Plant Ecology

, Volume 153, Issue 1–2, pp 121–132 | Cite as

Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different?

  • Mike Shanahan
  • Stephen G. Compton


Fig trees (Ficus spp; Moraceae) are a common constituent of many tropical forests, where they produce figs that are eaten by a wide range of bird and mammal species. In our Bornean field site six Ficus seed dispersal guilds can be recognised, differentially attracting subsets of the frugivore community. Guild membership appears to be determined by figs' size, colour, crop size and height above ground, and frugivores' size, sensory and locomotory physiology and foraging height. Vertical stratification therefore appears to be an important determinant of fig and frugivore partitioning. The guild structure observed is discussed with respect to implications for seed dispersal and the differences between the canopy and understorey. Regarding figs eaten primarily by birds, larger fruit and crops can be found in the canopy where they are exposed to larger assemblages of potential frugivores than those presented in the understorey.

Borneo Ficus Frugivory Fruit design characters Keystone resource Seed dispersal guilds 


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  1. Ashton, P. S. & Hall, P. 1992. Comparisons of structure among mixed dipterocarp forests of north-western Borneo. J. Ecol. 80: 459–481.Google Scholar
  2. Baker, J. R. & Baker, Z. 1936. The seasons in a tropical rain forests. Part 3. The fruit bats. J. Linn. Soc. Lond. (Zool). 40: 123–141.Google Scholar
  3. Berg, C. C. 1990. Classification and distribution of Ficus. Exper. 45: 605–611.Google Scholar
  4. Borges, R. M. 1993. Figs, Malabar giant squirrels and fruit shortages within two tropical Indian forests. Biotropica 25: 183–190.Google Scholar
  5. Chivers, D. J (ed.) 1980. Malayan Forest Primates. Ten years study in tropical rain forest. Plenum Press, New York.Google Scholar
  6. Corlett, R. T. 1984. The phenology of Ficus benjamina and Ficus microcarpa in Singapore. J. Sing. Nat. Acad. Sci. 13: 30–31.Google Scholar
  7. Corner, E. J. H. 1965. Check list of Ficus in Asia and Australasia, with keys to identification. Gard. Bull. (Singapore) 21: 1–186.Google Scholar
  8. Corner, E. J. H. 1988. Wayside Trees of Malaya. United Selangor Press, Kuala Lumpur, Malaysia.Google Scholar
  9. Cowles, G. S. & Goodwin, D. 1959. Seed digestion by the fruit eating pigeon Treron. Ibis 101: 253–254.Google Scholar
  10. Crome, F. H. J. 1975. The ecology of fruit pigeons in tropical north Queensland. Austr. Wildl. Res. 2: 155–185.Google Scholar
  11. Diamond, J. M. 1973. Distributional ecology of New Guinea birds. Science 179: 767.Google Scholar
  12. Fischer, K. E. & Chapman, C. A. 1993. Frugivores and fruit syndromes: differences in patterns at the genus and species level. Oikos 66: 472–482.Google Scholar
  13. Fleming, T. H. 1979. Do tropical frugivores compete for food? Amer. Zool. 19: 1157–1172.Google Scholar
  14. Fleming, T. H., Breitwisch, R. & Whitesides, G. H. 1987. Patterns of tropical vertebrate frugivore foraging diversity. Annu. Rev. Ecol. Syst. 18: 91–109.Google Scholar
  15. Francis, C. M. 1990. Trophic structure of bat communities in the understorey of lowland dipterocarp rain forest in Malaysia. J. Trop. Ecol. 6: 421–431.Google Scholar
  16. Francis, C. M. 1994. Vertical stratification of fruit bats (Pteropodidae) in lowland dipterocarp rain forest in Malaysia. J. Trop. Ecol. 10: 523–530.Google Scholar
  17. Gautier-Hion, A., Hecketsweiler, P., Sourd, C., Tiollay, J. M., Rousilhon, C., Quris, R., Decoux, J. P., Dubost, G., Duplantier, J. M., Erard, C., Emmons, L., Feer, F. & Moungazi, A. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecol. 65: 324–337.Google Scholar
  18. Gautier-Hion, A. & Michaloud, P. 1989. Figs: are they keystone resources for vertebrates throughout the tropics? A test in Gabon. Ecology 70: 1826–1833.Google Scholar
  19. Harrison, J. L. 1962. The distribution of feeding habits among animals in a tropical rain forest. J. Anim. Ecol. 31: 53–63.Google Scholar
  20. Harrison, R.D. 1998. Guide to the Ficus flora of Lambir Hills. National Park, Sarawak. Unpublished report. 34 pp.Google Scholar
  21. Hartwig, H.-G. 1993. The central nervous system of birds: A study of functional morphology. Pp. 1–119. In:. Farner, D. S., King, J. R. & Parkes, K. C. (eds), Avian biology, Vol IX. Academic Press, London.Google Scholar
  22. Heydon, M. J. & Bulloh, P. 1997. Mousedeer densities in a tropical rain forest: the impact of selective logging. J. App. Ecol. 34: 484–496.Google Scholar
  23. Hill. M. O. 1979. DECORANA-a Fortran program for detrended correspondence analysis and reciprocal averaging. Cornell University, Ithaca, New York.Google Scholar
  24. Hnatiuk, S. H. 1978. Plant dispersal by the Aldabran giant tortoise Geochelone gigantea (Schweigger). Oecologia 36: 345–350.Google Scholar
  25. Inoue, T. & Hamid, A. A. (eds.). 1994. Plant reproductive systems and animal seasonal dynamics: Long-term study of dipterocarp forests in Sarawak. Center for Ecological Research, Kyoto University, Japan.Google Scholar
  26. Inoue, T., Yumoto, T., Hamid, A. A., Lee, H. S. & Ogino, K. 1995. Construction of a canopy observation system in a tropical rain forest of Sarawak. Selbyana 16: 24–35.Google Scholar
  27. Janson C. H. 1983. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219: 187–189.Google Scholar
  28. Janson, C. H., Stiles, E. W., & White, D. W. 1986. Selection on plant fruiting traits by brown capuchin monkeys: a multivariate approach. Pp. 82–92. In: Fleming, T. H. & Estrada, A. (eds), Frugivores and seed dispersal. Junk, Dordrecht.Google Scholar
  29. Janzen, D. H. 1971. Seed predation by animals. Annu. Rev. Ecol. Syst. 2: 465–492.Google Scholar
  30. Janzen, D. H. 1979. How to be a fig. Annu. Rev. Ecol. Syst. 10: 13–51.Google Scholar
  31. Janzen, D. H. 1985. On ecological fitting. Oikos 45: 308–310.Google Scholar
  32. Kalko, E. K. V., Herre, E. A. & Handley, C. O. J. 1996. Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics. J. Biogeogr. 23: 565–576.Google Scholar
  33. Kochummen, K. M. 1983. Moraceae. Pp. 135–162. In: Ng. F. S. P. (ed), Tree Flora of Malaya, Vol. 3. Longman, Kuala Lumpur.Google Scholar
  34. LaFrankie, J. V., Tan, S. & Ashton, P. S. 1995. Species List for the 52-ha Forest Dynamics Research Plot Lambir Hills National Park, Sarawak, Malaysia. Miscellaneous Internal Report (2/9/95). Center for Tropical Forest Science.Google Scholar
  35. Laman, T. G. 1995. Ficus stupenda germination and seedling establishment in a Bornean rain forest canopy. Ecology 76: 2617–2626.Google Scholar
  36. Laman, T. G. 1996. Ficus seed shadows in a Bornean rain forest. Oecologia 107: 347–355.Google Scholar
  37. Lambert, F. R. L. 1989a. Fig-eating by birds in aMalaysian lowland forest. J. Trop. Ecol. 5: 401–412.Google Scholar
  38. Lambert, F. R. L. 1989b. Pigeons as seed predators and dispersers of figs in a Malaysian lowland forest. Ibis 131: 521–527.Google Scholar
  39. Lambert, F. R. 1990. Some notes on fig-eating by arboreal mammals in Malaysia. Primates 31: 453–458.Google Scholar
  40. Lambert, F. R. & Marshall, A. G. 1991. Keystone characteristics of a bird-dispersed Ficus in aMalaysian lowland rain forest. J. Ecol. 79: 793–809.Google Scholar
  41. Leighton, M. 1982. Fruit resources and patterns of feeding, spacing and grouping among sympatric Bornean hornbills (Bucerotidae). PhD thesis. University of California.Google Scholar
  42. Leighton, M. & Leighton, D. R. 1983. Vertebrate responses to fruiting seasonality within a Bornean rain forest. Pp. 181–196. In: Sutton, S. L., Whitmore, T. C. & Chadwick, A. C. (eds), Tropical rain forest: ecology and management. Blackwell, Oxford.Google Scholar
  43. MacKinnon, J. & Phillipps, K. 1993. A Field Guide to the Birds of Borneo, Sumatra, Java and Bali. Oxford University Press Inc., New York.Google Scholar
  44. MacKinnon, K., Hatta, G., Halim, H. & Mangalik, A. 1996. The ecology of Kalimantan. Indonesian Borneo. Oxford University Press, Oxford.Google Scholar
  45. Marshall, A. G. 1985. Old World phytophagous bats (Megachiroptera) and their food plants: a survey. Zool. J. Linn. Soc. 83: 351–369.Google Scholar
  46. McClure, H. E. 1966. Flowering, fruiting and animals in the canopy of a tropical rain forest. Malay. Forester 29: 192–203.Google Scholar
  47. Medway, L. 1972. Phenology of a tropical forest in Malaysia. Biol. J. Linn. Soc. 4: 117–146.Google Scholar
  48. Medway, L. & Wells, D. R. 1971. Diversity and density of birds and mammals at Kuala Lompat, Pahang. Malay. Nat. J. 24: 238–247.Google Scholar
  49. Michaloud, G., Carriere, S. & Koobi, M. 1996. Exceptions to the one:one relationship between African fig trees and their fig wasp pollinators: possible evolutionary scenarios. J. Biogeogr. 23: 513–520.Google Scholar
  50. Midya, S. & Brahmachary, R. L. 1991. The effect of birds upon the germination of banyan (Ficus bengalensis) seeds. J. Trop. Ecol. 7: 537–538.Google Scholar
  51. Milton, K. & May, M. L. 1976. Body weight, diet and home range area in primates. Nature 259: 459–462.Google Scholar
  52. Mondolfi, E. 1989. Notes on the distribution, habitat, food habits, status and conservation of spectacled bears (Tremarctos ornatus Cuvier) in Venezuela. Mammalia 53: 525–544.Google Scholar
  53. O'Brien, T. G., Kinnaird, M. F., Dierenfeld, E. S., Conklin-Brittain, N. L., Wrangham, R. W. & Silver, S. C. 1998. What's so special about figs? Nature 392: 668.Google Scholar
  54. O'Dowd, D. J. & Gill, A. M. 1986. Seed dispersal syndromes in Australian Acacia. Pp. 87–121. In: Murray, D. R. (ed.), Seed Dispersal. Academic Press, Sydney.Google Scholar
  55. Patel, A. 1996. Variation in a mutualism: phenology and the maintenance gynodioecy in two Indian fig species. J. Ecol. 84: 667–680.Google Scholar
  56. Payne, J., Francis, C. M. & Phillipps, K. 1985. A Field Guide to the Mammals of Borneo. The Sabah Society & WWF Malaysia, Kota Kinabalu.Google Scholar
  57. Primack, R. B. 1983. Forester's guide to the Moraceae of Sarawak. Forest Department, Sarawak.Google Scholar
  58. Rabinowitz, A. R. 1991. Behaviour and movements of sympatric civet species in Huai Kha Khaeng Wildlife Sanctuary, Thailand. J. Zool. 223: 281–298.Google Scholar
  59. Richards, P.W. 1952. The Tropical Rain Forest. An ecological study. Cambridge University Press, Cambridge.Google Scholar
  60. Ridley, H. N. 1930. The Dispersal of Plants Throughout the World. L. Reeve & Co., Kent.Google Scholar
  61. Root, R. B. 1967. The niche exploitation pattern of the blue-headed flycatcher. Ecol. Mono. 37: 317–350.Google Scholar
  62. Sakai, S., Momose, K., Yumoto, T., Nagamitsu, T., Nagamasu, H., Hamid, A. A. & Nakashizuka, T. 1999. Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Amer. J. Bot. 86: 1414–1436.Google Scholar
  63. Schupp, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108: 15–29.Google Scholar
  64. Shanahan, M. & Compton, S. G. in press. Fig-eating by Bornean treeshrews (Tupaia spp.): evidence for a role as seed dispersers. Biotropica.Google Scholar
  65. SPSS (1997). SYSTAT 7.0 for Windows. SPSS, Inc.Google Scholar
  66. Tamboia, T., Cipollini, M. L. & Levey, D. J. 1996. An evaluation of vertebrate seed dispersal syndromes in four species of black nightshade (Solanum sect. Solanum). Oecologia 107: 522–532.Google Scholar
  67. Terborgh, J. 1986. Keystone plant resources in the tropical forest. Pp. 330–344. In: Soule, M. E. (ed.), Conservation biology, the science of scarcity and diversity. Sinauer, Sunderland, MA.Google Scholar
  68. Traveset, A. 1990. Ctenosaura similis Gray (Iguanidae) as a seed disperser in a Central American deciduous forest. Am. Midl. Nat. 123: 402–404.Google Scholar
  69. Turcek, F. J. 1963. Colour preferences in fruit and seed-eating birds. Pp. 285–292. In: Proceedings XIII International Ornithi. Congress 1962. Ithaca, New York.Google Scholar
  70. van der Pijl, L. 1957. The dispersal of plants by bats (Chiropterophily). Acta Bot. Neerl. 6: 291–315.Google Scholar
  71. van der Pijl, L. 1982. Principles of dispersal in higher plants. Springer-Verlag, Berlin.Google Scholar
  72. Wheelwright, N. T. 1985. Competition for dispersers, and the timing of flowering and fruiting in a guild of tropical trees. Oikos 44: 465–477.Google Scholar
  73. Wheelwright, N. T. & Janson, C. H. 1985. Colours of fruit displays of bird-dispersed plants in two tropical forests. Am. Nat. 126: 777–799.Google Scholar
  74. Whitney, K. D., Fogiel, M. K., Lamperti, A. M., Holbrook, K. M., Stauffer, D. J., Hardesty, B. D., Parker, V. T. & Smith, T. B. 1998. Seed dispersal by Ceratogymna hornbills in the Dja reserve, Cameroon. J. Trop. Ecol. 14: 351–371.Google Scholar
  75. Wiebes, J. T. 1979. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Syst. 10: 1–12.Google Scholar
  76. Wong, M. 1986. Trophic organisation of understorey birds in a Malaysian dipterocarp forest. Auk 103: 100–116.Google Scholar
  77. Yamakura, T. 1992. Structure and species diversity. Pp. 53–59. In: Shidei, T. & Kira, T. (eds), Considering of tropical forests. Jinbunshoin, Kyoto.Google Scholar
  78. Yumoto, T. & Inoue, T. 1995. Canopy Biology Program in Sarawak-Long term study of plant phenology and plant-animal interactions in a mixed dipterocarp forest. Tropics 4: 307–315.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Mike Shanahan
    • 1
  • Stephen G. Compton
    • 1
  1. 1.Centre for Biodiversity & Conservation, School of BiologyUniversity of LeedsLeedsUK

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