Abstract
Gibbons are among the best-studied Asian primates, but few studies address their demography and life history strategies. We used annual censuses to study the demography of agile gibbons (Hylobates agilis) between 1998 and 2009 in rain forests of Bukit Barisan Selatan National Park, Indonesia. The population declined from 22 individuals (9 groups) to 14 individuals (5 groups) over the 12 yr of study. Infant survival to the juvenile age class was 33.3%, and 16.7% of infants survived to the subadult age class. The interbirth interval was 3.83 ± 1.15 yr and birth rate was 0.22–0.28 infants female–1 yr–1. Two groups colonized the study area but subsequently disappeared. We documented 7 immigrations, 17 disappearances, and ≥10 transients in the population. Compared to lar gibbons (Hylobates lar) and Bornean white-bearded gibbons (Hylobates albibarbis), Way Canguk’s agile gibbon population is characterized by slow reproduction, low survival, and high group turnover. We hypothesize that, although the habitat is high in fruit resources, agile gibbons may be displaced or excluded from the best fruit resources by larger and more numerous competitors, incurring costs of decreased opportunities to forage and increased travel, and leading to higher mortality for young agile gibbons. The reproductive potential of this agile gibbon population is insufficient to compensate for high mortality, and the population is unlikely to persist without immigration from outside the area. Given the agile gibbons’ endangered status and limited capacity to respond demographically to change, it is likely that intensive management interventions will be required to conserve this species.
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References
Altmann, J. (1980). Baboon mothers and infants. Cambridge: Harvard University Press.
Bartlett, T. Q. (2007). The hylobatidae small apes of Asia. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 274–289). Oxford: Oxford University Press.
Borries, C., Savini, T., & Koenig, A. (2010). Social monogamy and the threat of infanticide in larger mammals. Behavioral Ecology and Sociobiology. doi:10.1007/s00265-010-1070-5.
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.
Butynski, T. T. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-density subpopulations. Ecological Monographs, 60, 1–26.
Chapman, C. A., Gillespie, T. R., & Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology, 14, 134–144.
Chivers, D. J. (1974). The siamang in Malaya: a field study of a primate in a tropical rain forest. In H. Kuhn, W. P. Luckett, C. R. Noback, A. H. Schultz, D. Starck, & F. S. Szalay (Eds.), Contributions to primatology (Vol. 4, pp. 1–335). Basel: S. Karger.
Chivers, D. J., & Raemaekers, J. J. (1980). Long-term changes in behavior. In D. Chivers (Ed.), Malayan Forest primates: Ten years’ study in tropical rain forest (pp. 209–258). New York: Plenum Press.
Collias, N., & Southwick, C. (1952). A field study of population density and social organization in howling monkeys. Proceedings of the American Philosophical Society, 96, 143–156.
Elder, A. A. (2010). Sleeping strategies of three sympatric primate species at Way Canguk, Sumatra. In American Society of Primatology Conference (Abstract) Elder abstract #113, Location Louisville, KY on 16–19 June 2010. http://www.asp.org/asp2010/abstractDisplay.cfm?abstractID=2840&confEventID=3079
Geissmann, T. (1991). Reassessment of age of sexual maturity in gibbons (Hylobates ssp.). American Journal of Primatology, 23, 11–22.
Geissman, T. (2007). Status reassessment of the gibbons: results of the Asian primate Red List workshop 2006. Gibbon Journal, 1, 5–15.
Gillespie, T. R., Nunn, C. L., & Leendertz, F. H. (2008). Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. Yearbook of Physical Anthropology, 51, 53–69.
Hopkins, M. E., & Nunn, C. L. (2007). A global gap analysis of infectious agents in wild primates. Diversity and Distributions, 13, 561–572.
IUCN (2010). IUCN Red list of threatened species. Version 2010.3. Retrieved from www.iucnredlist.org.
Janson, C. H., & van Schaik, C. P. (1993). Ecological risk aversion in juvenile primates: slow and steady wins the race. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development and behavior (pp. 57–74). Oxford: Oxford University Press.
Kinnaird, M. F., & O’Brien, T. G. (1998). Ecological effects of wildfire on lowland rainforest in Sumatra. Conservation Biology, 12, 954–956.
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 L. Dew & J. P. Boubli (Eds.), Fruits and frugivores: The search for strong interactors (pp. 155–184). Dordrecht: Springer.
Kinnaird, M. F., Sanderson, E. W., O’Brien, T. G., Wibisono, H. T., & Woolmer, G. (2003). Deforestation trends in a tropical landscape and implications for forest mammals. Conservation Biology, 17, 245–257.
Lappan, S. (2005). Biparental care and male reproductive strategies in siamangs (Symphalangus syndactylus) in southern Sumatra. Ph.D. thesis, New York University.
Lappan, S. (2007). Patterns of dispersal in Sumatran siamangs (Symphalangus syndactylus): preliminary mtDNA evidence suggests more frequent male than female dispersal to adjacent groups. American Journal of Primatology, 69, 692–698.
Leighton, D. (1987). Gibbons: territoriality and monogamy. In B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham, & T. Struhsaker (Eds.), Primate societies (pp. 135–145). Chicago: University of Chicago Press.
Marshall, A. J. (2004). The population ecology of gibbons and leaf monkeys across a gradient of Bornean forest types. Ph.D. thesis, Harvard University.
Marshall, A. J. (2009). Are montane forests demographic sinks for Bornean white-bearded gibbons Hylobates albibarbis? Biotropica, 41, 257–267.
Marshall, A. J., & Leighton, M. (2006). How does food availability limit the population density of agile gibbons? In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology of the apes (pp. 313–335). Cambridge: Cambridge University Press.
Marshall, A. J., Cannon, C. H., & Leighton, M. (2009). Competition and niche overlap between gibbons (Hylobates albibarbis) and other frugivorous vertebrates in Gunung Palung National Park, West Kalimantan, Indonesia. In S. Lappan & D. Whittaker (Eds.), The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology (pp. 161–188). Developments in Primatology: Progress and Prospects. New York: Springer.
May, R. M., & Anderson, R. M. (1979). Population biology of infectious disease: Part II. Nature, 280, 455–461.
Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler (Alouatta palliata) population in Panama. Journal of Zoology, 239, 39–63.
Mitani, J. (1987). Territoriality and monogamy among agile gibbons (Hylobates agilis). Behavioral Ecology and Sociobiology, 20, 265–269.
Mitani, J. (1990). Demography of agile gibbons (Hylobates agilis). International Journal of Primatology, 11, 411–424.
Morino, L. (2010). Clouded leopard predation on a wild juvenile siamang. Folia Primatologica, 81, 362–368.
Nunn, C. L., & Altizer, S. M. (2006). Infectious diseases in primates: Behavior, ecology, and evolution. Oxford: Oxford University Press.
O’Brien, T. G., & Kinnaird, M. F. (2003). Caffeine and conservation. Science, 300, 587.
O’Brien, T. G., Kinnaird, M. F., Nurcahya, A., Prasetyaningrum, M., & Iqbal, M. (2003). Fire, demography, and the persistence of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest. Animal Conservation, 6, 115–121.
O’Brien, T. G., Kinnaird, M. F., Nurcahya, A., Iqbal, M., & Rusmanto, M. (2004). Abundance and distribution of sympatric gibbons in a threatened Sumatran rainforest. International Journal of Primatology, 25, 267–284.
Palombit, R. A. (1992). Pair bonds and monogamy in wild siamang (Hylobates syndactylus) and white-handed gibbon (Hylobates lar) in Northern Sumatra. Ph.D. thesis, University of California, Davis.
Palombit, R. A. (1995). Longitudinal patterns of reproduction in wild female siamang (Hylobates syndactylus) and white-handed gibbon (Hylobates lar). International Journal of Primatology, 16, 739–760.
Pulliam, H. R. (1988). Sources, sinks and population regulation. American Naturalist, 132, 652–661.
Pulliam, H. R. (1996). Sources and sinks: Empirical evidence and population consequences. In O. E. J. Rhodes, R. K. Chesser, & M. H. Smith (Eds.), Population dynamics in ecological space and time (pp. 45–69). Chicago: University of Chicago Press.
Rabinowitz, A. (1989). The density and behavior of large cats in a dry tropical forest mosaic in Huai Kha Khaeng Wildlife Sanctuary, Thailand. Natural History Bulletin of the Siam Society, 37, 235–251.
Raemaekers, J. J. (1979). Ecology of sympatric gibbons. Folia Primatologica, 31, 227–245.
Raemaekers, J. J., & Chivers, D. J. (1980). Socio-ecology of Malayan forest primates. In D. J. Chivers (Ed.), Malayan Forest primates: Ten years’ study in tropical rain forest (pp. 279–316). New York: Plenum Press.
Reichard, U. H. (1998). Sleeping sites, sleeping places, and pre-sleep behavior of gibbons. American Journal of Primatology, 46, 35–62.
Reichard, U. H. (2003). Social monogamy in gibbons: The male perspective. In U. H. Reichard & C. Boesch (Eds.), Monogamy: Mating strategies and partnerships in birds, humans and other mammals (pp. 3–25). Cambridge: Cambridge University Press.
Reichard, U. H., & Barelli, C. (2008). Life history and reproductive strategies of Khao Yai Hylobates lar: Implications for social evolution in apes. International Journal of Primatology, 29, 823–844.
Rudran, R., & Fernandez-Duque, E. (2003). Demographic changes over thirty years in a red howler population in Venezuela. International Journal of Primatology, 24, 925–948.
Savini, T., Boesch, C., & Reichard, U. H. (2008). Home-range characteristics and the influence of seasonality on female reproduction in white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand. American Journal of Physical Anthropology, 135, 1–12.
Savini, T., Boesch, C., & Reichard, U. H. (2009). Varying ecological quality influences the probability of polyandry in white-handed gibbons (Hylobates lar) in Thailand. Biotropica, 41, 501–513.
Setchell, J. M., & Lee, P. C. (2004). Development and sexual selection in primates. In P. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: Causes, mechanisms and consequences (pp. 175–195). Cambrudge: Cambridge University Press.
Sokal, R. R., & Rolf, F. J. (1995). Biometry (3rd ed.). New York: Freeman.
Uhde, N. L., & Sommer, V. (2002). Antipredatory behavior in gibbons (Hylobates lar, Khao Yai/Thailand). In L. M. Miller (Ed.), Eat or be eaten: Predator sensitive foraging among nonhuman primates (pp. 268–291). Cambridge: Cambridge University Press.
van Schaik, C. P., & van Hooff, J. A. R. A. M. (1983). On the ultimate causes of primate social systems. Behaviour, 85, 91–117.
van Schaik, C. P., Preuschoft, S., & Watts, D. P. (2004). Great ape social systems. In A. E. Russon & D. R. Begun (Eds.), The evolution of thought: Evolutionary origins of great ape intelligence (pp. 190–209). Cambridge: Cambridge University Press.
Walsh, T. D., Abernethy, K. A., Bermejo, M., Beyers, R., de Wachter, P., Akou, M. E., et al. (2003). Catastrophic ape decline in western equatorial Africa. Nature, 422, 611–614.
Whittaker, D. J., & Lappan, S. (2009). The diversity of small apes and the importance of population-level studies. In S. Lappan & D. J. Whittaker (Eds.), The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology (pp. 3–10). Development in Primatology: Progress and Prospects. New York: Springer.
Yanuar, A. (2009). The population distribution and abundance of siamangs (Symphalangus syndactylus) and Agile gobbons (Hylobates agilis) in West Central Sumatra, Indonesia. In S. Lappan & D. J. Whittaker (Eds), The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology (pp. 453–465). Development in Primatology: Progress and Prospects. New York: Springer.
Yanuar, A., & Sugardjito, J. (1993). Population survey of primates in Way Kambas National Park, Sumatra, Indonesia. Tigerpaper, 20, 30–36.
Acknowledgments
This research is a collaborative effort by the Wildlife Conservation Society and the Indonesian Ministry of Forestry, Directorate General for Nature Conservation (PHKA). Our research was funded by the Wildlife Conservation Society, the U.S. Fish and Wildlife Service Great Apes Conservation Fund (grant no. 98210-1-G084), the Disney Conservation Fund, and E. McBean. We thank A. Dwiyahreni, M. Iqbal, A. Nurcahyo, M. Nusawalo, M. Prasetyaningrum, M. Rusmanto, Sunarto, D. Suyadi, N. Winarni, Aris, Bawk, Tegu, and Wariono for assistance with data collection over the years. A. Elder provided valuable insights into the interspecific relationships of Way Canguk primates, L. Morino provided details of clouded leopard predation on a juvenile siamang at Way Canguk, and R Palombit and C. van Schaik provided information on the relationships of lar gibbons and siamangs in northern Sumatra. Our manuscript was greatly improved by the comments of J. Setchell and 2 anonymous reviewers.
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O’Brien, T.G., Kinnaird, M.F. Demography of Agile Gibbons (Hylobates agilis) in a Lowland Tropical Rain Forest of Southern Sumatra, Indonesia: Problems in Paradise. Int J Primatol 32, 1203–1217 (2011). https://doi.org/10.1007/s10764-011-9537-4
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DOI: https://doi.org/10.1007/s10764-011-9537-4