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International Journal of Primatology

, Volume 38, Issue 2, pp 172–193 | Cite as

Dispersal of a Human-Cultivated Crop by Wild Chimpanzees (Pan troglodytes verus) in a Forest–Farm Matrix

  • Kimberley J. Hockings
  • Gen Yamakoshi
  • Tetsuro Matsuzawa
Article

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.

Keywords

Anthropogenic habitat Cacao (Theobroma cacaoCultivated foods Human–wildlife interactions Niche construction Seed dispersal 

Notes

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.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10764_2016_9924_MOESM1_ESM.docx (24 kb)
ESM 1 (DOCX 23 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. 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.Google Scholar
  3. 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.Google Scholar
  4. Babweteera, F., & Brown, N. (2009). Can remnant frugivore species effectively disperse tree seeds in secondary tropical rain forests? Biodiversity and Conservation, 18, 1611–1627.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. Beaune, D. (2015). What would happen to the trees and lianas if apes disappeared? Oryx, 49, 442–446.CrossRefGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Candolin, U., & Wong, B. B. M. (2012). Behavioural responses to a changing world: mechanisms and consequences. Oxford: Oxford University Press.CrossRefGoogle Scholar
  11. Chapman, C. A. (1989). Primate seed dispersal: The fate of dispersed seeds. Biotropica, 21, 148–154.CrossRefGoogle Scholar
  12. Chapman, C. A., & Chapman, L. J. (1995). Survival without dispersers: Seedling recruitment under parents. Conservation Biology, 9, 675–678.CrossRefGoogle Scholar
  13. 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.Google Scholar
  14. 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.Google Scholar
  15. Corlett, R. T. (2015). The Anthropocene concept in ecology and conservation. Trends in Ecology & Evolution, 30, 36–41.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. Fuentes, A. (2012). Ethnoprimatology and the anthropology of the human-primate interface. Annual Review of Anthropology, 41, 101–117.CrossRefGoogle Scholar
  20. Fuentes, A., & Hockings, K. J. (2010). The ethnoprimatological approach in primatology. American Journal of Primatology, 72, 841–847.CrossRefPubMedGoogle Scholar
  21. Fuentes, A., & Wolfe, L. D. (2002). Primates face to face: The conservation implications of human–nonhuman primate interconnections. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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 Scholar
  24. 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.CrossRefGoogle Scholar
  25. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge: Harvard University Press.Google Scholar
  26. 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.Google Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2006). Road-crossing in chimpanzees: A risky business. Current Biology, 16, 668–670.CrossRefGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. Howes, F. N. (1946). The early introduction of cocoa to West Africa. African Affairs, 45, 152–153.CrossRefGoogle Scholar
  35. Humle, T. (2011). Location and ecology. In T. Matsuzawa, T. Humle, & Y. Sugiyama (Eds.), Chimpanzees of Bossou and Nimba (pp. 13–21). Tokyo: Springer.CrossRefGoogle Scholar
  36. Janson, C. H. (1983). Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science, 219, 187–189.CrossRefPubMedGoogle Scholar
  37. Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forests. The American Naturalist, 104, 501–528.CrossRefGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Laland, K., & Booget, N. (2008). Niche construction, co-evolution and biodiversity. Ecological Economics, 69, 731–736.CrossRefGoogle Scholar
  41. 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.Google Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. Levine, J. M., & Murrell, D. J. (2003). The community-level consequences of seed dispersal patterns. Annual Review of Ecology and Systematics, 34, 549–574.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefPubMedGoogle Scholar
  47. Matsuzawa, T., Humle, T., & Sugiyama, Y. (2011). The chimpanzees of Bossou and Nimba. Tokyo: Springer.CrossRefGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. McLennan, M. R., & Hockings, K. J. (2014). Wild chimpanzees show group differences in selection of agricultural crops. Scientific Reports, 4, 5956.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Paterson, J. D., & Wallis, J. (2005). Commensalism and conflict: The human-primate interface. Norman: American Society of Primatologists.Google Scholar
  54. 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.CrossRefGoogle Scholar
  55. 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.Google Scholar
  56. 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.CrossRefPubMedGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.Google Scholar
  60. Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 108, 15–29.Google Scholar
  61. Seiler, N., & Robbins, M. (2016). Factors influencing ranging on community land and crop raiding by mountain gorillas. Animal Conservation, 19, 176–188.CrossRefGoogle Scholar
  62. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. Sokal, R. R., & Rohlf, F. J. (1995). The principles and practice of statistics in biological research (3rd ed.). New York: W. H. Freeman.Google Scholar
  66. 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.CrossRefGoogle Scholar
  67. Strum, S. C. (2010). The development of primate raiding: Implications for management and conservation. International Journal of Primatology, 31, 133–156.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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.CrossRefGoogle Scholar
  69. Sugiyama, Y. (2004). Demographic parameters and life history of chimpanzees at Bossou, Guinea. American Journal of Physical Anthropology, 124, 154–165.CrossRefPubMedGoogle Scholar
  70. 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.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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.CrossRefPubMedGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. 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.CrossRefGoogle Scholar
  76. 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.CrossRefPubMedGoogle Scholar
  77. 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.CrossRefGoogle Scholar
  78. Wong, B., & Candolin, U. (2015). Behavioural responses to changing environments. Behavioral Ecology, 26, 665–673.CrossRefGoogle Scholar
  79. Woodroffe, R., Thirgood, S., & Rabinowitz, A. (2005). People and wildlife: Conflict or coexistence? Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  80. 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
  81. 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.CrossRefGoogle Scholar
  82. 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.CrossRefGoogle Scholar
  83. 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.CrossRefGoogle Scholar
  84. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Kimberley J. Hockings
    • 1
    • 2
  • Gen Yamakoshi
    • 3
  • Tetsuro Matsuzawa
    • 4
    • 5
    • 6
  1. 1.Centre for Research in Anthropology (CRIA-FCSH/UNL)LisbonPortugal
  2. 2.Anthropology Centre for Conservation, Environment and DevelopmentOxford Brookes UniversityOxfordUK
  3. 3.Center for African Area StudiesKyoto UniversityKyotoJapan
  4. 4.Institute for Advanced StudyKyoto UniversityKyotoJapan
  5. 5.Primate Research InstituteKyoto UniversityInuyamaJapan
  6. 6.Japan Monkey CentreInuyamaJapan

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