Dance displays in gibbons: biological and linguistic perspectives on structured, intentional, and rhythmic body movement
Language English Country Japan Media print-electronic
Document type Journal Article
Grant support
788077
HORIZON EUROPE European Research Council
Orisem
HORIZON EUROPE European Research Council
ANR-17-EURE-0017
Agence Nationale de la Recherche
ANR-11-LABX-0027-01
Agence Nationale de la Recherche
Career development programme
Universitetet i Oslo
945408
H2020 Marie Skłodowska-Curie Actions
PubMed
39365409
PubMed Central
PMC11735528
DOI
10.1007/s10329-024-01154-4
PII: 10.1007/s10329-024-01154-4
Knihovny.cz E-resources
- Keywords
- Dance syntax, Isochrony, Primate communication, Small apes, Super linguistics,
- MeSH
- Video Recording MeSH
- Hylobates * physiology MeSH
- Animal Communication * MeSH
- Movement MeSH
- Dancing * MeSH
- Animals MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
Female crested gibbons (genus Nomascus) perform conspicuous sequences of twitching movements involving the rump and extremities. However, these dances have attracted little scientific attention and their structure and meaning remain largely obscure. Here we analyse close-range video recordings of captive crested gibbons, extracting descriptions of dance in four species (N. annamensis, N. gabriellae, N. leucogenys and N. siki). In addition, we report results from a survey amongst relevant professionals clarifying behavioural contexts of dance in captive and wild crested gibbons. Our results demonstrate that dances in Nomascus represent a common and intentional form of visual communication restricted to sexually mature females. Whilst primarily used as a proceptive signal to solicit copulation, dances occur in a wide range of contexts related to arousal and/or frustration in captivity. A linguistically informed view of this sequential behaviour demonstrates that movement within dances is organized in groups and follows an isochronous rhythm - patterns not described for visual displays in other non-human primates. We argue that applying the concept of dance to gibbons allows us to expand our understanding of communication in non-human primates and to develop hypotheses on the rules and regularities characterising it. We propose that crested gibbon dances likely evolved from less elaborate rhythmic proceptive signals, similar to those found in siamangs. Although dance displays in humans and crested gibbons share a number of key characteristics, they cannot be assumed to be homologous. Nevertheless, gibbon dances represent a striking model behaviour to investigate the use of complex gestural signals in hominoid primates.
Institut Jean Nicod Paris France
Institute for Cell Biology Heinrich Heine University Düsseldorf Germany
Super Linguistics Research Group University of Oslo Oslo Norway
See more in PubMed
Baldwin LA, Teleki G (1976) Patterns of gibbon behavior on Hall’s Island, Bermuda: A preliminary ethogram for Hylobates lar. In: Rumbaugh DM (ed) Gibbon and Siamang, vol 4. Suspensory behavior, locomotion, and other behaviors of captive gibbons. Cognition. Karger, Basel, Switzerland, pp 21–105
Barca B, Vincent C, Soeung K, Nuttall M, Hobson K (2016) Multi-female group in the southernmost species of Nomascus: field observations in eastern Cambodia reveal multiple breeding females in a single group of southern yellow-cheeked crested gibbon Nomascus gabriellae. Asian Primates Journal 6(1):15–19
Berthet M, Coye C, Dezecache G, Kuhn J (2023) Animal linguistics: a primer. Biol Rev 98(1):81–98 PubMed PMC
Bertolo M, Singh M, Mehr SA (2021) Sound-induced motion in chimpanzees does not imply shared ancestry for music or dance. Proc Natl Acad Sci USA 118(2):e2015664118 PubMed PMC
Berwick RC, Okanoya K, Beckers GJ, Bolhuis JJ (2011) Songs to syntax: the linguistics of birdsong. Trends Cogn Sci 15(3):113–121 PubMed
Bolechova P, Chaloupkova H, Hradec M, Janova E, Doležalová J (2019) Fur color change and hormonal development in captive females of Northern white-cheeked (Nomascus leucogenys) and buff-cheeked (Nomascus gabriellae) gibbons. Gen Comp Endocrinol 282:113210 PubMed
Botting J, Bastian M (2019) Orangutans (Pongo pygmaeus and hybrid) and gorillas (Gorilla gorilla gorilla) modify their visual, but not auditory, communicative behaviors, depending on the attentional state of a human experimenter. Int J Primatol 40(2):244–262
Burns BL, Judge DS (2016) The varied path to adulthood: Plasticity in developmental timing in hylobatids. Am J Primatol 78(6):610–625 PubMed
Byrne RW, Cartmill E, Genty E, Graham KE, Hobaiter C, Tanner J (2017) Great ape gestures: intentional communication with a rich set of innate signals. Anim Cog 20:755–769 PubMed PMC
Carbone L, Alan Harris R, Gnerre S, Veeramah KR, Lorente-Galdos B, Huddleston J et al (2014) Gibbon genome and the fast karyotype evolution of small apes. Nature 513(7517):195–201 PubMed PMC
Cartmill EA, Byrne RW (2010) Semantics of primate gestures: intentional meanings of orangutan gestures. Anim Cog 13:793–804 PubMed
Caspar KR, Kammerer C, Hradec M (2020) Attention-getting in a white-cheeked gibbon by means of a novel vocalization? Behaviour 157(14–15):1245–1255
CCTV (2016) The Power of Nature, Episode 2. Chinese television documentary. Retrieved from: https://youtu.be/4OiCht-jXSM?si=9kDaK87K_d6tDpSh
Charnavel I (2019) Steps toward a universal grammar of dance: local grouping structure in basic human movement perception. Front Psychol 10:1364 PubMed PMC
Cheyne SM (2006) Unusual behaviour of captive-raised gibbons: implications for welfare. Primates 47:322–326 PubMed
Clarke E, Reichard UH, Zuberbühler K (2006) The syntax and meaning of wild gibbon songs. PLoS ONE 1:e73 PubMed PMC
Cooke CM, Schillaci MA (2007) Behavioral responses to the zoo environment by white-handed gibbons. Anim Behav Sci 106(1–3):125–133
Delacour J (1933) On the Indochinese gibbons (Hylobates concolor). J Mammal 14(1):71–73
Dooley HM, Judge DS (2015) Kloss gibbon (Hylobates klossii) behavior facilitates the avoidance of human predation in the Peleonan forest, Siberut Island, Indonesia. Am J Primatol 77(3):296–308 PubMed
Dufour V, Poulin N, Curé C, Sterck EH (2015) Chimpanzee drumming: a spontaneous performance with characteristics of human musical drumming. Sci Rep 5(1):11320 PubMed PMC
Fan PF, Ma CY, Garber PA, Zhang W, Fei HL, Xiao W (2016) Rhythmic displays of female gibbons offer insight into the origin of dance. Sci Rep 6(1):1–8 PubMed PMC
Florkiewicz B, Skollar G, Reichard UH (2018) Facial expressions and pair bonds in hylobatids. Am J Phys Anthropol 167(1):108–123 PubMed
Francis ST (1991) The origins of dance: the perspective of primate evolution. Dance Chronicle 14(2–3):203–220
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7(11):1325–1330
Fröhlich M, Bartolotta N, Fryns C, Wagner C, Momon L, Jaffrezic M et al (2021) Orangutans have larger gestural repertoires in captivity than in the wild—A case of weak innovation? Iscience 24(11):103304 PubMed PMC
Geissmann T (2002) Duet-splitting and the evolution of gibbon songs. Biol Rev 77:57–76 PubMed
Geissmann T, Nguyen XD, Lormée N, Momberg F (2000) Vietnam primate conservation status review 2000 - Part 1: Gibbons, English. Fauna Flora Int., Indochina Programme, Hanoi, Vietnam.
Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cog 12:527–546 PubMed PMC
De Gregorio C, Raimondi T, Valeria B, Chiara P, Valente D, Carugati F, Bandoli F, Favaro L, Lefaux, B, Ravignani A, Gamba M (2023) Isochronous singing in three crested gibbon species (Nomascus spp.). Curr Zool, zoad029 PubMed PMC
Guan ZH, Ma CY, Fei HL, Huang B, Ning WH, Ni QY et al (2018) Ecology and social system of northern gibbons living in cold seasonal forests. Zool Res 39(4):255–265 PubMed PMC
Hanna JL (1979) To dance is human: a theory of nonverbal communication. University of Chicago Press, Chicago, IL, USA
Hanna JL (2017) Dancing to resist, reduce and escape stress. In: Karkou V, Sue O, Lycouris S (eds) The Oxford Handbook of Dance and Wellbeing. Oxford University Press, Oxford, UK, pp 97–112
Hopkins WD, Washburn DA (2002) Matching visual stimuli on the basis of global and local features by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). Anim Cog 5:27–31 PubMed PMC
Hosey GR, Skyner LJ (2007) Self-injurious behavior in zoo primates. Int J Primatol 28:1431–1437
Hu Y, Xu HL, Yang D (1989) The studies on ecology in Hylobates leucogenys. Zool Res 10(Supplement):61–67
Huang B, Guan Z, Ni Q, Orkin JD, Fan P, Jiang X (2013) Observation of intra-group and extra-group copulation and reproductive characters in free ranging groups of western black crested gibbon (Nomascus concolor jingdongensis). Integr Zool 8(4):427–440 PubMed
Kenyon M, Roos C, Binh VT, Chivers D (2011) Extrapair paternity in golden-cheeked gibbons (Nomascus gabriellae) in the secondary lowland forest of Cat Tien National Park. Vietnam Folia Primatol 82(3):154–164 PubMed
King A (2021) The thinking skills of two gibbon species: representation, reasoning & reflection in Hoolock leuconedys and Nomascus leucogenys. Doctoral dissertation. The Australian National University, Canberra, Australia
Kumar A, Sharma M (2017) Reproductive biology of eastern hoolock gibbon Hoolock leuconedys in conservation breeding centre at biological park, Itanagar, Arunachal Pradesh. India Int J Zool Res 13:93–104
Laland K, Wilkins C, Clayton N (2016) The evolution of dance. Curr Biol 26(1):R5–R9 PubMed
Lameira AR, Hardus ME, Ravignani A, Raimondi T, Gamba M (2024) Recursive self-embedded vocal motifs in wild orangutans. eLife, 12:RP88348 PubMed PMC
Lerdahl F, Jackendoff R (1983) An overview of hierarchical structure in music. Music Percept 1(2):229–252
Li P, Garber PA, Bi Y, Jin K, Qi X, Zhou J (2022) Diverse grouping and mating strategies in the Critically Endangered Hainan gibbon (Nomascus hainanus). Primates 63(3):237–243 PubMed PMC
Liebal K, Pika S, Tomasello M (2004) Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates 45(1):41–57 PubMed
Lukas KE, Barkauskas RT, Maher SA, Jacobs BA, Bauman JE, Henderson AJ, Calcagno JM (2002) Longitudinal study of delayed reproductive success in a pair of white-cheeked gibbons (Hylobates leucogenys). Zoo Biol 21(5):413–434
Ma H, Wang Z, Han P, Fan P, Chapman CA, Garber PA, Fan P (2024) Small apes adjust rhythms to facilitate song coordination. Curr Biol 34(5):935–945 PubMed
Malone NM, Fuentes A (2009) The ecology and evolution of hylobatid communities: causal and contextual factors underlying inter- and intraspecific variation. In: Whittaker D, Lappan S (eds) The gibbons: new perspectives on small ape socioecology and population biology. Springer, New York City, NY, USA, pp 241–264
Margulis SW, Hálfdanardótti MR (2021) Hormones and color change in female white-cheeked gibbons, Nomascus leucogenys. Int J Primatol 42:201–219
Maxwell S (1984) Gibbons in captivity: observations and comments on their diet, behavior, breeding, housing, health, and sanitation. — In: Proceedings of the AAZPA western regional conference, gibbon and gallinaceous bird center, Saugus, CA; p. 202–210.
Mootnick AR, Baker E (1994) Masturbation in captive Hylobates (gibbons). Zoo Biol 13(4):345–353
Mootnick AR, Fan PF (2011) A comparative study of crested gibbons (Nomascus). Am J Primatol 73(2):135–154 PubMed
Mootnick AR, Cunningham C, Baker E (2012) Phylogenetic separation in limb use in captive gibbons (Hylobatidae): a comparison across the primate order. Am J Primatol 74(11):1035–1043 PubMed
Orgeldinger M (1999) Paarbeziehung beim Siamang-Gibbon (Hylobates syndactylus) im Zoo: Untersuchungen über den Einfluss von Jungtieren auf die Paarbindung. Schüling, Münster, Germany
Palombit RA (1992) Pair bonds and monogamy in wild siamang (Hylobates syndactylus) and white-handed gibbon (Hylobates lar) in northern Sumatra. Doctoral dissertation, University of California, Davis, CA, USA.
Perry S (1996) Intergroup encounters in wild white-faced capuchins (Cebus capucinus). Int J Primatol. 10.1007/BF02736624
R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ravignani A, Madison G (2017) The paradox of isochrony in the evolution of human rhythm. Front Psychol 8:280885 PubMed PMC
Roos C (2016) Phylogeny and classification of gibbons (Hylobatidae). In: Reichard UH, Hirai H, Barelli C (eds) Evolution of gibbons and siamang. Springer, New York City, New York, USA, pp 151–165
Scheider L, Waller BM, Oña L, Burrows AM, Liebal K (2016) Social use of facial expressions in hylobatids. PLoS ONE 11(3):e0151733 PubMed PMC
Scholes E, Gillis JM, Laman TG (2017) Visual and acoustic components of courtship in the bird-of-paradise genus Astrapia (Aves: Paradisaeidae). PeerJ 5:e3987 PubMed PMC
Shi CM, Yang Z (2018) Coalescent-based analyses of genomic sequence data provide a robust resolution of phylogenetic relationships among major groups of gibbons. Mol Biol Evol 35(1):159–179 PubMed PMC
Thinh VN, Rawson B, Hallam C, Kenyon M, Nadler T, Walter L, Roos C (2010) Phylogeny and distribution of crested gibbons (genus Nomascus) based on mitochondrial cytochrome b gene sequence data. Am J Primatol 72(12):1047–1054 PubMed
De Vries J, (2004) A white-cheeked crested gibbon ethogram. Thesis, Van Hall Institute, Leeuwarden, the Netherlands.
Wertheimer M (1938) Laws of organization in perceptual forms. Psychol Forschung 4:301–350
Winking S (2016) Behavior of gibbons in the presence of a mirror - A study at Duisburg Zoo. Bachelor’s thesis, University of Duisburg-Essen, Essen, Germany.
Zheng RQ (1988) A preliminary observation on mating behavior in Hylobates concolor. Zool Res 9:112 (In Chinese)
Zhou J, Wei F, Li M, Pui Lok CB, Wang D (2008) Reproductive characters and mating behaviour of wild Nomascus hainanus. Int J Primatol 29(4):1037–1046