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

Published online by Cambridge University Press:  02 August 2011

Kara L. Moses  and
Stuart Semple
Kara L. Moses*
Affiliation:
Centre for Research in Evolutionary Anthropology, Department of Life Sciences, Roehampton University, UK
Stuart Semple
Affiliation:
Centre for Research in Evolutionary Anthropology, Department of Life Sciences, Roehampton University, UK
*
1Corresponding author. Email: [email protected]
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Abstract:

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.

Keywords

deinhibitiondispersal distancegermination trialslemurMadagascarseed dispersalseed sizespatially restricted dispersal
Type
Research Article
Information
Journal of Tropical Ecology , Volume 27 , Issue 5 , September 2011 , pp. 529 - 538
Copyright
Copyright © Cambridge University Press 2011

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References

LITERATURE CITED

ALTMANN, J. 1974. Observational study of behaviour: sampling methods. Behaviour 49:227–265.CrossRefGoogle ScholarPubMed
ANDRESEN, E. 2002. Primary seed dispersal by red howler monkeys and the effect of defecation pattern on the fate of dispersed seeds. Biotropica 34:261–272.CrossRefGoogle Scholar
AUGSPURGER, C. K. 1984. Seedling survival among tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712.CrossRefGoogle Scholar
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 61:211–217.CrossRefGoogle ScholarPubMed
BOWMAN, J., JAEGER, J. A. G. & FAHRIG, L. 2002. Dispersal distance of mammals is proportional to home range size. Ecology 83:2049–2055.CrossRefGoogle Scholar
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 310:1029–1031.CrossRefGoogle Scholar
CHAPMAN, C. A. & RUSSO, S. E. 2007. Primate seed dispersal: Linking behavioral ecology with forest community structure. Pp. 510–525 in Campbell, C., Fuentes, A., MacKinnon, K., Stumpf, R. M. & Bearder, S. (eds.). Primates in perspective. Oxford University Press, Oxford. 720 pp.Google Scholar
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pp. 298–312 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. Pudoc, Wageningen.Google Scholar
CRAMER, J. M., MESQUITA, R. & WILLIAMSON, G. B. 2007. Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation 137:415–423.CrossRefGoogle Scholar
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 26:35–43.CrossRefGoogle Scholar
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.Google Scholar
DEW, J. L. & WRIGHT, P. 1998. Frugivory and seed dispersal by four species of primates in Madagascar's eastern rain forest. Biotropica 30:425–437.CrossRefGoogle Scholar
DEWAR, R. E. 1984. Recent extinctions in Madagascar: the loss of the subfossil fauna. Pp. 574–593 in Martin, P. S. & Klein, R. G. (eds.). Quaternary extinctions. University of Arizona Press, Arizona.Google Scholar
DRANSFIELD, J. & BEENTJE, H. 2003. Arecaceae, palms. Pp. 448–457 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.Google Scholar
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 18:529–536.3.0.CO;2-D>CrossRefGoogle Scholar
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 5:25–32.CrossRefGoogle Scholar
GANZHORN, J. U., FIETZ, J., RAKOTOVAO, E., SCHWAB, D. & ZINNER, D. 1999. Lemurs and regeneration of dry deciduous forest in Madagascar. Conservation Biology 13:794–804.CrossRefGoogle Scholar
GARBER, P. A. 1986. The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). American Journal of Primatology 10:155–170.CrossRefGoogle ScholarPubMed
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 404:493–495.CrossRefGoogle Scholar
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201–228.CrossRefGoogle Scholar
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 16:859–875.CrossRefGoogle Scholar
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 31:43–52.CrossRefGoogle Scholar
JANSON, C. H. 1983. Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science 219:187–189.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forest. American Naturalist 104:501–528.CrossRefGoogle Scholar
JOLLY, A. 1966. Lemur behaviour. University of Chicago Press, Chicago. 187 pp.Google Scholar
JOLLY, A. 1984. The puzzle of female feeding priority. Pp. 197–215 in Small, M. (ed.). Female primates: studies by women primatologists. Alan R. Liss, New York.Google Scholar
LAMBERT, J. E. 2001. Red-tailed guenons (Cercopithecus ascanius and Strychnos mitis): evidence for plant benefits beyond seed dispersal. International Journal of Primatology 22:189–201.CrossRefGoogle Scholar
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 22:235–246.CrossRefGoogle Scholar
LOISELLE, B. A. 1990. Seeds in droppings of tropical fruit-eating birds: importance of considering seed composition. Oecologia 82:494–500.CrossRefGoogle ScholarPubMed
MALHI, Y. & GRACE, J. 2000. Tropical forests and atmospheric carbon dioxide. Trends in Ecology and Evolution 15:332–337.CrossRefGoogle ScholarPubMed
MCCONKEY, K. R. 2000. Primary seed shadow generated by gibbons in the rainforests of Barito Ulu, Central Borneo. American Journal of Primatology 52:13–29.3.0.CO;2-Y>CrossRefGoogle Scholar
OVERDORFF, D. J. & JOHNSON, S. 2003. Eulemur, true lemurs. Pp. 1320–1324 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.Google Scholar
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.Google Scholar
RATSIRARSON, J. 2003. Dypsis decaryi, Triangle Palm, Lafa. Pp. 457–460 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.Google Scholar
SAMUELS, I. A. & LEVEY, D. J. 2005. Effects of gut passage on seed germination: do experiments answer the questions they ask? Functional Ecology 19:365–368.CrossRefGoogle Scholar
SCHATZ, G. E. 2001. Generic tree flora of Madagascar. Royal Botanic Gardens, Kew and Missouri Botanical Garden, St Louis. 477 pp.Google Scholar
SCHUPP, E. W. 1988. Factors affecting post-dispersal seed survival in a tropical forest. Oecologia 76:525–530.CrossRefGoogle Scholar
SCHUPP, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108:15–29.CrossRefGoogle Scholar
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 6:13–21.Google Scholar
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 50:275–289.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
TATTERSALL, I. 1982. The primates of Madagascar. Columbia University Press, New York. 382 pp.Google Scholar
TERBORGH, J. N., PITMAN, M., SILMAN, H., SCHICHTER, P. & NUNEZ, V. 2002. Maintenance of tree diversity in tropical forests. Pp. 1–18 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford.Google Scholar
TRAVESET, A., ROBERTSON, A. W. & RODRIGUEZ-PÉREZ, J. 2007. A review on the role of endozoochory on seed germination. Pp. 78–103 in Dennis, A. J., Schupp, E. W. & Green, R. J. (eds.). Seed dispersal: theory and its application in a changing world. CABI Publishing, Wallingford.CrossRefGoogle Scholar
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 7:181–199.CrossRefGoogle Scholar
VASEY, N. 2003. Varecia, Ruffed lemurs. Pp. 1332–1336 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. The University of Chicago Press, Chicago.Google Scholar
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 91:677–685.CrossRefGoogle Scholar
WHEELWRIGHT, N. T. 1985. Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818.CrossRefGoogle Scholar
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 64:124–131.CrossRefGoogle Scholar
WRANGHAM, R. W., CHAPMAN, C. A. & CHAPMAN, L. J. 1994. Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology 10:355–368.CrossRefGoogle Scholar
WRIGHT, P. C. 1997. The future of biodiversity in Madagascar: a view from Ranomafana National Park. Pp. 381–405 in Patterson, B. D. & Goodman, S. M. (eds.). Environmental change in Madagascar. Smithsonian Institution Press, Washington.Google Scholar
WRIGHT, P. C. 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yearbook of Physical Anthropology 42:31–72.3.0.CO;2-0>CrossRefGoogle Scholar
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 14:227–239.CrossRefGoogle Scholar