Skip to main content Accessibility help

Primary seed dispersal by the black-and-white ruffed lemur (Varecia variegata) in the Manombo forest, south-east Madagascar

  • Kara L. Moses (a1) and Stuart Semple (a1)

Seed dispersal is a pivotal ecological process but remains poorly understood on Madagascar, where lemurs are key dispersers. The black-and-white ruffed lemur (Varecia variegata) possesses many behavioural and ecological attributes potentially conducive to effective seed dispersal, but no studies have investigated dispersal patterns in this species. This 3-mo study quantified aspects of the primary seed dispersal patterns generated by two Varecia variegata groups (7 individuals). Feeding and ranging behaviour was quantified using behavioural observation (345.6 h), dispersal quantity and seed identity was determined by faecal analysis, and 10-wk germination trials tested effects of gut passage on germination of four species. Individual lemurs dispersed an estimated 104 seeds d−1, of 40 species. Most seeds were large (>10 mm); the largest was 42 mm long. Gut passage was rapid (mean 4.4 h) and generally increased germination speed and success. Mean and maximum inferred dispersal distances were 180 and 506 m respectively; low compared with many anthropoids, but possibly typical of lemurs. Though limited by a short study period, results suggest that the ruffed lemur is an effective disperser of seeds and possibly a critical disperser of large-seeded species which other frugivores cannot swallow. Loss of large-bodied seed dispersers such as Varecia variegata may have far-reaching ecological consequences including impacts on forest structure and dynamics.

Corresponding author
1Corresponding author. Email:
Hide All
ALTMANN, J. 1974. Observational study of behaviour: sampling methods. Behaviour 49:227265.
ANDRESEN, E. 2002. Primary seed dispersal by red howler monkeys and the effect of defecation pattern on the fate of dispersed seeds. Biotropica 34:261272.
AUGSPURGER, C. K. 1984. Seedling survival among tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:17051712.
AUGSPURGER, C. K. & KELLY, C. K. 1984. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211217.
BOWMAN, J., JAEGER, J. A. G. & FAHRIG, L. 2002. Dispersal distance of mammals is proportional to home range size. Ecology 83:20492055.
BUNKER, D. E., DECLERCK, F., BRADFORD, J. C., COLWELL, R. K., PERFECTO, I., PHILLIPS, O. L., SANKARAN, M. & NAEEM, S. 2005. Species loss and aboveground carbon storage in a tropical forest. Science 310:10291031.
CHAPMAN, C. A. & RUSSO, S. E. 2007. Primate seed dispersal: Linking behavioral ecology with forest community structure. Pp. 510525 in Campbell, C., Fuentes, A., MacKinnon, K., Stumpf, R. M. & Bearder, S. (eds.). Primates in perspective. Oxford University Press, Oxford. 720 pp.
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pp. 298312 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. Pudoc, Wageningen.
CRAMER, J. M., MESQUITA, R. & WILLIAMSON, G. B. 2007. Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation 137:415423.
DE MELO, F. P. L., MARTÍNEZ-SALAS, E., BENÍTEZ-MALVIDO, J. & CEBALLOS, G. 2010. Forest fragmentation reduces recruitment of large-seeded tree species in a semi-deciduous tropical forest of southern Mexico. Journal of Tropical Ecology 26:3543.
DEW, J. L. 2001. Synecology and seed dispersal in woolly monkeys (Lagothrix lagotricha poeppigii) and spider monkeys (Ateles belzebuth belzebuth) in Parque Naçional Yasuni, Ecuador. PhD dissertation, University of California, Davis.
DEW, J. L. & WRIGHT, P. 1998. Frugivory and seed dispersal by four species of primates in Madagascar's eastern rain forest. Biotropica 30:425437.
DEWAR, R. E. 1984. Recent extinctions in Madagascar: the loss of the subfossil fauna. Pp. 574593 in Martin, P. S. & Klein, R. G. (eds.). Quaternary extinctions. University of Arizona Press, Arizona.
DRANSFIELD, J. & BEENTJE, H. 2003. Arecaceae, palms. Pp. 448457 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.
EDWARDS, M. S. & ULLREY, D. E. 1999. Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. I. Ruffed Lemurs (Varecia variegata variegata and V. v. rubra). Zoo Biology 18:529536.
FOLEY, J. A., ASNER, G. P., COSTA, M. H., COE, M. T., DE FRIES, R., GIBBS, H. K., HOWARD, E. A., OLSON, S., PATZ, J., RAMANKUTTY, N. & SNYDER, P. 2007. Amazonia revealed: forest degradation and loss of ecosystem goods and services in the Amazon Basin. Frontiers in Ecology and the Environment 5:2532.
GANZHORN, J. U., FIETZ, J., RAKOTOVAO, E., SCHWAB, D. & ZINNER, D. 1999. Lemurs and regeneration of dry deciduous forest in Madagascar. Conservation Biology 13:794804.
GARBER, P. A. 1986. The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). American Journal of Primatology 10:155170.
HARMS, K. E., WRIGHT, S. J., CALDERON, O., HERNANDEZ, A. & HERRE, E. A. 2000. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493495.
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201228.
HUBBELL, S. P., AHUMADA, J. A., CONDIT, R. & FOSTER, R. B. 2001. Local neighborhood effects on long-term survival of individual trees in a neotropical forest. Ecological Research 16:859875.
JANSEN, P. A., BONGERS, F. & Van Der MEER, P. J. 2008. Is farther seed dispersal better? Spatial patterns of offspring mortality in three rainforest tree species with different dispersal abilities. Ecography 31:4352.
JANSON, C. H. 1983. Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science 219:187189.
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forest. American Naturalist 104:501528.
JOLLY, A. 1966. Lemur behaviour. University of Chicago Press, Chicago. 187 pp.
JOLLY, A. 1984. The puzzle of female feeding priority. Pp. 197215 in Small, M. (ed.). Female primates: studies by women primatologists. Alan R. Liss, New York.
LAMBERT, J. E. 2001. Red-tailed guenons (Cercopithecus ascanius and Strychnos mitis): evidence for plant benefits beyond seed dispersal. International Journal of Primatology 22:189201.
LINK, A. & DI FIORE, A. 2006. Seed dispersal by spider monkeys and its importance in the maintenance of Neotropical rain-forest diversity. Journal of Tropical Ecology 22:235246.
LOISELLE, B. A. 1990. Seeds in droppings of tropical fruit-eating birds: importance of considering seed composition. Oecologia 82:494500.
MALHI, Y. & GRACE, J. 2000. Tropical forests and atmospheric carbon dioxide. Trends in Ecology and Evolution 15:332337.
MCCONKEY, K. R. 2000. Primary seed shadow generated by gibbons in the rainforests of Barito Ulu, Central Borneo. American Journal of Primatology 52:1329.
OVERDORFF, D. J. & JOHNSON, S. 2003. Eulemur, true lemurs. Pp. 13201324 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.
RATSIMBAZAFY, J. H. 2002. On the brink of extinction and the process of recovery: responses of black-and-white ruffed lemurs (Varecia variegata variegata) to disturbance in Manombo forest, Madagascar. PhD dissertation. State University of New York at Stony Brook, USA.
RATSIRARSON, J. 2003. Dypsis decaryi, Triangle Palm, Lafa. Pp. 457460 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.
SAMUELS, I. A. & LEVEY, D. J. 2005. Effects of gut passage on seed germination: do experiments answer the questions they ask? Functional Ecology 19:365368.
SCHATZ, G. E. 2001. Generic tree flora of Madagascar. Royal Botanic Gardens, Kew and Missouri Botanical Garden, St Louis. 477 pp.
SCHUPP, E. W. 1988. Factors affecting post-dispersal seed survival in a tropical forest. Oecologia 76:525530.
SCHUPP, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108:1529.
SPEHN, S. & GANZHORN, J. U. 2000. Influence of seed dispersal by brown lemurs on removal rates of three Grewia species (Tiliaceae) in the dry deciduous forest of Madagascar. Ecotropica 6:1321.
STEVENSON, P. R. 2000. Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology 50:275289.
SUTHERLAND, G. D., HARESTAD, A. S., PRICE, K. & LERTZMAN, K. P. 2000. Scaling of natal dispersal distances in terrestrial birds and mammals. Conservation Ecology 4:16.
TATTERSALL, I. 1982. The primates of Madagascar. Columbia University Press, New York. 382 pp.
TERBORGH, J. N., PITMAN, M., SILMAN, H., SCHICHTER, P. & NUNEZ, V. 2002. Maintenance of tree diversity in tropical forests. Pp. 118 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford.
TRAVESET, A., ROBERTSON, A. W. & RODRIGUEZ-PÉREZ, J. 2007. A review on the role of endozoochory on seed germination. Pp. 78103 in Dennis, A. J., Schupp, E. W. & Green, R. J. (eds.). Seed dispersal: theory and its application in a changing world. CABI Publishing, Wallingford.
TUTIN, C. E. G., WILLIAMSON, E. A., ROGERS, M. E. & FERNANDEZ, M. 1991. A case study of a plant–animal relationship: Cola lizae and lowland gorillas in The Lope Reserve, Gabon. Journal of Tropical Ecology 7:181199.
VASEY, N. 2003. Varecia, Ruffed lemurs. Pp. 13321336 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.
WEHNCKE, E. V., HUBBELL, S. P., FOSTER, R. B. & DALLING, J. W. 2003. Seed dispersal patterns produced by white-faced monkeys: implications for the dispersal limitation of Neotropical tree species. Journal of Ecology 91:677685.
WHEELWRIGHT, N. T. 1985. Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808818.
WHITE, F. J., OVERDORFF, D. J., BALKO, E. A. & WRIGHT, P. C. 1995. Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar. Folia Primatologica 64:124131.
WRANGHAM, R. W., CHAPMAN, C. A. & CHAPMAN, L. J. 1994. Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology 10:355368.
WRIGHT, P. C. 1997. The future of biodiversity in Madagascar: a view from Ranomafana National Park. Pp. 381405 in Patterson, B. D. & Goodman, S. M. (eds.). Environmental change in Madagascar. Smithsonian Institution Press, Washington.
WRIGHT, P. C. 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yearbook of Physical Anthropology 42:3172.
WRIGHT, S. J., ZEBALLOS, H., DOMINGUEZ, I., GALLARDO, M. M., MORENO, M. C. & IBANEZ, R. 2000. Poachers alter mammal abundance, seed dispersal, and seed predation in a Neotropical forest. Conservation Biology 14:227239.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of Tropical Ecology
  • ISSN: 0266-4674
  • EISSN: 1469-7831
  • URL: /core/journals/journal-of-tropical-ecology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed