It is usually thought that Nomascus gabriellae is the only Nomascus sp. in Cambodia. We studied vocal diversity among different wild populations of Nomascus in Cambodia to assess their taxonomic relationships and to examine whether their vocal patterns correspond to forms previously described for Nomascus leucogenys siki and Nomascus gabriellae. We tape-recorded crested gibbon songs in southern Mondulkiri Province, in central Rattanakiri Province, and in 2 different districts of the Virachey National Park in northern Rattanakiri. We also tape-recorded typical songs of Nomascus leucogenys siki near the type locality of the taxon in the Bach Ma National Park in central Vietnam. We analyzed 40 song bouts from different gibbon groups, including 151 phrases of 33 females and 235 phrases of 39 males. Discriminant analyses revealed marked separation of the most southern songs (Mondulkiri) from those of all other localities. Vocal differences among the 3 gibbon populations in northeast Cambodia (Rattanakiri) are less pronounced; they do not differ more among each other than each of them differs from the northernmost sample from Bach Ma (Vietnam). Vocal characteristics of the study populations revealed no cline, and populations do not differ significantly in vocal variability. We conclude that Cambodian crested gibbons represent 2 distinct taxa: Those from southern Mondulkiri are Nomascus gabriellae, those from northeast Cambodia (Rattanakiri) closely correspond to the sample from Bach Ma (Vietnam) and, together with the latter, represent a different taxon. We provisionally assign them to Nomascus leucogenys siki because of the close geographic distance between Bach Ma and the type locality of the taxon. We postulate that a taxonal boundary exists between southern Mondulkiri and central Rattanakiri and discuss the possible factors that may have acted as distribution barriers.
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REFERENCES
Arcady, A. C. (1996). Phrase structure of wild chimpanzee pant hoots: Patterns of production and interpopulation variability. Am. J. Primatol. 39: 159–178.
Baker, M. C. (1974). Genetic structure of 2 populations of white-crowned sparrows with different song dialects. Condor 76: 351–356.
Baker, M. C. (1975). Song dialects and genetic differences in white-crowned sparrows (Zonotrichia leucophrys). Evolution 29: 226–241.
Baker, L. R., Geissmann, T., Nadler, T., Long, B., and Walston, J. (2002). Cambodia: Primate Field Guide. Phnom Penh, Cambodia: Fauna & Flora Cambodia (English and Khmer text).
Brockelman, W. Y., and Schilling, D. (1984). Inheritance of stereotyped gibbon calls. Nature 312: 634–636.
Charif, R. A., Mitchell, S., and Clark, C. W. (1995). Canary 1.2.4 user's manual. Cornell Laboratory of Ornithology, Ithaca, New York.
Creel, N., and Preuschoft, H. (1984). Systematics of the lesser apes: A quantitative taxonomic analysis of craniometric and other variables. In Preuschoft, H., Chivers, D. J., Brockelman, W. Y., and Creel, N. (eds), The Lesser Apes. Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh, pp. 562–613.
Dallmann, R., and Geissmann, T. (2001). Different levels of variability in the female song of wild silvery gibbons (Hylobates moloch). Behaviour 138: 629–648.
Dallmann, R., and Geissmann, T. (2006). Individual and geographical variability in the songs of wild silvery gibbons (Hylobates moloch) on Java, Indonesia. Am. J. Primatol 68: 1–19.
Delacour, J. (1951). La systematique des gibbons indochinois. Mammalia 15: 118–123 (French text).
Deputte, B. L. (1982). Duetting in male and female songs of the white-cheeked gibbon (Hylobates concolor leucogenys). In Snowdon, S. T., Brown, C. H., and Petersen, M. R. (eds), Primate Communication. Cambridge University Press, Cambridge, UK, pp. 67–93.
Fischer, J., Hammerschmidt, K., and Todt, D. (1998). Local variation in barbary macaque shrill barks. Anim. Behav. 56: 623–629.
Geissmann, T. (1984). Inheritance of song parameters in the gibbon song, analyzed in 2 hybrid gibbons (Hylobates pileatus x H. lar). Folia Primatol. 42: 216–235.
Geissmann, T. (1993). Evolution of Communication in Gibbons (Hylobatidae). Ph.D. thesis, Zürich University, Switzerland.
Geissmann, T. (1994). Systematik der Gibbons. Z. Kölner Zoo 37: 65–77 (German text, English abstract).
Geissmann, T. (1995). Gibbon systematics and species identification. Int. Zoo News 42: 467–501.
Geissmann, T. (2002a). Duet-splitting and the evolution of gibbon songs. Biol. Rev. 77: 57–76.
Geissmann, T. (2002b). Taxonomy and evolution of gibbons. Evol. Anthropol. 11 (Suppl. 1): 28–31.
Geissmann, T. (2003). Vergleichende Primatologie. Springer-Verlag, Berlin and Heidelberg.
Geissmann, T., Nguyen Xuan Dang, Lormée, N., and Momberg, F. (2000). Vietnam Primate Conservation Status Review 2000, Part 1: Gibbons (English edition). Fauna & Flora International, Indochina Programme Office, Hanoi.
Goustard, M. (1976). The vocalizations of Hylobates. In Rumbaugh, D. M. (ed), Gibbon and Siamang. (Karger, Basel, pp. 135–166.
Groves, C. P. (1972). Systematics and phylogeny of gibbons. In Rumbaugh, D. M. (ed), Gibbon and Siamang. (Karger, Basel, pp. 1–89.
Groves, C. P. (2001). Primate Taxonomy. Smithsonian Institution Press, Washington.
Groves, C. P. (2004). Taxonomy and biogeography of primates in Vietnam and neighbouring regions. In (Nadler, T., Streicher, U., and Ha Thang Long (eds.), Conservation of Primates in Vietnam. Frankfurt Zoological Society, Vietnam Primate Conservation Programme, and Endangered Primate Rescue Center, Cuc Phuong National Park, Hanoi, pp. 15–22.
Hafen, T. (1998). Dialekte bei Lemuren. Bioakustische, morphometrische und molekulargenetische Untersuchungen zur intraspezifischen Variabilität beim grauen Mausmaki (Microcebus murinus). Cuvillier Verlag, Göttingen.
Haimoff, E. H. (1983). Gibbon Songs: An Acoustical, Organizational, and Behavioural Analysis. Ph.D. Thesis, Cambridge University, UK.
Haimoff, E. H. (1984a). Acoustic and organizational features of gibbon songs. In Preuschoft, H., Chivers, D. J., Brockelman, W. Y., and Creel, N. (eds), The Lesser Apes. Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh, pp. 333–353.
Haimoff, E. H. (1984b). The organization of song in the Hainan black gibbon (Hylobates concolor hainanus). Primates 25: 225–235.
Haimoff, E. H., Chivers, D. J., Gittins, S. P., and Whitten, A. J. (1982). A phylogeny of gibbons (Hylobates spp.) based on morphological and behavioural characters. Folia Primatol. 39: 213–237.
Haimoff, E. H., Gittins, S. P., Whitten, A. J., and Chivers, D. J. (1984). A phylogeny and classification of gibbons based on morphology and ethology. In Preuschoft, H., Chivers, D. J., Brockelman, W. Y., and Creel, N. (eds), The Lesser Apes. Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh, pp. 614–632.
Legris, P., and Blasco, F. (1971). Cambodge: Carte internationale du tapis vegetal et des conditions écologique. Institut français, Pondichéry.
Maeda, T., and Masataka, N. (1987). Locale-specific vocal behaviour of the tamarin (Saguinus l. labiatus). Ethology 7: 525–530.
Manly, B. F. J. (1994). Multivariate Statistical Methods: A Primer, 2nd edition. Chapman & Hall/CRC, Boca Raton and London.
Marshall, J. T., and Marshall, E. R. (1976). Gibbons and their territorial songs. Science 193: 235–237.
Marshall, J. T., and Sugardjito, J. (1986). Gibbon systematics. In Swindler, D. R., and Erwin, J. (eds), Comparative Primate Biology, Vol. 1: Systematics, Evolution, and Anatomy. Alan R. Liss, New York, pp. 137–185.
Marshall, J. T., Sugardjito, J., and Markaya, M. (1984). Gibbons of the lar group: Relationships based on voice. In Preuschoft, H., Chivers, D. J., Brockelman, W. Y., and Creel, N. (eds). The Lesser Apes. Evolutionary and Behavioural Biology. (eds). Edinburgh University Press, Edinburgh, pp. 533–541.
Mather, R. (1992). A Field Study of Hybrid Gibbons in Central Kalimantan, Indonesia. Ph.D. Thesis, Cambridge University, UK.
Mitani, J. C., Hasegawa, T., Gros-Louis, J., Marler, P., and Byrne, R. W. (1992). Dialects in wild chimpanzees? Am. J. Primatol. 27: 233–243.
Mitani, J. C., Hunley, K. L., and Murdoch, M. E. (1999). Geographic variation in the calls of wild chimpanzees: A reassessment. Am. J. Primatol. 47: 133–151.
Morris, R. C. (1943). Rivers as barriers to the distribution of gibbons. J. Bombay Nat. Hist. Soc. 43: 656.
Norusis, M. J. (1994). SPSS Professional Statistics 6.1. SPSS Inc., Chicago.
Parsons, R. E. (1940). Rivers as barriers to the distribution of gibbons. J. Bombay Nat. Hist. Soc. 42: 434.
Parsons, R. E. (1941). Rivers as barriers to the distribution of gibbons. J. Bombay Nat. Hist. Soc. 42: 926.
Ralin, D. B. (1977). Evolutionary aspects of mating call variation in a diploid-tetraploid species complex of treefrogs (Anura). Evolution 31: 721–736.
Roos, C. (2004). Molecular evolution and systematics of Vietnamese primates. In Nadler, T., Streicher, U., and Ha Thang Long (eds). Conservation of primates in Vietnam Frankfurt Zoological Society, Vietnam Primate Conservation Programme, and Endangered Primate Rescue Center, Cuc Phuong National Park, Hanoi, pp. 23–28.
Roos, C., and Geissmann, T. (2001). Molecular phylogeny of the major hylobatid devisions. Mol. Phylogen. Evol. 19: 486–494.
Schilling, D. (1984a). Gibbons in European zoos, with notes on the identification of subspecies of concolor gibbon. In Preuschoft, H., Chivers, D. J., Brockelman, W. Y., and Creel, (eds), The Lesser Apes. Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh, pp. 51–60.
Schilling, D. (1984b). Song bouts and duetting in the concolor gibbon. In Preuschoft, H., Chivers, D. J., Brockelman, W. Y., and Creel, N. (eds). The Lesser Apes. Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh, pp. 390–403.
Siegel, S., and Castellan, N. J. Jr., (1988). Nonparametric Statistics for the Behavioral Sciences, 2nd ed. McGraw-Hill, Singapore.
Smith, J. D. (ed.). (2001). Biodiversity, the Life of Cambodia—Cambodian Biodiversity Status Report 2001. Cambodian Biodiversity Enabling Activity, Phnom Penh, Cambodia.
Sneath, P. H., and Sokal, R. R. (1973). Numerical Taxonomy. Principles and Practice of Numerical Classification. W. H. Freeman, San Francisco.
Srikosamatara, S., and Doungkhae, S. (1982). Dry dipterocarp forest as a barrier to gibbon dispersal: A survey in Phu Phan National Park, northeast Thailand. Nat. Hist. Bull. Siam Soc. 30: 25–32.
Tallents, L., Geissmann, T., Trinh Dinh Hoang, and La Quang Trung (2001). Survey for Crested Gibbons (genus Nomascus) in Bach Ma National Park, Viet Nam, April 2001. Fauna & Flora International, Indochina Programme Office, Hanoi.
Tenaza, R. (1985). Songs of hybrid gibbons (Hylobates lar × H. muelleri). Am. J. Primatol. 8: 249–253.
Thorpe, W. H. (1961). Bird-Song. The Biology of Vocal Communication and Expression in Birds. (Cambridge monographs in experimental biology, No. 12). Cambridge University Press, Cambridge.
ACKNOWLEDGMENTS
Several people kindly made their tape-recordings of wild crested gibbons available to T. Geissmann that we either included in the analysis or that stimulated our study: Peter Davidson, Frédéric Goes, Trinh Dinh Hoang, Tim Redford, Craig Robson, and La Quang Trung. Richard Paley (FFI, Cambodia Programme Co-ordinator), Frank Momberg (FFI, SE-Asia Programme Co-ordinator), Ben Rawson, Tom Clements (Technical Advisor, WCS Cambodia), Andrew Maxwell (Technical Advisor, WWF Cambodia), and Carl Traeholt (Technical Advisor, FFI Cambodia) generously facilitated our field work. We thank Fauna and Flora International (FFI) and Wildlife Conservation Fund (WCS) for providing logistic support during some of our field trips. We thank Ben Rawson, Meng Hor, Roth Bunthoeun, Chea Virak, Mon Samuth, Sok Vuthin, Thak Sophat, Kam Pon, Kuntejae, So Kun, Ka Ian, Sud Bonme, La Quang Trung, Trinh Dinh Hoang, and Lucy Tallents for assistance in the field. The Biodiversity and Protected Areas Management Project (BPAMP) facilitated the field trips to Virachey National Park. We acknowledge the support of Klaus Schmitt (Senior Project Advisor) and all staff members of the BPAMP. Koy Sokha, director of Virachey National Park, and Im Sokhon (Ministry of Environment Lomphat District) kindly gave permission to undertake field work in Virachey National Park and Lomphat Wildlife Sanctuary, respectively. We are grateful to Alexandra Müller and 2 anonymous reviewers for constructive comments on earlier versions of this manuscript and to Dominic Schuhmacher for helpful advise in multivariate analysis. R. Konrad received financial support from the A. H. Schultz Foundation and the SANW (Schweizerische Akademie der Naturwissenschaften), and T. Geissmann from the FFI bureaus in Phnom Penh/Cambodia and Hanoi/Vietnam.
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APPENDIX: LIST OF VOCAL VARIABLES
APPENDIX: LIST OF VOCAL VARIABLES
Multimodulated Phrase of the Male
Overall Variables: 1. Number of notes, 2. Duration of entire male phrase (s).
Note 1: 3. Duration of first note (s), 4. Maximum duration (s), 5. Minimum duration (s), 6. Duration of horizontal part (s), 7. Rel. duration of horizontal part (%), 8. Duration of trough part (s), 9. Rel. duration of trough part (%), 10. Start frequency (Hz), 11. Maximum frequency of horizontal part (Hz), 12. Maximum frequency (Hz), 13. Minimum frequency (Hz), 14. Frequency range (Hz), 15. Frequency halfway (Hz), 16. Frequency range to halfway point (Hz), 17. Rel. frequency range to halfway point (%), 18. Duration to maximum bend (s), 19. Rel. duration to maximum bend (%), 20. Frequency at maximum bend (Hz), 21. Duration to peak intensity (s), 22. Rel. duration to peak intensity (%), 23. Frequency at peak intensity (Hz), 24. Frequency range to peak intensity (Hz), 25. Rel. frequency range to peak intensity (%).
Note 2: 26. Duration of second note (s), 27. Duration of initial part (s), 28. Rel. duration of initial part (%), 29. Duration of roll part (s), 30. Rel. duration of roll part (%), 31. Number of rolls, 32. Number of “long” troughs in roll part, 33. Duration of first roll in roll part (s), 34. Duration of terminal part (s), 35. Rel. duration of terminal part (%), 36. Start frequency (Hz), 37. Maximum frequency (Hz), 38. Minimum frequency (Hz), 39. Frequency range (Hz), 40. Minimum frequency of initial part (Hz), 41. Frequency range of initial part (Hz), 42. Frequency at first trough in roll part (Hz), 43. Frequency range to first trough in roll part (Hz), 44. Frequency at last trough in roll part (Hz), 45. Frequency range to last trough in roll part (Hz), 46. Frequency range to lowest trough in roll part (Hz), 47. Minimum frequency of terminal part (Hz).
Note 3: 48. Duration of third note (s), 49. Number of rolls, 50. Start frequency (Hz), 51. Maximum frequency (Hz), 52. Minimum frequency (Hz), 53. Frequency range (Hz), 54. Internotes frequency range (Hz).
Note 4: 55. Duration of fourth note (s), 56. Start frequency (Hz), 57. Maximum frequency (Hz), 58. Minimum frequency (Hz), 59. Frequency range (Hz).
Great Call Phrase of the Female
Overall Variables: 60. Duration of entire great call (s), 61. Number of notes, 62. Range of start frequencies (Hz), 63. Maximum start frequency (Hz), 64. Number of oo notes, 65. Duration of oo phase (s), 66. Rel. duration of oo phase (%), 67. Number of bark notes, 68. Duration of bark phase (s), 69. Rel. duration of bark-phase (%), 70. Rel. duration of twitter part (%), 71. Duration of inter-phrase interval (s).
Single-note variables: 72. Duration of first oo note (s), 73. Frequency range of first oo note (Hz), 74. Duration of second oo note (s), 75. Frequency range of second oo note (Hz), 76. Duration of first bark note (s), 77. Frequency range of first bark note (Hz), 78. Duration of last bark note (s).
Successive notes variables: 79. First inter-note interval (s), 80. Second inter-note interval (s), 81. Last inter-note interval (s), 82. First start frequency range (Hz), 83. Second start frequency range (Hz), 84. Last start frequency range (Hz).
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Konrad, R., Geissmann, T. Vocal Diversity and Taxonomy of Nomascus in Cambodia. Int J Primatol 27, 713–745 (2006). https://doi.org/10.1007/s10764-006-9042-3
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DOI: https://doi.org/10.1007/s10764-006-9042-3