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International Journal of Primatology

, Volume 38, Issue 3, pp 533–552 | Cite as

Female Songs of the Nonduetting Javan Gibbons (Hylobates moloch) Function for Territorial Defense

  • Soojung Ham
  • Susan Lappan
  • Daniela Hedwig
  • Jae Chun Choe
Article

Abstract

Duets in territorial, pair-living primates may function to maintain intragroup cohesion, promote intergroup avoidance, and assist in territorial and resource defense, as well as advertising and reinforcing pair bonds. Despite the absence of duetting in Javan gibbons (Hylobates moloch), recent playback experiments suggested that Javan gibbon songs also play a role in pair-bond advertisement as well as territorial and mate defense. However, playback experiments only assess motivations of the listener, which may not reflect the motivations of the caller. We conducted an observational study of naturally occurring female songs in two groups of Javan gibbons from July 2009 to March 2010 and from March to November 2011 in Gunung Halimun–Salak National Park, Indonesia. We investigated female singing rates in relation to singing location, daily path length, occurrence of intergroup encounters, feeding rate, allogrooming rate, and distance between pair mates. The two females produced 47 songs during 164 observation days. Females in the area of their home range that overlapped with neighboring groups sang more frequently than expected based on time spent in the area of overlap vs. the home range interior. Groups also had longer daily path lengths on days when females sang than on nonsinging days, and on days when they visited the area of overlap than on nonvisiting days. Our findings indicate that, like the duets of other pair-living territorial primates, female Javan gibbon songs function for territorial defense, but we found no support for other functions such as intergroup avoidance, resource defense, and pair-bond reinforcement.

Keywords

Nonduetting gibbons Primate long-distance calls Ranging behavior Social monogamy Song functions 

Notes

Acknowledgements

This project was conducted in collaboration with the Department of Natural Resource Conservation and Ecotourism at the Institut Pertanian Bogor (IPB). We thank the Indonesian Ministry of Research and Technology (RISTEK), the Indonesian Ministry of Forestry’s Department for the Protection and Conservation of Nature (PHKA), and the Gunung Halimun-Salak National Park (GHSNP) for granting us research permissions. We thank Rinekso Soekmadi, Agus Hikmat, Dones Rinaldi, Bambang Supriyanto, and GHSNP staff for their assistance and cooperation. We are grateful to Christophe Boesch, Catherine Crockford and Kurt Hammerschmidt for their advice on the discussion of this manuscript, to Roger Mundry and Colleen Stephens for their help with statistical analysis, and to Joanna Setchell and two anonymous reviewers for many helpful comments on the manuscript. Thanks to Sanha Kim for contributions to the establishment of the field site and advice on the progress of this study and the manuscript; Sunyoung Ahn for administrative support and coordination; and Aris, Nui, Sahri, Ami, and Jaya for assistance in the field. The authors declare that none of us have any conflict of interest in this research. This research was financially supported by the Amore Pacific Academic and Cultural Foundation (AACF), Ewha Womans University, National Institute of Ecology (NIE), German Academic Exchange Service (DAAD), the Max Planck Society (MPG), and Appalachian State University.

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References

  1. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.CrossRefPubMedGoogle Scholar
  2. Amsler, S. J. (2010). Energetic costs of territorial boundary patrols by wild chimpanzees. American Journal of Primatology, 72, 93–103.PubMedGoogle Scholar
  3. Baayen, R. H. (2008). Analyzing linguistic data: A practical introduction to statistics using R. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  4. Baldwin, J. D., & Baldwin, J. I. (1973). Interactions between adult female and infant howling monkeys (Alouatta palliata). Folia Primatologica, 20, 27–71.CrossRefGoogle Scholar
  5. Barelli, C., Boesch, C., Heistermann, M., & Reichard, U. H. (2008). Female white-handed gibbons (Hylobates lar) lead group movements and have priority of access to food resources. Behaviour, 145, 965–981.CrossRefGoogle Scholar
  6. Barelli, C., Reichard, U. H., & Mundry, R. (2011). Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar? Animal Behaviour, 82, 801–809.CrossRefGoogle Scholar
  7. Barr, D. J., Levy, R., Scheepers, C., & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68, 255–278.CrossRefGoogle Scholar
  8. Bartlett, T. Q. (2007). The Hylobatidae: Small apes of Asia. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, & S. K. Bearder (Eds.), Primates in perspective (pp. 300–312). New York: Oxford University Press.Google Scholar
  9. Bartlett, T. Q. (2009a). Seasonal home range use and defendability in white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand. In D. Whittaker & S. Lappan (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 265–275). Developments in primatology: Progress and prospects. New York: Springer Science+Business media.Google Scholar
  10. Bartlett, T. Q. (2009b). Territoriality and intergroup encounters. In R. W. Sussmann & N. Vasey (Eds.), The gibbons of Khao Yai: Seasonal variation in behaviour and ecology (pp. 103–119). Upper Saddle River: Pearson Prentice Hall.Google Scholar
  11. Bartlett, T. Q., Light, L. E. O., & Brockelman, W. Y. (2016). Long-term home range use in white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand. American Journal of Primatology, 78, 192–203.CrossRefPubMedGoogle Scholar
  12. Bates, D., Maechler, M., Bolker, B., & Walker, S. (2013). lme4: Linear mixed-effects models using Eigen and S4 classes. R package version 10–4. http://CRAN.R-project.org/package=lme4.
  13. Beyer, H.L. (2012). Geospatial modelling environment (v0.7.2.0). http://www.spatialecology.com/gme.
  14. Bivand, R. S., Pebesma, E. J., & Gomez-Rubio, V. (2013). Applied spatial data analysis with R. New York: Springer Science+Business Media.CrossRefGoogle Scholar
  15. Brockelman, W. Y., Reichard, U., Treesucon, U., & Raemaekers, J. J. (1998). Dispersal, pair formation and social structure in gibbons (Hylobates lar). Behavioral Ecology and Sociobiology, 42, 329–339.CrossRefGoogle Scholar
  16. Calenge, C. (2006). The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals. Ecological Modelling, 197, 516–519.CrossRefGoogle Scholar
  17. Cheney, D. L. (1987). Interactions and relationships between groups. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 267–281). Chicago: University of Chicago Press.Google Scholar
  18. Chivers, D. (1969). On the daily behaviour and spacing of howling monkey groups. Folia Primatologica, 10, 48–102.CrossRefGoogle Scholar
  19. Chivers, D. J. (1976). Communication within and between family groups of siamang (Symphalangus syndactylus). Behaviour, 57, 116–135.CrossRefGoogle Scholar
  20. Chivers, D. J., Anandam, M. V., Groves, C. P., Molur, S., Rawson, B. M., et al (2013). Family Hylobotidae (gibbons). In R. A. Mittermeier, A. B. Rylands, & D. E. Wilson (Eds.), Handbook of the mammals of the world (pp. 754–791). Barcelona: Lynx Edicions.Google Scholar
  21. Chivers, D. J., & MacKinnon, J. (1977). On the behaviour of siamang after playback of their calls. Primates, 18, 943–948.CrossRefGoogle Scholar
  22. Clarke, E., Reichard, U. H., & Zuberbühler, K. (2006). The syntax and meaning of wild gibbon song. PloS One, 1, e73.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cleveland, J., & Snowdon, C. T. (1982). The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus). Zeitschrift für Tierpsychologie, 58, 231–270.CrossRefGoogle Scholar
  24. Cohen, J., Cohen, P., West, S. G., & Aiken, L. S. (2003). Applied multiple regression/correlation analysis for the behavioral sciences. Mahwah: Lawrence Erlbaum.Google Scholar
  25. Cowlishaw, G. (1992). Song function in gibbons. Behaviour, 121, 131–153.CrossRefGoogle Scholar
  26. Dooley, H. M., Judge, D. S., & Schmitt, L. H. (2013). Singing by male and female Kloss gibbons (Hylobates klossii) in the Peleonan Forest, Siberut Island, Indonesia. Primates, 54, 39–48.CrossRefPubMedGoogle Scholar
  27. Ellefson, J. O. (1968). Territorial behavior in the common white-handed gibbon, Hylobates lar Linn. In P. C. Jay (Ed.), Primates: Studies in adaptation and variability (pp. 180–199). New York: Holt, Rinehart and Winston.Google Scholar
  28. ESRI (2011). ArcMap 10. Redlands: Environmental Systems Research Institute.Google Scholar
  29. Fan, P. F., & Jiang, X. L. (2008). Effects of food and topography on ranging behavior of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang Mountain, Yunnan, China. American Journal of Primatology, 70, 871–878.CrossRefPubMedGoogle Scholar
  30. Fan, P. F., Xiao, W., Huo, S., & Jiang, X. L. (2009). Singing behavior and singing functions of black-crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Central Yunnan, China. American Journal of Primatology, 71, 539–547.CrossRefPubMedGoogle Scholar
  31. Field, A. (2005). Discovering statistics using SPSS. London: SAGE.Google Scholar
  32. Forstmeier, W., & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology, 65, 47–55.CrossRefPubMedGoogle Scholar
  33. Fox, J., & Weisberg, S. (2011). An R companion to applied Rregression. Thousand Oaks: SAGE.Google Scholar
  34. Geissmann, T. (2000). Gibbon songs and human music from an evolutionary perspective. In N. L. Wallin, B. Merker, & S. Brown (Eds.), The origins of music (pp. 103–123). Cambridge: MIT Press.Google Scholar
  35. Geissmann, T. (2002). Duet-splitting and the evolution of gibbon songs. Biological Reviews of the Cambridge Philosophical Society, 77, 57–76.CrossRefPubMedGoogle Scholar
  36. Geissmann, T., & Nijman, V. (2006). Calling in wild silvery gibbons (Hylobates moloch) in java (Indonesia): Behavior, phylogeny, and conservation. American Journal of Primatology, 68, 1–19.CrossRefPubMedGoogle Scholar
  37. Geissmann, T., & Orgeldinger, M. (2000). The relationship between duet songs and pair bonds in siamangs, Hylobates syndactylus. Animal Behaviour, 60, 805–809.CrossRefPubMedGoogle Scholar
  38. Gittins, S. P. (1984). Territorial advertisement and defence in gibbons. In H. Preuschoft, D. J. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The lesser apes: Evolutionary and behavioural biology (pp. 420–424). Edinburgh: Edinburgh University Press.Google Scholar
  39. Gursky, S. (2000). Sociality in the spectral tarsier, Tarsius spectrum. American Journal of Primatology, 51, 89–101.CrossRefPubMedGoogle Scholar
  40. Haimoff, E. H. (1986). Convergence in the duetting of monogamous old world primates. Journal of Human Evolution, 15, 51–59.CrossRefGoogle Scholar
  41. Ham, S., Hedwig, D., Lappan, S., & Choe, J. C. (2016). Song functions in nonduetting gibbons: Evidence from playback experiments on Javan gibbons (Hylobates moloch). International Journal of Primatology, 37(2), 225–240.CrossRefGoogle Scholar
  42. Hothorn, T., & Hornik, K. (2013). exactRankTests: Exact distributions for rank and permutation tests. R package version, 0.8–027. http://CRAN.R-project.org/package=exactRankTests.
  43. Kappeler, M. (1984). Vocal bouts and territorial maintenance in the moloch gibbon. In H. Preuschoft, D. J. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The lesser apes: Evolutionary and behavioural biology (pp. 376–389). Edinburgh: Edinburgh University Press.Google Scholar
  44. Kim, S., Lappan, S., & Choe, J. C. (2011). Diet and ranging behavior of the endangered Javan gibbon (Hylobates moloch) in a submontane tropical rainforest. American Journal of Primatology, 73, 270–280.CrossRefPubMedGoogle Scholar
  45. Kim, S., Lappan, S., & Choe, J. C. (2012). Responses of Javan gibbon (Hylobates moloch) groups in submontane forest to monthly variation in food availability: Evidence for variation on a fine spatial scale. American Journal of Primatology, 74, 1154–1167.CrossRefPubMedGoogle Scholar
  46. Kinnaird, M. F., & O’Brien, T. G. (2005). Fast foods of the forest: The influence of figs on primates and hornbills across Wallace's line. In J. L. dew & J. P. Boubli (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 155–184). Dordrecht, the Netherlands: Springer.Google Scholar
  47. Kinzey, W. G., & Becker, M. (1983). Activity pattern of the masked titi monkey, Callicebus personatus. Primates, 24, 337–343.CrossRefGoogle Scholar
  48. Kinzey, W. G., & Robinson, J. G. (1983). Intergroup loud calls, range size, and spacing in Callicebus torquatus. American Journal of Physical Anthropology, 60, 539–544.CrossRefPubMedGoogle Scholar
  49. Leighton, D. R. (1987). Gibbons: Territoriality and monogamy. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 135–145). Chicago: University of Chicago Press.Google Scholar
  50. MacKinnon, J., & MacKinnon, K. (1980). The behavior of wild spectral tarsiers. International Journal of Primatology, 1, 361–379.CrossRefGoogle Scholar
  51. Malone, N., & Fuentes, A. (2009). The ecology and evolution of hylobatid communities: Causal and contextual factors underlying inter-and intraspecific variation. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 241–264). Developments in primatology progress and prospects. New York: Springer Science+Business media.Google Scholar
  52. McCullagh, P., & Nelder, J. A. (1989). Generalized linear models. New York: Chapman & Hall.CrossRefGoogle Scholar
  53. Mendez-Cardenas, M. G., & Zimmermann, E. (2009). Duetting: A mechanism to strengthen pair bonds in a dispersed pair-living primate (Lepilemur edwardsi)? American Journal of Physical Anthropology, 139, 523–532.CrossRefPubMedGoogle Scholar
  54. Mennill, D. J., & Vehrencamp, S. L. (2008). Context-dependent functions of avian duets revealed by microphone-array recordings and multispeaker playback. Current Biology, 18, 1314–1319.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Mitani, J. C. (1984). The behavioral regulation of monogamy in gibbons (Hylobates muelleri). Behavioral Ecology and Sociobiology, 15, 225–229.CrossRefGoogle Scholar
  56. Mitani, J. C. (1985a). Gibbon song duets and inter-group spacing. Behaviour, 92, 59–95.CrossRefGoogle Scholar
  57. Mitani, J. C. (1985b). Location-specific responses of gibbons (Hylobates muelleri) to male songs. Zeitschrift für Tierpsychologie, 70, 219–224.CrossRefGoogle Scholar
  58. Mitani, J. C. (1987). Territoriality and monogamy among agile gibbons (Hylobates agilis). Behavioral Ecology and Sociobiology, 20, 265–269.CrossRefGoogle Scholar
  59. Mitani, J. C., & Rodman, P. S. (1979). Territoriality: The relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behavioral Ecology and Sociobiology, 5, 241–251.CrossRefGoogle Scholar
  60. Müller, A. E., & Anzenberger, G. (2002). Duetting in the titi monkey Callicebus cupreus: Structure, pair specificity and development of duets. Folia Primatologica, 73, 104–115.CrossRefGoogle Scholar
  61. Pebesma, E. J., & Bivand, R. S. (2005). Classes and methods for spatial data in R. R News, 5, 9–13.Google Scholar
  62. R Development Core Team (2013). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org.Google Scholar
  63. Raemaekers, P. M., & Raemaekers, J. J. (1985). Long-range vocal interactions between groups of gibbons (Hylobates lar). Behaviour, 95, 26–44.CrossRefGoogle Scholar
  64. Rasoloharijaona, S., Randrianambinina, B., Braune, P., & Zimmermann, E. (2006). Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi). American Journal of Physical Anthropology, 129, 591–600.CrossRefPubMedGoogle Scholar
  65. Riley, E. P. (2005). The loud call of the Sulawesi Tonkean macaque, Macaca tonkeana. Tropical Biodiversity, 8, 199–209.Google Scholar
  66. Robinson, J. G. (1979). Vocal regulation of use of space by groups of titi monkeys Callicebus moloch. Behavioral Ecology and Sociobiology, 5, 1–15.CrossRefGoogle Scholar
  67. Ryan, M. J., & Kime, N. M. (2003). Selection on long-distance acoustic signals. In A. M. Simmons, A. N. Popper, & R. R. Fay (Eds.), Acoustic communication (pp. 225–274). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  68. Schielzeth, H., & Forstmeier, W. (2009). Conclusions beyond support: Overconfident estimates in mixed models. Behavioral Ecology, 20, 416–420.CrossRefPubMedGoogle Scholar
  69. Tenaza, R. R. (1976). Songs, choruses and countersinging of Kloss’ gibbons (Hylobates klossii) in Siberut Island, Indonesia. Zeitschrift für Tierpsychologie, 40, 37–52.CrossRefPubMedGoogle Scholar
  70. Waser, P. M. (1977). Individual recognition, intragroup cohesion and intergroup spacing: Evidence from sound playback to forest monkeys. Behaviour, 60, 28–74.CrossRefGoogle Scholar
  71. Whitten, A. J. (1982). The ecology of singing in Kloss gibbons (Hylobates klossii) on Siberut Island, Indonesia. International Journal of Primatology, 3, 33–51.CrossRefGoogle Scholar
  72. Wich, S. A., Assink, P. R., Becher, F., & Sterck, E. H. M. (2002). Playbacks of loud calls to wild Thomas langurs (primates; Presbytis thomasi): The effect of location. Behaviour, 139, 65–78.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Laboratory of Behavior and Ecology, Division of EcoScienceEwha Womans UniversitySeoulRepublic of Korea
  2. 2.Anthropology DepartmentAppalachian State UniversityBooneUSA
  3. 3.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  4. 4.Elephant Listening Project, Bioacoustics Research Program, Cornell Lab of OrnithologyCornell UniversityIthacaUSA
  5. 5.National Institute of EcologySeocheon, Chungcheongnam-doRepublic of Korea

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