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Ecological services performed by the bonobo (Pan paniscus): seed dispersal effectiveness in tropical forest

Published online by Cambridge University Press:  20 September 2013

David Beaune*
Affiliation:
Max-Planck-Institute for Evolutionary Anthropology, Department of Primatology, Leipzig, Germany Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, Dijon, France
François Bretagnolle
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, Dijon, France UMR 5175 CEFE-CNRS 1919, route de Mende, 34293 Montpellier 5
Loïc Bollache
Affiliation:
Université de Bourgogne, UMR1347 Agroécologie, BP 86510, F-21000 Dijon, France
Chloé Bourson
Affiliation:
Max-Planck-Institute for Evolutionary Anthropology, Department of Primatology, Leipzig, Germany Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, Dijon, France
Gottfried Hohmann
Affiliation:
Max-Planck-Institute for Evolutionary Anthropology, Department of Primatology, Leipzig, Germany
Barbara Fruth
Affiliation:
Max-Planck-Institute for Evolutionary Anthropology, Department of Primatology, Leipzig, Germany
*
1Corresponding author. Email: [email protected]

Abstract:

Survival of Afrotropical primary forests depends not only on habitat protection but also on the protection of animal species such as frugivorous primates, recognized as the most important seed dispersers for many plants. Here we investigate seed-dispersal services by the bonobo (Pan paniscus) in an evergreen lowland tropical rain forest of the Congo Basin. In the long-term research site of LuiKotale, we investigated food habits and seed processing based on 22 mo of behavioural observation, seed trial experiment and long-term daily GPS tracking of a habituated ape community. Bonobos were mainly frugivores (66% of all feeding sessions), spending about 3.5 h d−1 swallowing seeds that were transported for an average of 24 h in the gut. On average, an individual bonobo dispersed 172 kg y−1 of seeds (or 220000 seeds y−1) of more than 91 plant species by endozoochory over an average distance of 1.2 km from the parent tree. Passed seeds germinated more rapidly, more successfully and had greater post-dispersal survival than unpassed seeds. Bonobo-dispersed plants accounted for 40% of tree species and 65% of individual trees in the study site (12 1-ha plots census). Since bonobos show little functional overlap with other frugivores, the loss of their seed-dispersal services is likely to affect forest structure and dynamics. Our results justify description of the threatened bonobo as a gardener of the Congo forest.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

LITERATURE CITED

ALTMANN, J. 1974. Observational study of behavior: sampling methods. Behaviour 49:227267.CrossRefGoogle ScholarPubMed
BADRIAN, N. & MALENKY, R. 1984. Feeding ecology of Pan paniscus in the Lomako Forest, Zaire. Pp. 275299 in SUSMAN, R. L. (ed.). The pygmy chimpanzee: evolutionary biology and behavior. Plenum Press, New York.CrossRefGoogle Scholar
BEAUNE, D. 2012. Latest news from the bonobos: Pan paniscus myths and realities. Revue de Primatologie 4. http://primatologie.revues.org/1090Google Scholar
BEAUNE, D., BOLLACHE, L., BRETAGNOLLE, F. & FRUTH, B. 2012a. Dung beetles are critical in preventing post-dispersal seed removal by rodents in Congo rain forest. Journal of Tropical Ecology 28:507510.CrossRefGoogle Scholar
BEAUNE, D., BOLLACHE, L., FRUTH, B. & BRETAGNOLLE, F. 2012b. Bush pig (Potamochoerus porcus) seed predation of bush mango (Irvingia gabonensis) and other plant species in Democratic Republic of Congo. African Journal of Ecology 50:509512.CrossRefGoogle Scholar
BEAUNE, D., BOLLACHE, L., FRUTH, B., HOHMANN, G. & BRETAGNOLLE, F. 2012c. Density-dependent effect affecting elephant-seed dispersed tree recruitment (Irvingia gabonensis) in Congo forest. Pachyderm 52:97100.Google Scholar
BEAUNE, D., BRETAGNOLLE, F., BOLLACHE, L., HOHMANN, G., SURBECK, M. & FRUTH, F. 2013a. Seed dispersal strategies and the threat of defaunation in a Congo forest. Biodiversity and Conservation 22:225238.CrossRefGoogle Scholar
BEAUNE, D., FRUTH, B., BOLLACHE, L., HOHMANN, G. & BRETAGNOLLE, F. 2013b. Doom of the elephant-dependent trees in a Congo tropical forest. Forest Ecology and Management 295:109117.CrossRefGoogle Scholar
BEAUNE, D., BRETAGNOLLE, F., BOLLACHE, L., HOHMANN, G., SURBECK, M., BOURSON, C. & FRUTH, F. 2013c. The Bonobo–Dialium positive interactions: seed dispersal mutualism. American Journal of Primatology 75:394403.CrossRefGoogle ScholarPubMed
BEAUNE, D., BOLLACHE, L., MUGANZA, M. D., BRETAGNOLLE, F., HOHMANN, G. & FRUTH, B. 2013d. Artificial germination activation of Dialium corbisieri by imitation of ecological process. Journal of Sustainable Forestry 32:565575.CrossRefGoogle Scholar
BOHRER, G. I. L., NATHAN, R. A. N. & VOLIS, S. 2005. Effects of long-distance dispersal for metapopulation survival and genetic structure at ecological time and spatial scales. Journal of Ecology 93:10291040.CrossRefGoogle Scholar
BOURSON, C. 2011. La dispersion de graines par une communauté de singes dans le bassin du Congo (LuiKotale, RDC). M.Sc. dissertation, University of Burgundy, Dijon. 42 pp.Google Scholar
BRODIE, J. F., HELMY, O. E., BROCKELMAN, W. Y. & MARON, J. L. 2009. Bushmeat poaching reduces the seed dispersal and population growth rate of a mammal-dispersed tree. Ecological Applications 19:854863.CrossRefGoogle ScholarPubMed
CAIN, M. L., MILLIGAN, B. G. & STRAND, A. E. 2000. Long-distance seed dispersal in plant populations. American Journal of Botany 87:1217.CrossRefGoogle ScholarPubMed
CHAPMAN, C. A. & ONDERDONK, D. A. 1998. Forests without primates: primate/plant codependency. American Journal of Primatology 45:127141.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
CLARK, C., POULSEN, J. & PARKER, V. 2001. The role of arboreal seed dispersal groups on the seed rain of a lowland tropical forest. Biotropica 33:606620.CrossRefGoogle Scholar
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion isome marine mammals and in rain forest trees. Pp. 298310 in DEN BOER, P. J. & GRADWELL, G. (eds.). Dynamics of populations. PUDOC, Wageningen.Google Scholar
DOMINY, N. J. & DUNCAN, B. W. 2005. Seed-spitting primates and the conservation and dispersion of large-seeded trees. International Journal of Primatology 26:631649.CrossRefGoogle Scholar
EFFIOM, E. O., NUÑEZ-ITURRI, G., SMITH, H. G., OTTOSSON, U. & OLSSON, O. 2013. Bushmeat hunting changes regeneration of African rainforests. Proceedings of the Royal Society B: Biological Sciences 280:17591771.Google ScholarPubMed
FA, J. E., RYAN, S. F. & BELL, D. J. 2005. Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in afrotropical forests. Biological Conservation 121:167176.CrossRefGoogle Scholar
FENNER, M. 2000. Seeds: the ecology of regeneration in plant communities. CABI, New York. 410 pp.CrossRefGoogle Scholar
FLEMING, T. H. 1979. Do tropical frugivores compete for food? American Zoologist 19:11571172.CrossRefGoogle Scholar
FORGET, P., LAMBERT, J., HULME, P. & VANDER WALL, S. 2005. Seed fate: predation, dispersal and seedling establishment. CABI, Wallingford. 410 pp.CrossRefGoogle Scholar
FORGET, P., DENNIS, A., MAZER, S., JANSEN, P., KITAMURA, S., LAMBERT, J. & WESTCOTT, D. 2007. Seed allometry and disperser assemblages in tropical rainforests: a comparison of four floras on different continents. Pp. 536 in Dennis, A. J., Schupp, E. W., Green, R. J. & Westcott, D. A. (eds.). Seed dispersal: theory and its applications in a changing world. CAB International, Wallingford.CrossRefGoogle Scholar
FORGET, P.-M., JORDANO, P., LAMBERT, J. E., BÖHNING-GAESE, K., TRAVESET, A. & WRIGHT, S. J. 2011. Frugivores and seed dispersal (1985–2010); the ‘seeds’ dispersed, established and matured. Acta Oecologica 37:517520.CrossRefGoogle Scholar
FRUTH, B. 2011. The CBD in the Democratic Republic of Congo (DRC): the project “The Cuvette Centrale as a reservoir of medicinal plants” in the process of implementation. Curare 34:5162.Google Scholar
FRUTH, B., WILLIAMSON, E. A. & RICHARDSON, M. 2013. Bonobo Pan paniscus. Pp. 853854 in Mittermeier, R. A., Rylands, A. B. & Wilson, D. E. (eds.). Handbook of the mammals of the world. 3. Primates. Lynx Edicions, Barcelona.Google Scholar
GAUTIER-HION, A., DUPLANTIER, J. M., QURIS, R., FEER, F., SOURD, C., DECOUX, J. P., DUBOST, G., EMMONS, L., ERARD, C., HECKETSWEILER, P., MOUNGAZI, A., ROUSSILHON, C. & THIOLLAY, J. M. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324337.CrossRefGoogle Scholar
GROSS-CAMP, N. D. & KAPLIN, B. A. 2011. Differential seed handling by two African primates affects seed fate and establishment of large-seeded trees. Acta Oecologica 37:578586.CrossRefGoogle Scholar
HART, J. A., GROSSMANN, F., VOSPER, A. & ILANGA, J. 2008. Human hunting and its impact on bonobos in the Salonga National Park, Democratic Republic of Congo. Pp. 245272 in Furuichi, T. & Thompson, J. (eds.). Bonobos: behavior, ecology, and conservation. Springer, New York.CrossRefGoogle Scholar
HOHMANN, G. & FRUTH, B. 2003. Lui Kotal – A new site for field research on bonobos in the Salonga National Park. Pan Africa News 10:2527.CrossRefGoogle Scholar
HOWE, H. F. & MIRITI, M. N. 2004. When seed dispersal matters. BioScience 54:651660.CrossRefGoogle Scholar
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201228.CrossRefGoogle Scholar
IDANI, G. 1986. Seed dispersal by pygmy chimpanzees (Pan paniscus): a preliminary report. Primates 27:441447.CrossRefGoogle Scholar
JANSON, C. H. 1983. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219:187189.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104:501528.CrossRefGoogle Scholar
JORDANO, P. 2000. Fruits and frugivory. Pp. 105156 in FENNER, M. (ed.). Seeds: the ecology of regeneration in plant communities. CABI, Wallingford.Google Scholar
KANO, T. & MULAVWA, M. 1984. Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. Pp. 233274 in Susman, R. L. (ed.). The Pygmy chimpanzee: evolutionary biology and behavior. Plenum Press, New York.CrossRefGoogle Scholar
LAMBERT, J. E. 1998. Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology 7:820.3.0.CO;2-C>CrossRefGoogle Scholar
MOHNEKE, M. & FRUTH, B. 2008. Bonobo (Pan paniscus) density estimation in the SW-Salonga National Park, Democratic Republic of Congo: common methodology revisited. Pp. 151166 in Furuichi, T. & Thompson, J. (eds.). Bonobos: behavior, ecology, and conservation. Springer, New York.CrossRefGoogle Scholar
MILNER-GULLAND, E. J. & BENNETT, E. L. 2003. Wild meat: the bigger picture. Trends in Ecology and Evolution 18:351357.CrossRefGoogle Scholar
MULLER-LANDAU, H. C. 2007. Predicting the long-term effects of hunting on plant species composition and diversity in tropical forests. Biotropica 39:372384.CrossRefGoogle Scholar
NATHAN, R. & MULLER-LANDAU, H. C. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15:278285.CrossRefGoogle ScholarPubMed
NATHAN, R., PERRY, G., CRONIN, J. T., STRAND, A. E. & CAIN, M. L. 2003. Methods for estimating long-distance dispersal. Oikos 103:261273.CrossRefGoogle Scholar
NIELSEN, N. H., JACOBSEN, M. W., GRAHAM, L. L. L. B., MORROGH-BERNARD, H. C., D'ARCY, L. J. & HARRISON, M. E. 2011. Successful germination of seeds following passage through orang-utan guts. Journal of Tropical Ecology 27:433435.CrossRefGoogle Scholar
POULSEN, J. R., CLARK, C. J. & SMITH, T. B. 2001. Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology 17:787808.CrossRefGoogle Scholar
POULSEN, J. R., CLARK, C. J., CONNOR, E. F. & SMITH, T. B. 2002. Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83:228240.CrossRefGoogle Scholar
REAL, R. & VARGAS, J. M. 1996. The probabilistic basis of Jaccard's index of similarity. Systematic Biology 45:380385.CrossRefGoogle Scholar
REDFORD, K. H. 1992. The empty forest. Bioscience 42:412422.CrossRefGoogle Scholar
ROBERTSON, A. W., TRASS, A., LADLEY, J. J. & KELLY, D. 2006. Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Functional Ecology 20:5866.CrossRefGoogle Scholar
SCHUPP, E. 1992. The Janzen-Connell model for tropical tree diversity: population implications and the importance of spatial scale. American Naturalist 140:526530.CrossRefGoogle ScholarPubMed
SCHUPP, E. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Plant Ecology 107:1529.CrossRefGoogle Scholar
SCHUPP, E. W., JORDANO, P. & GOMEZ, J. M. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188:333353.CrossRefGoogle ScholarPubMed
TSUJI, Y., YANGOZENE, K. & SAKAMAKI, T. 2010. Estimation of seed dispersal distance by the bonobo, Pan paniscus, in a tropical forest in Democratic Republic of Congo. Journal of Tropical Ecology 26:115118.CrossRefGoogle Scholar
VANTHOMME, H., BELLÉ, B. & FORGET, P.-M. 2010. Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42:672679.CrossRefGoogle Scholar
VIDAL, M. M., PIRES, M. M. & GUIMARÃES, P. R. 2013. Large vertebrates as the missing components of seed-dispersal networks. Biological Conservation 163:4248.CrossRefGoogle Scholar
VOYSEY, B. C., MCDONALD, K. E., ROGERS, M. E., TUTIN, C. E. G. & PARNELL, R. J. 1999. Gorillas and seed dispersal in the Lope Reserve, Gabon. I: Gorilla acquisition by trees. Journal of Tropical Ecology 15:2338.CrossRefGoogle Scholar
WRANGHAM, R. W., CHAPMAN, C. A. & CHAPMAN, L. J. 1994. Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology 10:355368.CrossRefGoogle Scholar
WRIGHT, S. J., STONER, K. E., BECKMAN, N., CORLETT, R. T., DIRZO, R., MULLER LANDAU, H. C., NUÑEZ ITURRI, G., PERES, C. A. & WANG, B. C. 2007. The plight of large animals in tropical forests and the consequences for plant regeneration. Biotropica 39:289291.CrossRefGoogle Scholar