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Short-term post-dispersal fate of seeds defecated by two small primate species (Saguinus mystax and Saguinus fuscicollis) in the Amazonian forest of Peru

Published online by Cambridge University Press:  01 May 2009

Laurence Culot*
Affiliation:
Behavioural Biology Unit, University of Liège, Belgium Department of Behavioural Ecology and Sociobiology, Deutsches Primatenzentrum, Göttingen, Germany
Marie-Claude Huynen
Affiliation:
Behavioural Biology Unit, University of Liège, Belgium
Paul Gérard
Affiliation:
Department of Mathematics, University of Liège, Belgium
Eckhard W. Heymann
Affiliation:
Department of Behavioural Ecology and Sociobiology, Deutsches Primatenzentrum, Göttingen, Germany
*
1Corresponding author. Address: Université de Liège, Unité de Biologie du comportement: Ethologie et Psychologie animale, Quai Van Beneden, 22 Bât. I1, 4020 Liège. Email: Laurence.Culot@student.ulg.ac.be

Abstract:

Post-dispersal fate of seeds dispersed by large primates is well studied but little is known about this process in small frugivores like tamarins. This study in the Amazonian forest of Peru aimed at investigating if characteristics related to the defecation patterns of tamarins (Saguinus mystax and Saguinus fuscicollis) affected short-term post-dispersal seed fate, through secondary seed dispersal by dung beetles and removal by seed predators. Data on dung beetle activity were based on direct observations of 49 defecations while seed fate was studied using semi-controlled experiments (N = 458 for secondary dispersal and N = 398 for predation). Tamarins produce small defecations with a low number of seeds. Thirty-five per cent of defecations were visited by an average of 1.5 dung beetles that usually transport the faeces as pellets. Twenty-four per cent of seeds were buried by beetles at a mean depth of 3.5 cm. With increasing quantities of faecal matter, the probability of secondary seed dispersal increased but not the depth of burial. Seed predation pressure was low (17.6%) after 4 d and higher in faeces of S. mystax than in faeces of S. fuscicollis. Despite their small size, tamarins could be considered as high-quality seed dispersers, with a potential role for forest regeneration.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

LITERATURE CITED

ANDRESEN, E. 1999. Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica 31:145158.Google Scholar
ANDRESEN, E. 2001. Effects of dung presence, dung amount and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae) seeds in Central Amazonia. Journal of Tropical Ecology 17:6178.CrossRefGoogle Scholar
ANDRESEN, E. 2002a. Primary seed dispersal by red howler monkeys and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 34:261272.CrossRefGoogle Scholar
ANDRESEN, E. 2002b. Dung beetles in a Central Amazonian rainforest and their ecological role as a secondary seed dispersers. Ecological Entomology 27:257270.CrossRefGoogle Scholar
ANDRESEN, E. & LEVEY, D. 2004. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:4554.CrossRefGoogle ScholarPubMed
CHAMBERS, J. & MACMAHON, J. 1994. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25:263292.Google Scholar
CHAPMAN, C. 1989. Primate seed dispersal: the fate of dispersed seeds. Biotropica 21:148154.CrossRefGoogle Scholar
CHAPMAN, C. 1995. Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology 4:7482.CrossRefGoogle Scholar
CHAPMAN, C. & CHAPMAN, L. 1999. Forest restoration in abandoned agricultural land: a case study from East Africa. Conservation Biology 13:13011311.Google Scholar
CRAWLEY, M. 2000. Seed predators and plant population dynamics. Pp. 167182 in Fenner, M. (ed.). Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford.CrossRefGoogle Scholar
CULOT, L. 2005. Influence of tamarin (Saguinus fuscicollis and Saguinus mystax) behaviour and defecation pattern on the post-dispersal seed fate: predation pressure by rodents and secondary seed dispersal by dung beetles in the Amazonian forest of Peru. Master of Science Thesis, University of Liège, Liège.Google Scholar
DA SILVA, J., UHL, C. & MURRAY, G. 1996. Plant succession, landscape management, and the ecology of frugivorous birds in abandoned Amazonian pastures. Conservation Biology 10:491503.CrossRefGoogle Scholar
DAVIDSON, D. 1993. The effects of herbivory and granivory on terrestrial plant succession. Oikos 68:2335.Google Scholar
ENCARNACION, F. 1985. Introducción a la flora y vegetación de la Amazonía peruana: estado actual de los estudios, medio natural y ensayo de una clave de determinación de las formaciones vegetales en la llanura amazónica. Candollea 40:237252.Google Scholar
ESTRADA, A. & COATES-ESTRADA, R. 1984. Fruit eating and seed dispersal by howler monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxlas, Mexico. American Journal of Primatology 6:7792.Google Scholar
ESTRADA, A. & COATES-ESTRADA, R. 1991. Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology 7:459474.Google Scholar
FEER, F. 1999. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. Journal of Tropical Ecology 15:129142.CrossRefGoogle Scholar
FEER, F. & FORGET, P.-M. 2002. Spatio-temporal variation in post-dispersal seed fate. Biotropica 34:555566.Google Scholar
FORGET, P.-M. & CUIJPERS, L. 2008. Survival and scatterhoarding of frugivores-dispersed seeds as a function of forest disturbance. Biotropica 40:380385.Google Scholar
FORGET, P.-M., HAMMOND, D., MILLERON, T. & THOMAS, R. 2002. Seasonality of fruiting and food hoarding by rodents in Neotropical forests: consequences for seed dispersal and seedling recruitment. Pp. 241256 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford.Google Scholar
GARBER, P. 1986. The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). American Journal of Primatology 10:155170.Google Scholar
GORCHOV, D., CORNEJO, F., ASCORRA, C. & JARAMILLO, M. 1993. The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon. Vegetatio 107//π 108;339349.Google Scholar
HANSKI, I. & CAMBEFORT, Y. 1991. Dung beetle ecology. Princeton University Press, New Jersey. 481 pp.Google Scholar
HEYMANN, E. 1995. Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru. Journal of Zoology 237:211226.CrossRefGoogle Scholar
HOWE, H. 1984. Implications of seed dispersal by animals for tropical resource management. Biological Conservation 30:261281.CrossRefGoogle Scholar
HULME, P. 1998. Post-dispersal seed predation: consequences for plant-demography and evolution. Perspectives in Plant Ecology, Evolution and Systematics 1:3246.CrossRefGoogle Scholar
HULME, P. 2002. Seed-eaters: seed dispersal, destruction and demography. Pp. 257273 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution, and conservation. CAB International, Wallingford.Google Scholar
JONES, M. 1994. Secondary seed removal by ants, beetles, and rodents in a neotropical moist forest. Master's Thesis, University of Florida, Gainesville.Google Scholar
KAPLIN, B. & LAMBERT, J. 2002. Effectiveness of seed dispersal by Cercopithecus monkeys: implications for seed input into degraded areas. Pp. 351364 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution, and conservation. CAB International, Wallingford.Google Scholar
KNOGGE, C. & HEYMANN, E. 2003. Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: diversity and characteristics of plant species. Folia Primatologica 74:3347.CrossRefGoogle ScholarPubMed
KUNZ, B. & LINSENMAIR, E. 2007. Changes in baboon feeding behavior: maturity-dependent fruit and seed size selection within a food plant species. International Journal of Primatology 28:819835.CrossRefGoogle Scholar
LAMBERT, J. 2002. Exploring the link between animal frugivory and plant strategies: the case of primate fruit processing and post-dispersal seed fate. Pp. 365379 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution, and conservation. CAB International, Wallingford.Google Scholar
MEDELLÍN, R. & GAONA, O. 1999. Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, México. Biotropica 31:478485.CrossRefGoogle Scholar
MÜLLER, B. 2007. Determinants of the diversity of intestinal parasite communities in sympatric New World primates (Saguinus mystax, Saguinus fuscicollis, Callicebus cupreus). Doctoral dissertation, Tierärztliche Hochschule, Hannover.Google Scholar
NADJAFZADEH, M. & HEYMANN, E. 2008. Prey foraging of red titi monkeys, Callicebus cupreus, in comparison to sympatric tamarins, Saguinus mystax and Saguinus fuscicollis. American Journal of Physical Anthropology 135:5663.CrossRefGoogle ScholarPubMed
NEPSTAD, D., UHL, C., PEREIRA, C. & DA SILVA, J. 1996. A comparative study of tree establishment in abandoned pasture and mature forest of eastern Amazonia. Oikos 76:2539.Google Scholar
NOTMAN, E. & GORCHOV, D. 2001. Variation in post-dispersal seed predation in mature Peruvian lowland tropical forest and fallow agricultural sites. Biotropica 33:621636.Google Scholar
NOTMAN, E. & VILLEGAS, A. 2005. Patterns of seed predation by vertebrate versus invertebrate seed predators among different plant species, seasons and spatial distributions. Pp. 5575 in Forget, P.-M., Lambert, J., Hulme, P. & Vander Wall, S. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.CrossRefGoogle Scholar
OLIVEIRA, A. & FERRARI, S. 2000. Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): implications for the regeneration of degraded forest habitats in eastern Amazonia. Journal of Tropical Ecology 16:709716.Google Scholar
PASSOS, L. & OLIVEIRA, P. 2003. Interactions between ants, fruits and seeds in a restinga forest in south-eastern Brazil. Journal of Tropical Ecology 19:261270.Google Scholar
PECK, S. & HOWDEN, H. 1984. Response of a dung beetle guild to different sizes of dung bait in a Panamian rainforest. Biotropica 16:235238.Google Scholar
PERES, C. 1993. Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest. Journal of Zoology 230:567592.CrossRefGoogle Scholar
SCHUPP, E. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107//π 108:1529.Google Scholar
SHEPHERD, V. & CHAPMAN, C. 1998. Dung beetles as secondary seed dispersers: impact on seed predation and germination. Journal of Tropical Ecology 14:199215.CrossRefGoogle Scholar
SOINI, P. & COPPULA, M. 1981. Ecología y dinámica poblacional de pichico Saguinus fuscicollis (Primates, Callitrichidae). Informe de Pacaya 4:143.Google Scholar
SOINI, P. & SOINI, M. 1982. Distribución geográfica y ecología poblacional de Saguinus mystax (Primates, Callitrichidae). Informe de Pacaya 6:156.Google Scholar
STEVENSON, P., CASTELLANOS, M., PIZARRO, J. & GARAVITO, M. 2002. Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology 23:11871204.Google Scholar
STONER, K., RIBA-HERNANDEZ, P., VULINEC, K. & LAMBERT, J. 2007. The role of mammals in creating and modifying seedshadows in tropical forests and some consequences of their elimination. Biotropica 39:316327.Google Scholar
TERBORGH, J., PITMAN, N., SILMAN, M., SCHICHTER, H. & NÚÑEZ, P. 2002. Maintenance of tree diversity in tropical forests. Pp. 117 in Levey, D., Silva, W. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution, and conservation. CAB International, Wallingford.Google Scholar
VANDER WALL, S. & LONGLAND, W. 2004. Diplochory: are two seed dispersers better than one? Trends in Ecology and Evolution 19:155161.CrossRefGoogle ScholarPubMed
VANDER WALL, S. & LONGLAND, W. 2005. Diplochory and the evolution of seed dispersal. Pp. 297314 in Forget, P.-M., Lambert, J., Hulme, P. & VanderWall, S. Wall, S. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.Google Scholar
VILLAGRA, P., MARONE, L. & CONY, M. 2002. Mechanisms affecting the fate of Prosopis flexuosa (Fabaceae, Mimosoideae) seeds during early secondary dispersal in the Monte Desert, Argentina. Austral Ecology 27:416421.CrossRefGoogle Scholar
VULINEC, K., LAMBERT, J. & MELLOW, D. 2006. Primate and dung beetle communities in secondary growth rain forests: implications for conservation of seed dispersal systems. International Journal of Primatology 27:855879.CrossRefGoogle Scholar
WEHNCKE, E. & DALLING, J. 2005. Post-dispersal seed removal and germination selected tree species dispersed by Cebus capucinus on Barro Colorado Island, Panama. Biotropica 37:7380.CrossRefGoogle Scholar
WRANGHAM, R., CHAPMAN, C. & CHAPMAN, L. 1994. Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology 10:355368.Google Scholar