Fast Foods of the Forest: The Influence of Figs on Primates and Hornbills Across Wallace’s Line

  • Margaret F. Kinnaird
  • Timothy G. O’brien


We examine relationships between fruit production and patterns of primate and hornbill densities on Sulawesi and Sumatra, Indonesia. Sumatra lies within the Asian biogeographic realm and has greater biodiversity while Sulawesi lies within Wallacea and has greater endemism. Phenological samples share 51% families, 29% genera but only 7% species. Generally, Sumatran trees are dispersed more often by small birds, bats and squirrels. Sulawesi has more wind-dispersed species. Fruiting is more seasonal on Sulawesi and is related to rainfall while Sumatran fruiting patterns show no relationship with rainfall. Sulawesi has larger trees, larger crops and smaller fruits. Average fruit production is five times higher on Sulawesi. On both islands, figs contribute disproportionately to fruit biomass. Hornbill and primate assemblages are less complex on Sulawesi but biomass of both groups is significantly higher. Hornbills and primates share 41 and 45% of diet species on Sumatra and Sulawesi, respectively. Wide-ranging hornbills on both islands decline in number or leave study areas when fig availability is low. Primates and hornbills (except Buceros rhinoceros) do not respond to the availability of other important diet species in the Anacardiaceae, Annonaceae, Meliaceae or Myristicaceae families. Fig availability influences resource defense and grouping patterns of primates and hornbills. We suggest that figs are a keystone guild due to their prime influence on abundance, distribution and behavior of large frugivores in Asia and Wallacea.

Key words

Figs frugivory hornbills Indonesia primates Sulawesi Sumatra 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anggraini, K., M.F. Kinnaird, and T.G. O’Brien. 2000. The effects of fruit availability and habitat disturbance on a Sumatran hornbill community. Bird Conservation International, 10, 189–202.CrossRefGoogle Scholar
  2. Bonaccorso, F. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum for Biological Science, 4, 359–408.Google Scholar
  3. Borges, R.M. 1993. Figs, Malabar giant squirrels and fruit shortages within two tropical Indian forests. Biotropica, 25, 183–190.Google Scholar
  4. Bronstein, J.L. and K. Hoffmann. 1987. Spatial and temporal variation in frugivory at a Neotropical fig, Ficus pertusa. Oikos, 49, 261–268.Google Scholar
  5. Buckland, S.T., Anderson, D.R., Burnham, K.P. and Laake, J.L. 1993. DISTANCE Sampling: Estimating Abundance of Biological Populations. Chapman and Hall, London.Google Scholar
  6. Burnham, K.P, D.R. Anderson, and J.L Laake. 1980. Estimation of density from line-transect sampling of biological populations. Wildlife Monographs, 72, 1–222.Google Scholar
  7. Cahill, A.J. and J.S. Walker. 2000. The effects of forest fire on the nesting success of the Red-knobbed Hornbill, Aceros cassidix. Bird Conservation International, 10, 109–114.CrossRefGoogle Scholar
  8. Conklin, N. L. and R. W. Wrangham. 1994. The value of figs to a hind-gut fermenting frugivore: a nutritional analysis. Biochemical Systematics and Ecology, 22, 137–151.CrossRefGoogle Scholar
  9. Curran, L.M. and M. Leighton. 2000. Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs, 70, 101–128.Google Scholar
  10. Curran, L.M., I. Caniago, G.D. Paoli, D. Astianti, M. Kusneti, M. Leighton, C.E. Nirarita, and H. Haeruman. 1999. Impact of El Nino and logging on canopy tree recruitment in Borneo. Science, 286, 2184–2188.PubMedCrossRefGoogle Scholar
  11. Ernest, S.K.M. and J.H. Brown. 2001. Delayed compensation for missing keystone species by colonization. Science, 292, 101–104.PubMedGoogle Scholar
  12. Food and Agriculture Organization. 1981. Management plan for the Bukit Barisan Selatan National Park, Lampung, Sumatra. FAO, Bogor.Google Scholar
  13. Fooden, J. 1969. Taxonomy and evolution of the monkeys of Celebes. Biblioteca Primatologica, 10, 1–148.Google Scholar
  14. Foster, R. 1982. The seasonal rhythm of fruit fall on Barro Colorado Island. In E.G. Leigh, Jr., A.S. Rand, and D.M. Windsor (Eds.). The ecology of a tropical forest: seasonal rhythms and long-term change, pp. 151–172. Smithsonian Institution Press, Washington, D.C.Google Scholar
  15. Groves, C.P. 1980. Speciation in Macaca: the view from Sulawesi. In D.G. Lindburg (Ed.). The Macaques: studies in ecology, behavior and evolution, pp. 84–124. Van Nostrand, New York.Google Scholar
  16. Guitier-Hion, A., and J.P. Michaloud. 1989. Figs: are they keystone resources for frugivorous vertebrates throughout the tropics? A test in Gabon. Ecology, 70, 1826–1833.Google Scholar
  17. Hadiprakarso, Y. 2000. Study of diet composition for hornbill species of the Bukit Barisan Selatan National Park, Lampung. Unpublished undergraduate thesis, Pakuan University, Bogor, Indonesia. 71 pp (in Indonesian).Google Scholar
  18. Hadiprakarsa, Y. and M.F. Kinnaird. in press. Foraging characteristics for an assemblage of four Sumatran hornbill species. Bird Conservation International.Google Scholar
  19. Hulbert, S.H. 1997. Functional importance vs keystoneness: reformulating some questions in theoretical biocenology. Australian Journal of Ecology, 22, 369–382.Google Scholar
  20. International Council for Bird Preservation. 1992. Putting biodiversity on the map: priority areas for global conservation. ICBP, Cambridge.Google Scholar
  21. International Union for Conservation of Nature. 1991. Atlas of tropical rainforests. Gland: IUCN Special Publication.Google Scholar
  22. Janzen, D.H. 1979. How to be a fig. Annuual Review of Ecology and Systematics, 10, 13–52.Google Scholar
  23. Johns, A. 1983. Ecological effects of selective logging in a West Malaysian rain forest. Unpubl. PhD disseration. Cambridge University, Cambridge.Google Scholar
  24. Kalko, E.J., E.A. Herre, and C.O. Handley. 1996. Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics. Journal of Biogeography, 23, 565–576.Google Scholar
  25. Kemp, A. 1995. The Hornbills. Oxford University Press, Oxford, United Kingdom.Google Scholar
  26. Kinnaird, M.F. 1998. Evidence for effective seed dispersal by the Sulawesi Red-knobbed Hornbill, Aceros cassidix. Biotropica, 30, 50–55.Google Scholar
  27. Kinnaird, M.F., Y. Hadiprakarsa, and P. Thiensongrusamee. 2003. Aerial jousting by Helmeted Hornbills: observations from Indonesia and Thailand. Ibis, 145, 506–508.CrossRefGoogle Scholar
  28. Kinnaird, M. F. and T.G. O’Brien. 1998. Ecological effects of wildfire on lowland rainforest in Sumatra. Conser. Biol., 12, 954–956.Google Scholar
  29. Kinnaird, M.F. and T.G. O’Brien. 1999. Breeding ecology of the Sulawesi Red-knobbed Hornbill, Aceros cassidix. Ibis, 141, 60–69.Google Scholar
  30. Kinnaird, M.F., T.G. O’Brien, and S. Suryadi. 1996. Population fluctuation in Sulawesi Red-knobbed Hornbills: tracking figs in space and time. Auk, 113, 431–440.Google Scholar
  31. Kinnaird, M.F., T.G. O’Brien and S. Suryadi. 1999. Importance of figs to Sulawesi’s imperiled wildlife. Tropical Biodiversity, 6, 5–18.Google Scholar
  32. Kinnaird, M.F., E.W. Sanderson, T.G. O’Brien, H.T. Wibisono and G. Woolmer. 2003. Deforestation trends in a tropical landscape and the implications for endangered large mammals. Conservation Biology, 17, 245–257.CrossRefGoogle Scholar
  33. Laake, J. L, S.T. Buckland, D.R. Anderson, and K. P. Burnham. 1993. DISTANCE user’s guide version 2.0. Colorado Cooperative Fish and Wildlife Research Unit, Colorado State Univ., Fort Collins, Colorado.Google Scholar
  34. Lambert, F. 1990. Avifaunal changes following selective logging of a north Bornean rainforest. Institute of Tropical Biology, University of Aberdeen, Scotland.Google Scholar
  35. Lambert, F. R. & Marshall, A.G. 1991. Keystone characteristics of birds-dispersed Ficus in a Malaysian lowland rain forest. Journal of Ecology, 79, 793–809.Google Scholar
  36. Lambert, F. R. 1989. Fig eating and seed dispersal by pigeons in a Malaysian lowland forest. Ibis, 131, 512–527.Google Scholar
  37. Lambert, F. R. 1991. The conservation of fig-eating birds in Malaysia. Biol. Conser., 58, 31–40.Google Scholar
  38. Leighton, M. 1982. Fruit Resources and Patterns of Feeding, Spacing and Grouping Among Sympatric Bornean Hornbills (Bucerotidae). Unpubl. Ph.D. dissertation, University of California, Davis.Google Scholar
  39. Leighton, M. 1993. Modelling dietary selectivity by Bornean orangutans: Evidence for integration of multiple criteria in fruit selection. Intrnational Journal of Primatology, 14, 257–313.Google Scholar
  40. Leighton, M. and D.R. Leighton. 1983. Vertebrate responses to fruiting seasonality within a Bornean rain forest. In S.L. Sutton, T.C. Whitmore, and A.C. Chadwick (Eds.). Tropical rain forest: ecology and management. Blackwell Scientific Publications, Cambridge, United Kingdom.Google Scholar
  41. Chivers, D.J. 1974. The Siamang in Malaya. Contributions to Primatology 4, 1–335.PubMedGoogle Scholar
  42. Meffe, G.K. and C.R. Carroll. 1994. Principles of Conservation Biology. Sinauer Assoc. Sunderland, MA.Google Scholar
  43. Milton, K. E.M. Windsor, S.W. Morrison, and M.A. Estribit. 1982. Fruiting phonologies of two Neotropical Ficus species. Ecology, 63, 752–762.Google Scholar
  44. Nurcahyo, A. 1999. A study of the daily behavior of siamang (Hylobates syndactylus) in Bukit Barisan National Park. Unpubl. undergraduate thesis. University of Gadjah Mada, Yogyakarta, Indonesia. (In Indonesian).Google Scholar
  45. O’Brien, T.G. 1997. Behavioural ecology of the North Sulawesi Tarictic Hornbill, Penelopides exarhatus exarhatus, during the breeding season. Ibis, 139, 97–101.Google Scholar
  46. O’Brien, T.G. and M.F. Kinnaird. 1994. Notes on the density and distribution of the endemic Sulawesi tarictic hornbill (Penelopides exarhatus exarhatus) in the Tangkoko-Dua Saudara Nature Reserve, North Sulawesi. Tropical Biodiversity, 2, 252–260.Google Scholar
  47. O’Brien, T.G. and M.F. Kinnaird. 1996. Birds and mammals of the Bukit Barisan Selatan National Park, Sumatra, Indonesia. Oryx, 30, 207–217.CrossRefGoogle Scholar
  48. O’Brien, T.G. and M.F. Kinnaird. 1996. Changing populations of birds and mammals in North Sulawesi. Oryx, 30, 150–156.Google Scholar
  49. O’Brien, T.G. and M.F. Kinnaird. 1997. Behavior, diet and movement patterns of the Sulawesi crested black macaque, Macaca nigra. International Journal of Primatology, 18, 321–351.Google Scholar
  50. O’Brien, T.G. and M.F. Kinnaird. 2000. Differential vulnerability of large birds and mammals to hunting in North Sulawesi, Indonesia and the outlook for the future. In J. G. Robinson and E. Bennett (Eds.). Hunting for Sustainability in the Tropics, pp. 199–213. Columbia University Press, New York.Google Scholar
  51. O’Brien, T.G., M.F. Kinnaird, E.S. Dierenfeld, N.L. Conklin-Brittain, R. Wrangham, and S. Silver. 1998. What’s so special about figs. Nature, 392, 668.Google Scholar
  52. O’Brien, T.G., M.F. Kinnaird, P. Jepson, and I. Setiawan. 1998. Effect of forest size and structure on the distribution of Sumba Wreathed Hornbills, Aceros everetti. In P. Poonswad (Ed.). Proceedings of the Second Asian Hornbill Workshop, pp. 209–218. BRPT, Bangkok, Thailand.Google Scholar
  53. O’Brien, T.G., M.F. Kinnaird, A. Nurcahyo, M. Prasetyaningrum and M. Iqbal. 2003b. Effects of ENSO-related wildfires on siamangs in a Sumatran rainforest. Animal Conservation, 6, 115–121.Google Scholar
  54. O’Brien, T.G., M.F. Kinnaird, H.T. Wibisono. 2003a. Crouching tigers, hidden prey: Sumatran tiger and prey populations in a tropical forest landscape. Animal Conservation, 6, 131–139.Google Scholar
  55. Payne, J., C.M. Francis, and K. Phillipps. 1985. A field guide to the mammals of Borneo. Sabah Society, Sabah, Malaysia.Google Scholar
  56. Peres, C. 2000. Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. Journal of Tropical Ecology, 16, 1–31.CrossRefGoogle Scholar
  57. Poonswaad, P., A. Tsuji and C. Ngarmpngsai. 1987. A comparative ecological study of four sympatric hornbills. Acta XIX Congressus Internationalis Ornithologi. 2, 2781–2791.Google Scholar
  58. Power, M.E. & L.S. Mills. 1995. The keystone cops meet in Hilo. TREE, 10, 182–184.Google Scholar
  59. Powers, M.E., D. Tilman, J.A. Estes, B.A. Menge, W.J. Bond, L. S. Mills, G. Daily, J.C. Castilla, J. Lubchenco, and R.T. Paine. 1996. Challenges in the quest for keystones. BioScience, 46, 609–620.Google Scholar
  60. Rombang, W. 1999. The ecology of mixed species foraging flocks in the Bukit Barisan Selatan National Park. Unpubl. undergraduate thesis, University of Indonesia, Depok, Indonesia (in Indonesian).Google Scholar
  61. Rowe, N. 1996. The Pictorial Guide to the Living Primates. Pogonias Press, East Hampton, New York.Google Scholar
  62. Rusmanto, M. 2002. The role of siamangs (Symphalangus syndactylus) in seed dispersal in the Bukit Barisan Selatan National Park, Sumatra. Unpubl. undergraduate thesis, University of Gadjah Mada, Yogyakarta, Indonesia. (In Indonesian).Google Scholar
  63. Shanahan, M. S. So, S.G. Compton and R. Corlett. 2001. Fig-eating by vertebrate frugivores: a global review. Biological Review, 76, 529–572.Google Scholar
  64. Sitompul, A.F., M.F. Kinnaird and T.G. O’Brien. In press. Size matters: the effects of forest fragmentation and resource availability the endemic sumba island hornbill. Bird Conservation International.Google Scholar
  65. Smuts, B., D.L. Cheney, R. M. Seyfarth, R.W. Wrangham, and T.T. Struhsaker. 1987. Primate Societies. University of Chicago Press, Chicago, Illinois.Google Scholar
  66. Sokal, R.R. and J.F. Rohlf 1981. Biometry: Second Edition. W.H. Freeman and Co. New York.Google Scholar
  67. Sterck, L. 1995. Females, foods and fights: a socioecological comparison of the sympatric Thomas langur and long-tailed macaque. Unpubl. dissertation, Universiteit Utrecht, Utrecht, Netherlands.Google Scholar
  68. Stahle, D.W. et al. 1998. Experimental dendroclimatic reconstruction of the Southern Oscillation. Bulletin of the American Meteorological Society, 70, 2137–2152.Google Scholar
  69. Sugardjito, J. I.J.A. Te Boekhorst, and J.A.R.A.M. Van Hooff. 1987. Ecological constraints of the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indoensia. International Journal of Primatology, 8, 17–41.Google Scholar
  70. Sugardjito, J. C.H. Southwick, J. Supriatna, A. Kohlhaas, S. Baker, J. Erwin, K. Froelich, and N. Lerche. 1989. Population survey of macaques in Northern Sulawesi. American Journal of Primatology, 18, 285–301.CrossRefGoogle Scholar
  71. Suryadi, S., M.F. Kinnaird, and T.G. O’Brien. 1999. Home ranges and daily movements of the Sulawesi Red-knobbed Hornbill during the non-breeding season. In P. Poonswad (Ed.). Proceedings of the Second Asian Hornbill Workshop, pp. 159–170. BRTP, Bangkok, Thailand.Google Scholar
  72. Suryadi, S., M.F. Kinnaird, T.G. O’Brien, and J. Supriatna. 1996. Time budget of the Sulawesi Red-Knobbed Hornbill during the non-breeding season at Tangkoko-DuaSudara Nature Reserve, North Sulawesi. Pp. 123–126. In: Kitchener, D.L. and A. Suyanto (Eds.), Proceedings of the First International Conference on Eastern Indonesian-Australian Vertebrate Fauna.Google Scholar
  73. Suryadi, S., M.F. Kinnaird, T.G. O’Brien, J. Supriatna, and S. Somadikarta. 1994. Food preferences of the Sulawesi Red-knobbed Hornbill during the non-breeding season. Tropical Biodiversity, 2, 377–384.Google Scholar
  74. Terborgh, J. 1983. Five New World Primates: a study in comparative ecology. Princeton University Press, Princeton, New Jersey.Google Scholar
  75. Terborgh, J. 1986. Keystone plant resources. In M. Soule (Ed.). Conservation biology: the science of scarcity and diversity, pp 330–344. Sinauer, Sunderland, Massachusetts.Google Scholar
  76. van Schaik, C. 1996. Strangling figs: their role in the forest. In C. van Schaik and J. Supriatna (Eds.). Leuser: a Sumatran Sanctuary, pp. 112–120. Yayasan Bina Sains Hayati Indonesia, Depok, Indonesia.Google Scholar
  77. Whitmore, T.C. 1984, The Tropical Rainforest of the Far East, Second Edition. Clarendon Press, Oxford.Google Scholar
  78. Whitten, T., S.J. Damanik, J. Anwar, and N. Hisyam. 1997. Ecology of Sumatra. Periplus Editions, Singapore.Google Scholar
  79. Wrangham, R.W., N.L. Conklin, G. Etot, J. Obus, K.D. Hunt, M.D. Hauser, and A.P. Clark. 1993. The value of figs to chimpanzees. International Journal of Primatology, 14, 243–255.CrossRefGoogle Scholar
  80. Wright, S.J. and C.P. van Schaik. 1994. Light and the phenology of tropical trees. American Naturalist, 143, 192–199.CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Margaret F. Kinnaird
    • 1
    • 2
  • Timothy G. O’brien
    • 1
    • 2
  1. 1.Wildlife Conservation Society-Asia ProgramBronx
  2. 2.National Center for Ecological Analysis and SynthesisSanta BarbaraUSA

Personalised recommendations