Polyspecific associations (PSA) occur when 2 or more species maintain proximity or coordinate activities. PSA may provide ecological benefits similar to those of monospecific groups, i.e., protection against predation and improved foraging efficiency, but may also impart costs, such as feeding competition. I studied 3 New World Callitrichidae—Callimico goeldii, Saguinus fuscicollis, and S. labiatus—in northwestern Brazil over 18 mo between April 1999 and August 2003, during which single primary study groups of C. goeldii, S. labiatus, and S. fuscicollis consistently associated with one another. I compared patterns of PSA participation to variation in plant diets during wet and dry seasons. All 3 species associated an average 61% of observation time, but with significant seasonal variation in PSA. During the dry season, April–September, PSA occurred significantly less frequently than during the wet season, October–March (37% vs. 88%). The variation in PSA corresponded with seasonal shifts in plant food diets, resulting in less dietary overlap among all 3 species during the dry season, particularly between Callimico goeldii and Saguinus labiatus. Dietary richness, diversity, and evenness were also lower in the dry compared to the wet season for each species. The results suggest a link between PSA participation and diet among the taxa; foraging-related costs or feeding competition may constrain PSA during the dry season.
Similar content being viewed by others
REFERENCES
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour 49: 227–267.
Berner, T. O., and Grubb, T. C. (1985). An experimental analysis of mixed-species flocking in birds of deciduous woodland. Ecology 66: 1229–1236.
Bicca-Marques, J. C. (2000). Cognitive Aspects of Within-Patch Foraging Decisions in Wild Diurnal and Nocturnal New World Monkeys. Ph.D. Dissertation, University of Illinois, Urbana–Champaign.
Buchanan-Smith, H. (1990). Polyspecific association of two tamarin species, Saguinus labiatus and Saguinus fuscicollis, in Bolivia. Am. J. Primatol. 22: 205–214.
Buchanan-Smith, H. M. (1999). Tamarin polyspecific associations: Forest utilization and stability of mixed-species groups. Primates 40: 233–247.
Caldwell, G. S. (1981). Attraction to tropical mixed-species heron flocks: Proximate mechanism and consequences. Behav. Ecol. Sociobiol. 8: 99–103.
Castro, N. R. C. (1991). Behavioral Ecology of Two Coexisting Tamarin Species (Saguinus fuscicollis nigrifrons and Saguinus mystax mystax, Callitrichidae, Primates) in Amazonian Peru. Ph.D. Dissertation, Washington University, St. Louis.
Chapman, C. A., and Chapman, L. J. (1996). Mixed-species primate groups in the Kibale Forest: Ecological constraints on association. Int. J. Primatol. 17: 31–50.
Chapman, C. A., and Chapman, L. J. (2000a). Interdemic variation in mixed-species association patterns: Common diurnal primates of Kibale National Park, Uganda. Behav. Ecol. Sociobiol. 47: 129–139.
Chapman, C. A., and Chapman, L. J. (2000b). Determinants of group size in primates: The importance of travel costs. In Boinski, S., and Garber, P. A. (eds.), On the Move. University of Chicago Press, Chicago, pp. 24–42.
Chapman, C. A., Chapman, L. J., Wrangham, R. W., Hunt, K., Gebo, D., and Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica 24: 527–531.
Chapman, C. A., Wrangham, R. W., and Chapman, L. J. (1994). Indices of habitat-wide fruit abundance in tropical forests. Biotropica 26: 160–171.
Chapman, C. A., Wrangham, R. W., and Chapman, L. J. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behav. Ecol. Sociobiol. 36: 59–70.
Chapman, C. A., Wrangham, R. W., Chapman, L. J., Kennard, D. K., and Zanne, A. E. (1999). Fruit and flower phenology at two sites in Kibale National Park, Uganda. J. Trop. Ecol. 15: 189–211.
Cheney, D. (1987). Interactions and relationships between groups. In Smuts, B. B., Cheney, D. L., Seyfarth, F. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies. University of Chicago Press, Chicago, pp. 267–281.
Cheney, D., Seyfarth, R., and Smuts, B. (1986). Social relationships and social cognition in nonhuman primates. Science 234: 1361–1366.
Cole, L. C. (1949). The measurement of interspecific association. Ecology 30: 411–424.
Cords, M. (1987). Mixed-species associations of Cercopithecus monkeys in the Kakamega Forest, Kenya. U. Calif. Publ. Zool. 117: 1–109.
Cords, M. (1990). Mixed-species association of East African guenons: General patterns or specific examples? Am. J. Primatol. 21: 101–114.
Cords, M. (2000). Mixed-species association and group movement. In Boinski, S., and Garber, P. A. (eds.), On the Move. University of Chicago Press, Chicago, pp. 73–99.
Crandlemire-Sacco, J. (1986). The Ecology of the Saddle-Backed Tamarin, Saguinus fuscicollis, of Southeastern Peru. Ph.D. Dissertation, University of Pittsburgh.
Crowley, P. H. (1992). Resampling methods for computation-intensive data analysis in ecology and evolution. Annu. Rev. Evol. Systemat. 23: 405–447.
Dagosto, M. (1994). Testing positional behavior of Malagasy lemurs: A randomization approach. Am. J. Phys. Anthropol. 94: 189–202.
Dawson, G. A. (1977). Composition and stability of social groups of the tamarin, Saguinus oedipus geoffroyi, in Panama: Ecological and behavioral implications. In Kleiman, D. G. (ed.), The Biology and Conservation of the Callitrichidae. Smithsonian Institution Press, Washington, DC, pp. 23–37.
Dolby, A. S., and Grubb, T. C. Jr. (2000). Social context affects risk taking by a satellite species in a mixed-species foraging group. Behav. Ecol. 11: 110–114.
Dunbar, R. I. M. (1994). Ecological constraints on group size in baboons. In Animal Societies: Individuals Interactions, and Organisation. Kyoto University Press, Kyoto, pp. 221–236.
Eckardt, W., and Zuberbühler, K. (2004). Cooperation and competition in two forest monkeys. Behav. Ecol. 15: 400–411.
Edgington, E. S. (1980). Randomization Tests. Marcel Dekker, New York.
Fragaszy, D. M., and Visalberghi, E. (1996). Social learning in monkeys: Primate “primacy” reconsidered. In Heyes, C. M., and Galef, B. G. Jr, (eds.), Social Learning in Animals: The Roots of Culture. Academic Press, London, pp. 65–84.
Garber, P. A. (1988). Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour 105: 18–33.
Garber, P. A. (1993). Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability versus variability. Int. J. Primatol. 14: 145–166.
Garber, P. A., and Leigh, S. R. (2001). Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil. Am. J. Primatol. 54: 17–31.
Garber, P. A., Pruetz, J. D., and Isaacson, J. (1993). Patterns of range use, range defense, and intergroup spacing in moustached tamarin monkeys (Saguinus mystax). Primates 34: 11–25.
Gartlan, J. S., and Struhsaker, T. T. (1972). Polyspecific associations and niche separation of rain-forest anthropoids in Cameroon, West Africa. J. Zool. Lond. 168: 221–266.
Gautier-Hion, A., Quris, R., and Gautier, J. P. (1983). Monospecific vs polyspecific life: A comparative study of foraging and antipredatory tactics in a community of Cercopithecus monkeys. Behav. Ecol. Sociobiol. 12: 325–335.
Gillespie, T. R., and Chapman, C. A. (2001). Determinants of group size in the red colobus monkey (Procolobus badius): An evaluation of the generality of the ecological-constraints model. Behav. Ecol. Sociobiol. 50: 329–338.
Giraldeau, L. A. (1988). The stable group and the determinants of foraging group size. In Slobodchikoff, C. N. (ed.), The Ecology of Social Behavior. Academic Press, London, pp. 33–54.
Goldizen, A. W., Terborgh, J., Cornejo, F., Porras, D. T., and Evans, R. (1988). Seasonal food shortage, weight loss, and the timing of births in saddle-back tamarins (Saguinus fuscicollis). J. Anim. Ecol. 57: 893–901.
Hanson, A. M. (2000). Habitat Use in Relation to Diet, with Particular Emphasis on Mycophagy, by Callimico goeldii in Pando, Bolivia. Master's Thesis. SUNY—Stony Brook.
Hershkovitz, P. (1977). Living New World Monkeys (Platyrrhini), Vol. 1. University of Chicago Press, Chicago.
Heymann, E. W. (1990). Interspecific relations in a mixed-species troop of moustached tamarins, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis (Platyrrhini: Callitrichidae), at the Rio Blanco, Peruvian Amazonia. Am. J. Primatol. 21: 115–127.
Heymann, E. W. (1997). The relationship between body size and mixed-species troops of tamarins (Saguinus spp.). Folia Primatol. 68: 287–295.
IMAC – Núcleo de Cartografia (Rio Branco, AC). (1991). Atlas Geográfico Ambiental do Acre. Rio Branco, AC.
Janson, C. H., and Goldsmith, M. L. (1995). Predicting group size in primates: Foraging costs and predation risks. Behav. Ecol. 6: 326–336.
Lehner, P. N. (1979). Handbook of Ethological Methods. Garland STPM Press, New York.
Margalef, R. (1958). Information theory in ecology. Genet. Syst. 3: 36–71.
Morse, D. H. (1977). Feeding behavior and predator avoidance in heterospecific groups. Bioscience 27: 332–339.
Munn, C. A., and Terborgh, J. W. (1979). Multi-species territoriality in Neotropical foraging flocks. Condor 81: 338–347.
NCDC. Monthly climatic data for the world [database online]. Available from NNDC Climate Data Online, National Climatic Data Center. <http://ncdc.noaa.gov/oa/ncdc.html>
Noë, R., and Bshary, R. (1997). The formation of red colobus-diana monkey associations under predation pressure from chimpanzees. Proc. Roy. Soc. Lond. 264: 253–259.
Norconk, M. A. (1986). Interactions Between Primate Species in a Neotropical Forest: Mixed-Species Troops of Saguinus mystax and Saguinus fuscicollis (Callitrichidae). Ph.D. Dissertation, University of California, Los Angeles.
Norconk, M. A. (1990). Mechanisms promoting stability in mixed Saguinus mystax and S. fuscicollis troops. Am. J. Primatol. 21: 159–170.
Oates, J. F., and Whitesides, G. H. (1990). Association between olive colobus (Procolobus verus), Diana guenons (Cercopithecus diana), and other forest monkeys in Sierra Leone. Am. J. Primatol. 21: 129–146.
Peres, C. A. (1992a). Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and S. mystax. Behav. Ecol. Sociobiol. 31: 339–347.
Peres, C. A. (1992b). Consequences of joint territoriality in a mixed-species group of tamarin monkeys. Behaviour 123: 220–246.
Peres, C. A. (1993a). Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest. J. Zool. Lond. 230: 567–592.
Peres, C. A. (1993b). Anti-predation benefits in a mixed-species group of Amazonian tamarins. Folia Primatol. 61: 61–76.
Peres, C. A. (1996). Food patch structure and plant resource partitioning in interspecific associations of Amazonian tamarins. Int. J. Primatol. 17: 695–723.
Pielou, E. (1977). Mathematical Ecology. John Wiley & Sons, New York.
Podolsky, R. D. (1990). Effects of mixed-species association on resource use by Saimiri sciureus and Cebus apella. Am. J. Primatol. 21: 147–158.
Pook, A. G., and Pook, G. (1982). Polyspecific association between Saguinus fuscicollis, Saguinus labiatus, Callimico goeldii and other primates in North-western Bolivia. Folia Primatol. 38: 196–216.
Porter, L. M. (2000). The Behavior and Ecology of the Goeldi's Monkey (Callimico goeldii) in Northern Bolivia. Ph.D. Dissertation, SUNY—Stony Brook.
Porter, L. M. (2001a). Dietary differences among sympatric callitrichines in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and Saguinus labiatus. Int. J. Primatol. 22: 961–992.
Porter, L. M. (2001b). Benefits of polyspecific associations for the Goeldi's monkey, Callimico goeldii. Am. J. Primatol. 54: 143–158.
Potvin, C., and Roff, D. A. (1993). Distribution-free and robust statistical methods: Viable alternatives to parametric statistics? Ecology 74: 1617–1628.
Poulson, B. O. (1995). Relationship between frequency of mixed-species flocks, weather and insect activity in a montane cloud forest in Ecuador. Ibis 138: 466–470.
Ramirez, M. M. (1989). Feeding Ecology and Demography of the Moustached Tamarin Saguinus mystax in Northeastern Peru. Ph.D. Dissertation, City University of New York.
Rehg, J. A. (2003). Polyspecific Associations of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in Acre, Brazil. Ph.D. Dissertation, University of Illinois–Urbana-Champaign.
Robertson, D. R., Sweatman, H. P. A., Fletcher, E. A., and Cleland, M.G. (1976). Schooling as a mechanism for circumventing the territoriality of competitors. Ecology 57: 1208–1220.
Sauther, M. L. (2002). Group size effects on predation sensitive foraging in wild ring-tailed lemurs (Lemur catta). In Miller, L. E. (ed.), Eat or Be Eaten. Cambridge University Press, Cambridge, UK, pp. 107–125.
Stensland, E., Angerbjorn, A., and Berggren, P. (2003). Mixed species groups in mammals. Mammal Rev. 33: 205–223.
Stevenson, P. R., Quiñones, M. J., and Ahumada, J. A. (1998). Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. Int. J. Primatol. 19: 313–324.
Struhsaker, T. T. (1981). Polyspecific associations among tropical rain-forest primates. Zeit. Tierpsychol. 57: 268–304.
Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology. Princeton University Press, Princeton, NJ.
Terborgh, J. (1990). Mixed flocks and polyspecific associations: Costs and benefits of mixed groups to birds and monkeys. Am. J. Primatol. 21: 87–100.
Thompson, D. B. A., and Barnard, C. J. (1983). Anti-predator responses in mixed-species associations of lapwings, golden plovers and black-headed gulls. Anim. Behav. 31: 585–593.
Vadas, R. L. (1990). Competitive exclusion, character convergence, or optimal foraging: Which should we expect? Oikos 58: 123–128.
van Schaik, C. P. (1983). Why are diurnal primates living in groups? Behaviour 87: 120–143.
van Schaik, C. P., and van Hooff, J. A. R. A. M. (1983). Why are diurnal primates living in groups? Behaviour 87: 120–143.
Vos, D. R., Karssemeijer, G. J., and van Hooff, J. A. R. A. M. (1992). Ecological constraints on the behaviour of mother long-tailed macaques (Macaca fascicularis). Behav. Ecol. Sociobiol. 31: 385–391.
Waite, S. (2000). Statistical Ecology in Practice. Pearson Education Limited, Harlow, England.
Waser, P. M. (1980). Polyspecific associations of Cercocebus albigena: Geographic variation and ecological correlates. Folia Primatol. 33: 57–76.
Waser, P. M. (1982). Primate polyspecific associations: Do they occur by chance? Anim. Behav. 30: 1–8.
Waser, P. M. (1984). “Chance” and mixed-species associations. Behav. Ecol. Sociobiol. 15: 197–202.
Waser, P. M. (1987). Interactions among primate species. In Smuts, B. B., Cheney, D. L., Seyfarth, F. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies. University of Chicago Press, Chicago, pp. 210–226.
Whitten, P. L. (1988). Effects of patch size and feeding subgroup size on feeding success in vervet monkeys (Cercopithecus aethiops). Behaviour 105: 35–52.
Wiley, R. H. (1980). Multispecies antbird societies in lowland forests of Surinam and Ecuador: Stable membership and foraging differences. J. Zool. Lond. 191: 127–145.
Windfelder, T. L. (1997). Polyspecific Association and Interspecific Communication Between Two Neotropical Primates: Saddle-Back Tamarins (Saguinus fuscicollis) and Emperor Tamarins (Saguinus imperator). Ph.D. Dissertation, Duke University.
Wolda, H. (1981). Similarity indices, sample size and diversity. Oecologia 50: 296–302.
Wolf, N. G. (1985). Odd fish abandon mixed-species groups when threatened. Behav. Ecol. Sociobiol. 17: 47–52.
Wrangham, R. W. (1987). Evolution of social structure. In Smuts, B. B., Cheney, D. L., Seyfarth, F. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies. University of Chicago Press, Chicago, pp. 282–296.
Zoneamento Ecológico-Econômico do Acre (ZEE). Documento Final - 1° Fase, Volume I. (2000). Recursos Naturais e Meio Ambiente. Governo do Estado do Acre; Secretaria de Estado de Planejamento e Coordenação; Secretaria de Estado de Ciência, Tecnologia e Meio Ambiente. Rio Branco, AC.
ACKNOWLEDGMENTS
I thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Universidade Federal do Acre (UFAC) for granting me permission to conduct the research and to work at the Fazenda Experimental Catuaba. I also thank all the researchers, administrators, and technicians of the Universidade Federal do Acre and the Herbário do Parque Zoobotânico for their help, and in particular, Marco Antônio de Oliveira, Armando Muniz Calouro, and Maria Aparecida de Oliveira Azevedo Lopes. I also thank 2 anonymous reviewers of the manuscript for many helpful comments and suggestions. The Graduate College of the University of Illinois in part funded the research.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rehg, J.A. Seasonal Variation in Polyspecific Associations Among Callimico goeldii, Saguinus labiatus, and S. fuscicollis in Acre, Brazil. Int J Primatol 27, 1399–1428 (2006). https://doi.org/10.1007/s10764-006-9076-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-006-9076-6