Abstract
Polyspecific associations occur when species overlap in their environment by chance, converge at common resources, or in response to predation pressure. However, because larger groups may themselves attract the attention of predators, species forming associations must balance the costs and benefits of comingling. Experimental and observational research suggests red colobus (Piliocolobus badius) associate with Diana monkeys (Cercopithecus diana) in Taï National Park, Côte d’Ivoire in response to seasonally shifting predation pressure from chimpanzees (Pan troglodytes verus). Research on this system has focused on immediate behavioral effects of comingling by red colobus and Diana monkeys. We expand on these analyses and explore longer-term changes in Diana monkey behavior. We use scan samples (N = 7025) collected on three Diana monkey groups over 5 years (N = 380 days) to assess differences in diet, activity budget, and strata use in relation to associating with red colobus and chimpanzee hunting seasonality and test for interaction effects between these two variables. We found limited evidence showing Diana monkeys make more than ephemeral behavioral changes in response to comingling with red colobus during chimpanzees’ hunting season (September–November). Synergistic effects of association and hunting season include expanded use of the main canopy, decreased fruit consumption, and increased invertebrate consumption. We find little evidence indicating Diana monkeys minimize behaviors that increase risk of predation from chimpanzees while associated with red colobus during the season when chimpanzees hunt most often. We conclude that when there are few member costs to forming mixed groups, participating species may tolerate associations even without accruing any benefits.
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References
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behavior, 49, 227–267.
Anderson, D. P., Nordheim, E. V., Moermond, T. C., Gone Bi, Z. B., & Boesch, C. (2005). Factors influencing tree phenology in Taï National Park, Côte d’Ivoire. Biotropica, 37, 631–640.
Bahaa-el-din, L., Mills, D., Hunter, L., & Heschel, P. (2015). Caracal aurata. In The IUCN red list of threatened species 2015: E.T18306A50662138.
Boesch, C. (1994). Chimpanzees-red colobus monkeys: A predator-prey system. Animal Behavior, 47, 1135–1148.
Boesch, C., & Boesch, H. (1989). Hunting behavior of wild chimpanzees in the Taï National Park. American Journal of Physical Anthropology, 78, 547–573.
Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taï Forest: Behavioral ecology and evolution. Oxford: Oxford University Press.
Brown, J. S., & Kotler, B. P. (2004). Hazardous duty pay and the foraging cost of predation. Ecology Letters, 7, 999–1014.
Bshary, R., & Noë, R. (1997a). Anti-predation behavior of red colobus monkeys in the presence of chimpanzees. Behavioral Ecology and Sociobiology, 41, 321–333.
Bshary, R., & Noë, R. (1997b). Red colobus and Diana monkeys provide mutual protection against predators. Animal Behavior, 54, 1461–1474.
Burton, F. D., & Chan, L. (1996). Behavior of mixed species groups of macaques. In J. E. Fa, D. G. Lindberg, & D. G (Eds.), Evolution and ecology of macaque societies (pp. 389–412). Cambridge: Cambridge University Press.
Buzzard, P. J. (2006a). Cheek pouch use in relation to interspecific competition and predation risk for three guenon monkeys (Cercopithecus spp.). Primates, 47, 336–341.
Buzzard, P. J. (2006b). Ecological partitioning of Cercopithecus campbelli, C. petaurista, and C. diana in the Taï Forest. International Journal of Primatology, 27, 529–558.
Buzzard, P. J. (2006c). Ranging patterns in relation to seasonality and frugivory among Cercopithecus campbelli, C. petaurista, and C. diana in the Taï Forest. International Journal of Primatology, 27, 559–573.
Buzzard, P. (2010). Polyspecific associations of Cercopithecus campbelli and C. petaurista with C. diana: What are the costs and benefits? Primates, 51, 307–314.
Buzzard, P., & Eckardt, W. (2007). The social system of the guenons. In W. S. McGraw, K. Zuberbühler, & R. Noë (Eds.), Monkeys of the Taï Forest: An African primate community (pp. 51–71). Cambridge: Cambridge University Press.
Chapman, C. A., & Chapman, L. J. (1996). Mixed-species primate groups in the Kibale Forest: Ecological constraints on association. International Journal of Primatology, 17, 31–50.
Chapman, C. A., & Chapman, L. J. (2000). Interdemic variation in mixed-species association patterns: Common diurnal primates of Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 47, 129–139.
Cords, M. (1990). Vigilance and mixed-species association of some east African forest monkeys. Behavioral Ecology and Sociobiology, 26, 297–300.
Danish, L., Chapman, C. A., Hall, M. B., Rode, K. D., & O’Driscoll Worman, C. (2006). The role of sugar in diet selection in redtail and red colobus monkeys. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical, and behavioral aspects (pp. 471–485). Cambridge: Cambridge University Press.
Eckardt, W., & Zuberbühler, K. (2004). Cooperation and competition in two forest monkeys. Behavioral Ecology, 15, 400–411.
Galat, G., & Galat-Luong, A. (1985). La communauté de primates diurnes de la forêt de Taï, Côte d’Ivoire. Revue d’Écologie, 40, 3–32.
Gartlan, J. S., & Struhsaker, T. T. (1972). Polyspecific associations and niche separation of rain-forest anthropoids in Cameroon, West Africa. Journal of Zoology, 168, 221–265.
Gautier-Hion, A., Quris, R., & Gautier, J.-P. (1983). Monospecific vs. polyspecific life: A comparative study of foraging and antipredatory tactics in a community of Cercopithecus monkeys. Behavioral Ecology and Sociobiology, 12, 235–335.
Hamilton, W. D. (1971). Geometry for the selfish herd. Journal of Theoretical Biology, 31, 295–311.
Holenweg, A.-K., Noë, R., & Schabel, M. (1996). Waser’s gas model applied to association between red colobus and Diana monkeys in the Taï National Park, Ivory Coast. Folia Primatologica, 67, 125–136.
Höner, O. P., Leumann, L., & Noë, R. (1997). Dyadic associations of red colobus and Diana monkey groups in the Taï National Park, Ivory Coast. Primates, 38, 281–291.
Jaccard, J. (1998). Interaction effects in factorial analysis of variance. Thousand Oaks, CA: SAGE.
Kane, E. E., & Gnepa, F. (2016). An infanticide attempt after male takeover in Diana monkeys (Cercopithecus diana diana) in Taï, Côte d’Ivoire. African Primates, 11, 37–40.
Kane, E. E., & McGraw, W. S. (2017). Dietary variation in Diana monkeys (Cercopithecus diana): The effects of polyspecific associations. Folia Primatologica, 88, 455–482.
Keppel, G., & Wickens, T. D. (2004). Design and analysis: A researcher’s handbook (4th ed.). Upper Saddle River, NJ: Prentice Hall.
Korstjens, A. H. (2001). The mob, the secret sorority, and the phantoms: An analysis of the socio-ecological strategies of the three colobines of Taï. Doctoral Dissertation. University of Utrecht.
McGraw, W. S. (1996). Cercopithecid locomotion, support use, and support availability in the Taï Forest, Ivory Coast. American Journal of Physical Anthropology, 100, 507–522.
McGraw, W. S., & Bshary, R. (2002). Association of terrestrial mangabeys (Cercocebus atys) with arboreal monkeys: Experimental evidence for the effects of reduced ground predator pressure on habitat use. International Journal of Primatology, 23, 311–325.
McGraw, W. S., & Zuberbühler, K. (2008). Socioecology, predation, and cognition in a community of west African monkeys. Evolutionary Anthropology, 17, 254–266.
McGraw, W. S., Zuberbühler, K., & Noë, R. (2007). Monkeys of the Taï Forest: An African primate community. Cambridge: Cambridge University Press.
Nakagawa, S., & Cuthill, I. C. (2007). Effect size, confidence interval, and statistical significance: A practical guide for biologists. Biological Reviews, 82, 591–605.
Noë, R., & Bshary, R. (1997). The formation of red colobus-Diana monkey associations under predation pressure from chimpanzees. Proceedings of the Royal Academy of Sciences B. Biological Sciences, 264, 253–259.
Norconk, M. A. (1990). Mechanisms promoting stability in mixed Saguinus mystax and Saguinus fuscicollis troops. American Journal of Primatology, 21, 159–170.
Oates, J. F., & Whitesides, G. H. (1990). Association between olive colobus (Procolobus verus), Diana guenons (Cercopithecus diana), and other forest monkeys in Sierra Leone. American Journal of Primatology, 21, 129–146.
Peres, C. A. (1992). Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and S. mystax. Behavioral Ecology and Sociobiology, 31, 339–347.
Porter, L. M., & Garber, P. A. (2007). Niche expansion of a cryptic primate, Callimico goeldii, while in mixed species troops. American Journal of Primatology, 69, 1340–1353.
Pulliam, H. R., & Caraco, T. (1984). Living in groups: Is there an optimal group size? In J. R. Krebs & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (pp. 122–147). London: Blackwell Scientific.
Shultz, S. (2001). Notes on interactions between monkeys and African crowned eagles in Taï National Park, Ivory Coast. Folia Primatologica, 72, 248–250.
Shultz, S. (2002). Population density, breeding chronology and diet of crowned eagles Stephanoaetus coronatus in Taï National Park, Ivory Coast. Ibis, 144, 135–138.
Shultz, S., Noë, R., McGraw, W. S., & Dunbar, R. I. M. (2004). A community-level evaluation of the impact of prey behavioral and ecological characteristics on predator diet composition. Proceedings of the Royal Society of London B: Biological Sciences, 271, 725–732.
Stanford, C. B. (1995). The influence of chimpanzee predation on group size and anti-predator behavior in red colobus monkeys. Animal Behavior, 49, 577–587.
Stanford, C. B. (2002). Avoiding predators: Expectations and evidence in primate antipredator behavior. International Journal of Primatology, 23, 741–757.
Stanford, C. B., Wallis, J., Matama, H., & Goodall, J. (1994). Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, 1982–1991. American Journal of Physical Anthropology, 94, 213–228.
Stensland, E., Angerbjörn, A., & Berggren, P. (2003). Mixed species groups in mammals. Mammalogy Review, 33, 205–223.
Stephan, C., & Zuberbühler, K. (2008). Predation increases acoustic complexity in primate alarm calls. Biology Letters, 4, 641–644.
Terborgh, J. (1990). Mixed flocks and polyspecific associations: Costs and benefits of mixed groups to birds and monkeys. American Journal of Primatology, 21, 87–100.
Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997). The primate community of the Lopé reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42, 1–24.
Wachter, B., Schabel, M., & Noë, R. (1997). Diet overlap and polyspecific associations of red colobus and Diana monkeys in the Taï National Park, Ivory Coast. Ethology, 103, 514–526.
Waser, P. M. (1982). Primate polyspecific associations: Do they occur by chance? Animal Behavior, 30, 1–8.
Waser, P. M. (1984). Chance and mixed-species associations. Behavioral Ecology and Sociobiology, 15, 197–202.
Whitesides, G. H. (1989). Interspecific associations of Diana monkeys, Cercopithecus diana, in Sierra Leone, West Africa: Biological significance or chance? Animal Behavior, 37, 760–776.
Whitesides, G. H., Oates, J. F., Green, S. M., & Kluberdanz, R. P. (1988). Estimating primate densities from transects in a west African rain forest: A comparison of techniques. Journal of Animal Ecology, 57, 345–367.
Zuberbühler, K., & Jenny, D. (2002). Leopard predation and primate evolution. Journal of Human Evolution, 43, 873–886.
Zuberbühler, K., Jenny, D., & Bshary, R. (1999). The predator deterrence function of primate alarm calls. Ethology, 105, 477–490.
Acknowledgments
This article was greatly improved by comments from the editor and three anonymous reviewers. We thank the skilled assistants of the Tai Monkey Project for their invaluable work during all phases of the project, particularly Ferdinand Bele. We are grateful to our funders, including the National Science Foundation, which funded the data collection for this study (BCS 0921770 and 0922429); Yerkes National Primate Research Center; and the Ohio State University Department of Anthropology. For permission to work in Tai National Park we thank the Ministere de l’Enseignement Superieur et de la Recherche Scientifique, Direction Generale de la Recherche Scientifique et de l’Innovation Technologie, and the Ministere de l’Environement, des Eaux et Forets, Office Ivorien de Parcs et Reserves. Finally, we thank the Centre Suisse de Recherche Scientifique for logistical assistance. W. S. McGraw oversaw data collection. E. E. Kane analyzed the data. E. E. Kane and W. S. McGraw wrote the manuscript.
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Kane, E.E., McGraw, W.S. Effects of Chimpanzee (Pan troglodytes) Hunting Seasonality and Red Colobus (Piliocolobus badius) Association on Diana Monkeys (Cercopithecus diana) in Taï National Park, Côte d’Ivoire. Int J Primatol 39, 532–546 (2018). https://doi.org/10.1007/s10764-018-0050-x
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DOI: https://doi.org/10.1007/s10764-018-0050-x