal communication and sociality in primates. — Biol. Lett. 1: 381-385.

  • MitaniJ.C.Gros-LouisJ.MacedoniaJ.M. (1996). Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. — Int. J. Primatol. 17: 569-583.

  • MitaniJ.C.MarlerP. (1989). A phonological analysis of male gibbon singing behavior. — Behaviour 109: 20-45.

  • MortonE.S. (1975). Ecological sources of selection on avian sounds. — Am. Nat. 109: 17-34.

  • NelsonD.A.MarlerP. (1989). Categorical perception of a natural stimulus continuum: birdsong. — Science 244: 976-978.

  • NkurunungiJ.B.GanasJ.RobbinsM.M.StanfordC.B. (2005). A comparison of two mountain gorilla habitats in Bwindi Impenetrable National Park, Uganda. — Afr. J. Ecol. 42: 289-297.

  • OuattaraK.LemassonA.ZuberbühlerK. (2009). Campbell’s monkeys concatenate vocalizations into context-specific call sequences. — Proc. Natl. Acad. Sci. USA 106: 22026-22031.

  • OwrenM.J.AmossR.T.RendallD. (2011). Two organizing principles of vocal production: implications for nonhuman and human primates. — Am. J. Primatol. 73: 530-544.

  • PfefferleD.FischerJ. (2003). Sounds and size — identification of variables that reflect body size in hamadryas baboons. — Folia Primatol. 74: 212.

  • R Core Development Team (2011). R: a language and environment for statistical computing. — R Foundation for Statistical ComputingVienna.

  • RevelleW. (2011). Psych: procedures for personality and psychological research. — R Foundation for Statistical ComputingVienna.

  • RobbinsM.M. (2008). Feeding competition and agonistic relationships among Bwindi Gorilla beringei. — Int. J. Primatol. 29: 999-1018.

  • RobbinsM.M. (2010). Gorillas: diversity in ecology and behaviour. — In: Primates in perspective ( CampbellC.J.FuentesA.MacKinnonK.C.BearderS.StumpfR. eds). Oxford University PressOxford p.  326-339.

  • RobinsonJ.G. (1984). Syntactic structures in the vocalizations of wedge-capped capuchin monkeys, Cebus olivaceus. — Behaviour 90: 46-79.

  • RousseeuwP.J. (1987). Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. — Comput. Appl. Math. 20: 53-65.

  • SalmiR.HammerschmidtK.Doran-SheehyD.M. (2013). Western gorilla vocal repertoire and contextual use of vocalizations. — Ethology 119: 831-847.

  • SchallerG.B. (1963). The mountain gorilla. — University of Chicago PressChicago, IL.

  • SchelA.M.MachandaZ.TownsendS.W.ZuberbühlerK.SlocombeK.E. (2013). Chimpanzee food calls are directed at specific individuals. — Anim. Behav. 86: 955-965.

  • SchwarzG.E. (1978). Estimating the dimension of a model. — Ann. Stat. 6: 461-464.

  • SeyfarthR.M.CheneyD.L.HarcourtA.H.StewartK.J. (1994). The acoustic features of gorilla double grunts and their relation to behaviour. — Am. J. Primatol. 33: 31-50.

  • ShapiroA.D.TyackP.L.SeneffS. (2011). Comparing call-based versus subunit-based methods for categorizing Norwegian killer whale, Orcinus orca, vocalizations. — Anim. Behav. 81: 377-386.

  • SicotteP. (1994). Effect of male competition on male–female relationships in bi-male groups of mountain gorillas. — Ethology 97: 47-64.

  • SilkJ.B.KaldorE.BoydR. (2000). Cheap talk when interests conflict. — Anim. Behav. 59: 423-432.

  • SlocombeK.E.ZuberbühlerK. (2005). Functionally referential communication in a chimpanzee. — Curr. Biol. 15: 1779-1784.

  • SlocombeK.E.TownsendS.W.ZuberbühlerK. (2009). Wild chimpanzees (Pan troglodytes schweinfurthii) distinguish between different scream types: evidence from a playback study. — Anim. Cogn. 12: 441-449.

  • SnowdonC.T.PolaY.V. (1978). Interspecific and intraspecific responses to synthesized pygmy marmoset vocalizations. — Anim. Behav. 26: 192-206.

  • SnowdonC.T. (1997). Affiliative processes and vocal development. — Ann. N.Y. Acad. Sci. 807: 340-351.

  • SokalR.R.RohlfF.J. (1995). The principles and practice of statistics in biological research. — W.H. FreemanNew York, NY.

  • StebbinsW.C.SommersM.S. (1992). Evolution, perception, and the comparative method. — In: The evolutionary biology of hearing ( WebsterD.B.FayR.R.PopperA.N. eds). SpringerNew York, NY p.  211-227.

  • StewartK.J.HarcourtA.H. (1994). Gorillas’ vocalizations during rest periods: signals of impending departure?Behaviour 130: 29-40.

  • SugiuraH. (2007). Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese macaques. — Am. J. Primatol. 69: 1412-1424.

  • SuzukiT.N. (2014). Communication about predator type by a bird using discrete, graded and combinatorial variation in alarm calls. — Anim. Behav. 87: 59-65.

  • TalletC.LinhartP.PolichtR.HammerschmidtK.ŠimečekP.KratinovaP.ŠpinkaM. (2013). Encoding of situations in the vocal repertoire of piglets (Sus scrofa): a comparison of discrete and graded classifications. — PloS ONE 8: e71841.

  • ten CateC.OkanoyaK. (2012). Revisiting the syntactic abilities of non-human animals: natural vocalizations and artificial grammar learning. — Phil. Trans. Roy. Soc. B 367: 1984-1994.

  • WaserP.M.BrownC.H. (1986). Habitat acoustics and primate communication. — Am. J. Primatol. 10: 135-154.

  • WattsD.P. (1991). Mountain gorilla reproduction and sexual behavior. — Am. J. Primatol. 24: 211-225.

  • WhithamJ.C.GeraldM.S.MaestripieriD. (2007). Intended receivers and functional significance of grunt and girney vocalizations in free-ranging female rhesus macaques. — Ethology 113: 862-874.

  • WichS.A.KrutzenM.LameiraA.R.NaterA.AroraN.BastianM.L.MeulmanE.Morrogh-BernardH.C.AtmokoS.S.U.PamungkasJ.Perwitasari-FarajallahD.HardusM.E.van NoordwijkM.van SchaikC.P. (2012). Call Cultures in Orang-Utans?PLoS ONE 7: e36180.

  • WymanM.T.MooringM.S.McCowanB.PenedomM.C.T.RebyD.HartL.A. (2012). Acoustic cues to size and quality in the vocalizations of male North American bison, Bison bison. — Anim. Behav. 84: 1381-1391.

  • WyttenbachR.A.MayM.L.HoyR.R. (1996). Categorical perception of sound frequency by crickets. — Science 273: 1542-1544.

  • ZuberbühlerK. (2002). A syntactic rule in forest monkey communication. — Anim. Behav. 63: 293-299.

  • HornJ.L. (1965). A rationale and test for the numbp-valueer of factors in factor analysis. — Psychometrika 30: 179-185.

  • FraleyC.RafteryA.ScruccaL. (2012). MClust: Normal mixture modelling for model-based clustering classification and density estimation. — R Foundation for Statistical ComputingVienna.

  • RafteryA.E. (1995). Bayesian model selection and social research. — Sociol. Methodol. 25: 111-163.

  • RevelleW. (2011). Psych: Procedures for Personality and Psychological Research. — R Foundation for Statistical ComputingVienna.

  • RousseeuwP.J. (1987). Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. — Comput. Appl. Math. 20: 53-65.

  • SchwarzG.E. (1978). Estimating the dimension of a model. — Ann. Stat. 6: 461-464.


  • View in gallery

    Spectrograms of representative gorilla close calls recorded in this study, their subdivision into units and categorization into unit types. Spectrograms a–f illustrate typical examples of syllabled calls: (a–e) double grunts, (f) single grunt. Spectrograms g–k illustrate non-syllabled calls: (g) grumble; (h, i) hums; (j, k) mixed calls. Calls were subdivided into units (indicated by black lines) based on the occurrence of periods of silence of less than 2 s duration (a–e, h, i) or abrupt changes in the distribution of energy (j, k). The units were categorized as atonal or tonal according to the presence/absence of harmonic frequency bands. Indicated above the lines are the unit type each unit was assigned to via cluster analysis: a1, atonal grunts; t1, short hums; t2, short tonal grunts; t3, long hums; t4, grumbles.

  • View in gallery

    Operational definitions and schematic overview of analyses used in this study.

  • View in gallery

    Spectrograms of the 5 unit types. Short hums (t1) were usually under 1-s short, tonal, high pitched units. Tonal grunts (t2) were short, low pitched grunts. Atonal grunts (a1) were on average short, noisy grunts that, however, could be up to 2 s long. Grumbles (t4) were up to 5 s long and low pitched. Long hums (t3) were long tonal, high pitched units.

  • View in gallery

    Combinatorial associations between unit types in both gorilla groups. Lines indicate the average Dice index of combinatorial association as a measure of how frequently any two unit types were observed together in the same call. Average values were calculated from the individuals’ Dice indices for a given pair of unit types. The legend shows the thickness of the lines corresponding to the minimum and maximum average Dice index.

  • View in gallery

    Sequential associations between unit types in the blackbacks and adult females of the mountain gorilla group. Lines indicate the average Dice index for sequential association as a measure of how frequently any two unit types followed one another in immediate succession. Average values were calculated from the individuals’ Dice indices for a given pair of unit types. The legend depicts the thickness of the lines corresponding to the minimum and maximum average Dice index. For reasons of clarity illustrations include only transitions with a Dice index > 0.05.

  • View in gallery

    Results of Spearman correlations between acoustic parameters measured for (a) atonal and (b) tonal units. (a) Correlations between acoustic parameters measured for atonal units. (b) Correlations between acoustic parameters measured for tonal units.

  • View in gallery

    Goodness of fit (using BIC) of different cluster solutions for atonal and tonal units as a function of the number of unit types (clusters). Differently coloured lines indicate different parameterizations of cluster solutions, varying in cluster shape. The best cluster solution is indicated by an arrow. (a) Atonal units; (b) tonal units.

  • View in gallery

    Silhouette coefficients of the different cluster solutions for tonal and atonal units as a function of the number of unit types (clusters). A silhouette coefficient < 0.25 indicates strong intergradation, silhouette coefficients between 0.25 to 0.5 weak clustering.

  • View in gallery

    Silhouette plots illustrating the most discrete cluster solutions with four unit types (clusters) for atonal units, with an overall silhouette coefficient of 0.15 (left) and with four unit types for tonal units, with an overall silhouette coefficient of 0.48 (right). The plot displays the silhouette widths for each unit as horizontal bars, ordered by clusters and by silhouette value within cluster. The silhouette width is a measure of how clearly a unit belongs to its assigned cluster. Compact clusters consist of units with high silhouette widths. N indicates the number of units allocated to each cluster. S(cn) is the silhouette coefficient of each cluster.

  • View in gallery

    Best cluster solutions for 2 to 10 unit types (clusters) of tonal units. Indicated are the values of the principal component for acoustic parameters describing the fundamental frequency on the y-axis and the transformed duration on the x-axis. Different colours and symbols indicate different clusters. For each cluster the cluster mean is marked and ellipses indicate corresponding covariance. Note that an increase in the number of clusters usually largely lead to a split of a certain cluster rather than a more fundamental change in the arrangement of units into clusters.

  • View in gallery

    Sequential associations between unit types in the adult females of both gorilla groups. Lines indicate the average Dice index of sequential association as a measure of how frequently any two unit types followed one another in immediate succession. Average values were calculated from the individuals’ Dice indices for a given pair of unit types. The legend depicts the thickness of the lines corresponding to the minimum and maximum average Dice index. Included are only unit types shared by all adult females.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 75 75 8
Full Text Views 138 138 2
PDF Downloads 7 7 2
EPUB Downloads 0 0 0