Abstract
With the conversion of natural habitats to farmland, nonhuman primates (hereafter primates) are increasingly exposed to agricultural crops. Although frugivorous primates are important seed dispersers that sometimes feed on agricultural fruits, evidence for dispersal of crops by primates is lacking. Here, we examine flexible feeding on cacao (Theobroma cacao) fruit and seed dispersal patterns by chimpanzees (Pan troglodytes verus) at Bossou in Guinea, and consequent cacao germination and survival. From direct observations, we confirm that cacao fruit is not an important food to chimpanzees, representing 0.23 % of focal animal feeding time. Chimpanzees ingest cacao pulp and either spit out the large seeds intact from unripe cacao fruit or swallow the seeds from ripe cacao fruits, which are consequently deposited in feces. From ecological surveys we show that chimpanzees distributed cacao extensively throughout their home range, at a mean distance of 407 m ± SE 0.6 (N = 90 clusters, range: 4–1130 m) from cacao plantations. As distance from the cacao plantation increased, cacao plants were more likely to survive. Other factors, including number of cacao plants in a cluster, plant height, and openness of the understory did not predict short-term cacao survival. Cacao plants within the forest did not produce fruit. By contrast, when chimpanzees deposited seeds in a plantation, cacao plants produced fruits as a result of farmers’ maintenance of the area. Our local-scale findings emphasize the complex behavioral and ecological interconnections between coexisting humans and primates in agricultural landscapes and generate interesting questions regarding primate niche construction and crop “ownership” related to who “plants” the crop.
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Albert, A., McConkey, K., Savini, T., & Huynen, M. C. (2014). The value of disturbance-tolerant cercopithecine monkeys as seed dispersers in degraded habitats. Biological Conservation, 170, 300–310.
Arroyo-Rodríguez, V., Andresen, E., Bravo, S. P., & Stevenson, P. R. (2015). Seed dispersal by howler monkeys: current knowledge, conservation implications, and future directions. In M. M. Kowalewski, P. A. Garber, L. Cortes-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 111–139). Developments in Primatology: Progress and Prospects. New York: Springer Science + Business Media.
Asare, R. (2006). Learning about neighbour trees in cocoa growing systems: A manual for farmer trainers. Forest and Landscape Development and Environment Series 4. Horsholm, Denmark: The Danish Centre for Forest, Landscape and Planning.
Babweteera, F., & Brown, N. (2009). Can remnant frugivore species effectively disperse tree seeds in secondary tropical rain forests? Biodiversity and Conservation, 18, 1611–1627.
Balcomb, S. R., & Chapman, C. A. (2003). Bridging the gap: Influence of seed deposition on seedling recruitment in a primate–tree interaction. Ecological Monographs, 73, 625–642.
Beaune, D. (2015). What would happen to the trees and lianas if apes disappeared? Oryx, 49, 442–446.
Beaune, D., Bretagnolle, F., Bollache, L., Hohmann, G., Surbeck, M., et al. (2013). The bonobo–dialium positive interactions: Seed dispersal mutualism. American Journal of Primatology, 75, 394–403.
Bessa, J., Sousa, C., & Hockings, K. J. (2015). Feeding ecology of chimpanzees (Pan troglodytes verus) inhabiting a forest–mangrove–savanna–agricultural matrix at Caiquene-Cadique, Cantanhez National Park, Guinea-Bissau. American Journal of Primatology, 77, 651–665.
Campbell-Smith, G., Campbell-Smith, M., Singleton, I., & Linkie, M. (2011). Raiders of the lost bark: Orangutan foraging strategies in a degraded landscape. PLoS ONE, 6, e20962.
Candolin, U., & Wong, B. B. M. (2012). Behavioural responses to a changing world: mechanisms and consequences. Oxford: Oxford University Press.
Chapman, C. A. (1989). Primate seed dispersal: The fate of dispersed seeds. Biotropica, 21, 148–154.
Chapman, C. A., & Chapman, L. J. (1995). Survival without dispersers: Seedling recruitment under parents. Conservation Biology, 9, 675–678.
Chapman, C. A., & Russo, S. E. (2007). Primate seed dispersal: Linking behavioural ecology and forest community structure. In C. J. Campbell, A. F. Fuentes, K. C. MacKinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 510–525). Oxford: Oxford University Press.
Connell, J. H. (1971). On the role of natural enemies in preventing competitive exclusion in some marine animals and rain forest trees. In P. J. de Boer & P. R. Gradwell (Eds.), Dynamics of populations (pp. 289–312). Wageningen: Centre for Agricultural Publishing and Documentation.
Corlett, R. T. (2015). The Anthropocene concept in ecology and conservation. Trends in Ecology & Evolution, 30, 36–41.
Cramer, J. M., Mesquita, R. C. G., & Williamson, G. B. (2007). Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation, 137, 415–423.
Dennis, A. J., Schupp, E. W., Green, R. J., & Westcott, D. A. (2007). Seed dispersal: theory and its application in a changing world. Wallingford: CAB International.
Estrada, A., Raboy, B. E., & Oliveira, L. C. (2012). Agroecosystems and primate conservation in the tropics: A review. American Journal of Primatology, 74, 696–711.
Fuentes, A. (2012). Ethnoprimatology and the anthropology of the human-primate interface. Annual Review of Anthropology, 41, 101–117.
Fuentes, A., & Hockings, K. J. (2010). The ethnoprimatological approach in primatology. American Journal of Primatology, 72, 841–847.
Fuentes, A., & Wolfe, L. D. (2002). Primates face to face: The conservation implications of human–nonhuman primate interconnections. Cambridge: Cambridge University Press.
Ganzhorn, J. U., Fietz, J., Rakotovao, E., Schwab, D., & Zinner, D. (1999). Lemurs and the regeneration of dry deciduous forest in Madagascar. Conservation Biology, 13, 794–804.
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.
Gonzalez-Varo, J. P., Arroyo, J. M., & Jordano, P. (2014). Who dispersed the seeds? The use of DNA barcoding in frugivory and seed dispersal studies. Methods in Ecology and Evolution, 5, 806–814.
Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge: Harvard University Press.
Haurez, B., Petre, C., & Doucet, J. (2013). Impacts of logging and hunting on western lowland gorilla (Gorilla gorilla gorilla) populations and consequences for forest regeneration: A review. Biotechnology, Agronomy, Society and Environment, 17, 364–372.
Haurez, B., Dainou, K., Tagg, N., Petre, C., & Doucet, J. (2015). The role of great apes in seed dispersal of the tropical forest tree species Dacryodes normandii (Burseraceae) in Gabon. Journal of Tropical Ecology, 31, 395–402.
Hockings, K. J., & McLennan, M. R. (2012). From forest to farm: Systematic review of cultivar feeding by chimpanzees – management implications for wildlife in anthropogenic landscapes. PLoS ONE, 7, e33391.
Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2006). Road-crossing in chimpanzees: A risky business. Current Biology, 16, 668–670.
Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2009). Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: Feeding dynamics in a human-influenced environment. American Journal of Primatology, 71, 636–646.
Hockings, K. J., Yamakoshi, G., Kabasawa, A., & Matsuzawa, T. (2010). Attacks on local persons by chimpanzees in Bossou, Republic of Guinea: Long-term perspectives. American Journal of Primatology, 72, 887–896.
Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2012). Socio-ecological adaptations by chimpanzees (Pan troglodytes verus) inhabiting an anthropogenically impacted habitat. Animal Behaviour, 83, 801–810.
Hockings, K. J., McLennan, M. R., Carvalho, S., Ancrenaz, M., Bobe, R., et al. (2015). Apes in the Anthropocene: Flexibility and survival. Trends in Ecology & Evolution, 30, 215–222.
Howes, F. N. (1946). The early introduction of cocoa to West Africa. African Affairs, 45, 152–153.
Humle, T. (2011). Location and ecology. In T. Matsuzawa, T. Humle, & Y. Sugiyama (Eds.), Chimpanzees of Bossou and Nimba (pp. 13–21). Tokyo: Springer.
Janson, C. H. (1983). Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science, 219, 187–189.
Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forests. The American Naturalist, 104, 501–528.
Jordano, P., Forget, P.-M., Lambert, J. E., Bohning-Gaese, K., Traveset, A., & Wright, S. J. (2011). Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters, 7, 321–323.
Krief, S., Cibot, M., Bortolamiol, S., Seguya, A., Krief, J.-M., & Masi, S. (2014). Wild chimpanzees on the edge: Nocturnal activities in croplands. PLoS ONE, 9, e109925.
Laland, K., & Booget, N. (2008). Niche construction, co-evolution and biodiversity. Ecological Economics, 69, 731–736.
Lambert, J. E. (1997). Digestive strategies, fruit processing, and seed dispersal in the chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius) of Kibale National Park, Uganda. PhD thesis, University of Illinois.
Lambert, J. E. (1999). Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. American Journal of Physical Anthropology, 109, 365–386.
Lambert, J. E., & Chapman, C. A. (2005). The fate of primate dispersed seeds: Deposition pattern, dispersal distance, and implications for conservation. In P.-M. Forget, J. E. Lambert, P. Hulme, & S. Vander Wall (Eds.), Seed fate: Predation, dispersal and seedling establishment (pp. 137–150). Wallingford: CAB International.
Levine, J. M., & Murrell, D. J. (2003). The community-level consequences of seed dispersal patterns. Annual Review of Ecology and Systematics, 34, 549–574.
Linder, J. M., & Oates, J. F. (2011). Differential impact of bushmeat hunting on monkey species and implications for primate conservation in Korup National Park, Cameroon. Biological Conservation, 144, 738–745.
Markl, J., Schleuning, M., Forget, P.-M., Jordano, P., Lambert, J. E., et al. (2012). Impact of human disturbance on seed dispersal by animals: A meta-analysis. Conservation Biology, 26, 1072–1081.
Matsuzawa, T., Humle, T., & Sugiyama, Y. (2011). The chimpanzees of Bossou and Nimba. Tokyo: Springer.
McKinney, T. (2011). The effects of provisioning and crop-raiding on the diet and foraging activities of human-commensal white-faced capuchins (Cebus capucinus). American Journal of Primatology, 73, 439–448.
McLennan, M. R. (2013). Diet and feeding ecology of chimpanzees (Pan troglodytes) in Bulindi, Uganda: Foraging strategies at the forest–farm interface. International Journal of Primatology, 34, 585–614.
McLennan, M. R., & Hockings, K. J. (2014). Wild chimpanzees show group differences in selection of agricultural crops. Scientific Reports, 4, 5956.
McLennan, M. R., & Hockings, K. J. (2016). The aggressive apes? Causes and contexts of great ape attacks on humans. In F. M. Angelici (Ed.), Problematic wildlife: A cross-disciplinary approach (pp. 373–394). Cham: Springer International Publishing.
Nathan, R., & Muller-Landau, H. C. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15, 278–285.
Paterson, J. D., & Wallis, J. (2005). Commensalism and conflict: The human-primate interface. Norman: American Society of Primatologists.
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, 228–240.
Pruetz, J. D. (2006). Feeding ecology of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 326–364). Cambridge: Cambridge University Press.
Riley, E. P. (2008). Ranging patterns and habitat use of Sulawesi Tonkean macaques (Macaca tonkeana) in a human-modified habitat. American Journal of Primatology, 70, 670–679.
Riley, E. P., Tolbert, B., & Farida, W. R. (2013). Nutritional content explains the attractiveness of cacao to crop raiding Tonkean macaques. Current Zoology, 59, 160–169.
Russo, S. E., & Augspurger, C. K. (2004). Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters, 7, 1058–1067.
Russo, S. E., & Chapman, C. A. (2011). Primate seed dispersal: Linking behavioural ecology and forest community structure. In C. J. Campbell, A. F. Fuentes, K. C. MacKinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 523–534). Oxford: Oxford University Press.
Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 108, 15–29.
Seiler, N., & Robbins, M. (2016). Factors influencing ranging on community land and crop raiding by mountain gorillas. Animal Conservation, 19, 176–188.
Sengupta, A., McConkey, K. R., & Radhakrishna, S. (2015). Primates, provisioning and plants: Impacts of human cultural behaviours on primate ecological functions. PLoS ONE, 10, e0140961.
Sih, A., Ferrari, M. C. O., & Harris, D. J. (2011). Evolution and behavioural responses to human-induced rapid environmental change. Evolutionary Applications, 4, 367–387.
Sih, A., Ehlman, S., & Halpin, R. (2015). On connecting behavioural responses to HIREC to ecological outcomes: A comment on Wong and Candolin. Behavioral Ecology, 26, 676–677.
Sokal, R. R., & Rohlf, F. J. (1995). The principles and practice of statistics in biological research (3rd ed.). New York: W. H. Freeman.
Stoner, K. E., Vulinec, K., Wright, S. J., & Peres, C. A. (2007). Hunting and plant community dynamics in tropical forests: A synthesis and future directions. Biotropica, 39, 385–392.
Strum, S. C. (2010). The development of primate raiding: Implications for management and conservation. International Journal of Primatology, 31, 133–156.
Strum, S. C., Stirling, G., & Kalusi Mutunga, S. (2015). The perfect storm: Land use change promotes Opuntia stricta’s invasion of pastoral rangelands in Kenya. Journal of Arid Environments, 118, 37–47.
Sugiyama, Y. (2004). Demographic parameters and life history of chimpanzees at Bossou, Guinea. American Journal of Physical Anthropology, 124, 154–165.
Takemoto, H. (2004). Seasonal change in terrestriality of chimpanzees in relation to microclimate in the tropical forest. American Journal of Physical Anthropology, 124, 81–92.
Treves, A., Wallace, R. B., Naughton-Treves, L., & Morales, A. (2006). Co-managing human–wildlife conflicts – a review. Human Dimensions of Wildlife, 11, 383–396.
Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997). The primate community of the Lope Reserve, Gabon: Diets, responses to fruit scarcity and effects on biomass. American Journal of Primatology, 42, 1–24.
Valenta, K., Hopkins, M. E., Meeking, M., Chapman, C. A., & Fedigan, L. M. (2015). Spatial patterns of primary seed dispersal and adult tree distributions: Genipa americana dispersed by Cebus capucinus. Journal of Tropical Ecology, 31, 491–498.
Vidal, M. M., Pires, M. M., & Guimarães, P. R. (2013). Large vertebrates as the missing components of seed-dispersal networks. Biological Conservation, 163, 42–48.
Wang, B. C., Sork, V. L., Leong, M. T., & Smith, T. B. (2007). Hunting of mammals reduces seed removal and dispersal of the afrotropical tree Antrocaryon klaineanum (Anacardiaceae). Biotropica, 39, 340–347.
Watts, D. P., Potts, K. B., Lwanga, J. S., & Mitani, J. C. (2012). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. Diet composition and diversity. American Journal of Primatology, 74, 114–129.
Webb, C. O., & Peart, D. R. (2001). High seed dispersal rates in faunally intact tropical rain forest: Theoretical and conservation implications. Ecology Letters, 4, 491–499.
Wong, B., & Candolin, U. (2015). Behavioural responses to changing environments. Behavioral Ecology, 26, 665–673.
Woodroffe, R., Thirgood, S., & Rabinowitz, A. (2005). People and wildlife: Conflict or coexistence? Cambridge: Cambridge University Press.
Wrangham, R. W., Chapman, C. A., & Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology, 10, 355–368.
Wright, S. J. (2003). The myriad consequences of hunting for vertebrates and plants in tropical forests. Perspectives in Plant Ecology Evolution and Systematics, 6, 73–86.
Wright, S. J. (2007). Seed dispersal in anthropogenic landscapes. In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 599–614). Wallingford: CAB International.
Yamakoshi, G. (2011). The ‘prehistory’ before 1976: Looking back on three decades of research on Bossou chimpanzees. In T. Matsuzawa, T. Humle, & Y. Sugiyama (Eds.), The chimpanzees of Bossou and Nimba (pp. 35–44). Tokyo: Springer.
Zárate, D. A., Andresen, E., Estrada, A., & Serio‐Silva, J. C. (2014). Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico. American Journal of Primatology, 76, 890–899.
Acknowledgments
We thank the DNRSIT and A. G. Soumah, director of the IREB, Guinea and local research assistants, especially B. Zogbila, for invaluable help and Bossou villagers for continuing support. We thank J. R. Anderson for initial discussions, A. Friend for GIS advice, and G. Donati for comments and statistical advice. The manuscript was greatly improved by comments from M. McLennan, N. Spagnoletti, J. Setchell, and two anonymous reviewers. Research was supported by an early career fellowship IF/01128/2014 and research grant PTDC/CS-ANT/121124/2010 to K. Hockings from Fundação para a Ciência e a Tecnologia, Portugal, and MEXT grant 24000001, JSPS core-to-core CCSN, JSPS leading graduate program U04 to T. Matsuzawa.
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Hockings, K.J., Yamakoshi, G. & Matsuzawa, T. Dispersal of a Human-Cultivated Crop by Wild Chimpanzees (Pan troglodytes verus) in a Forest–Farm Matrix. Int J Primatol 38, 172–193 (2017). https://doi.org/10.1007/s10764-016-9924-y
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DOI: https://doi.org/10.1007/s10764-016-9924-y