International Journal of Primatology

, Volume 18, Issue 4, pp 523–538 | Cite as

Seed Swallowing in Tamarins: Evidence of a Curative Function or Enhanced Foraging Efficiency?

  • P. A. Garber
  • U. Kitron


Nonhuman primates represent a major component of the frugivore biomass in several rain-forest communities. Although there is considerable evidence that prosimians, monkeys, and apes serve as dispersal agents for many tropical trees, little attention has been paid to the more basic questions of why certain species of primates swallow and void seeds, and what, if any, are the advantages to an animal of having a large, hard, bolus pass through its digestive tract. We examine patterns of fruit-eating and seed-swallowing in two species of free-ranging tamarins: Saguinus mystax and Saguinus geoffroyi. Fruits commonly eaten by tamarins contain large seeds surrounded by a fibrous and adhesive pulp or arilate seed coat. They generally swallow seeds and pulp together. Intact seeds are voided over a 1- to 3-h period. Measurements of 132 seeds naturally voided by Panamanian tamarins average 11.2 mm in length and 0.3 g. The greatest number of large seeds contained in the digestive tract of a single animal at one time was 13. In the case of moustached tamarins, we collected 220 seeds. Average seed length is 11.9 mm and average seed weight is 0.3 g. At the time of capture, one animal had 26 seeds in its digestive tract. In both tamarin species, there is evidence of sex-based differences in feeding behavior. Adult female moustached and Panamanian tamarins swallowed and voided seeds of larger size than adult males did. Seed size is positively correlated with pulp weight (p <. 001), therefore females were selecting food items with higher nutritional rewards than adult males did. Given their small body size and relatively short digestive tract, why do tamarins swallow such large seeds? Although several explanations are possible, we propose that the large number and size of undigested seeds continuously passing through the tamarin gut serve a curative role in mechanically dislodging and expelling intestinal parasites—Ancanthocephala (spiny-headed worms)—from their digestive tracts.

Saguinus mystax Saguinus geoffroyi parasites self-medication feeding behavior 


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  1. Appleton, C. C., and Henzi, S. P. (1993). Environmental correlates of gastro intestinalparasitism in montane and lowland baboons in Natal, South Africa. Int. J. Primatol. 14: 623–636.Google Scholar
  2. Brumpt, E., and Urbain, A. (1938). Épizootie vermineuse par acanthocéphales (Prosthenorchis)ayant sévi a la singerie du Museum de Paris. Ann. Parasil. Hum. Comp. 16: 289–300.Google Scholar
  3. Caine, N.G. (1993). Flexibility and cooperation as unifying themes in Saguinus socialorganization and behaviour: The role of predation pressure. In Rylands, A. B. (ed.), Marmosets and Tamarins: Systematics, Ecology and Behaviour, Oxford University Press, Oxford, pp. 200–219.Google Scholar
  4. Chapman, C. A. (1989). Primate seed dispersal: The fate of dispersed seeds. Biotropica 21: 148–154.Google Scholar
  5. Clarkson, T. B., Bullock, B. C., Lehner, N. D. M., and Manning, P. J. (1970). Diseases affectingthe usefulness of nonhuman primates for nutrition research. In Harris, R.S. (ed.), Feeding and Nutrition of Nonhuman Primates; Academic Press, New York, pp. 233–250.Google Scholar
  6. Clayton, D. H., and Wolfe, N. D. (1993). The adaptive significance of self-medication. Trends Ecol. Evol. 8: 60–63.Google Scholar
  7. Corlett, R. T., and Lucas, P. W. (1990). Alternative seed-handling strategies in primates: Seed-spitting by long-tailed macaques (Macaca fascicularis). Oecologia 82: 166–171.Google Scholar
  8. Cosgrove, G. E., Nelson, B., and Gengozian, N. (1968). Helminth parasites of the tamarin, Saguinus fuscicollis. Lab. Anim. Care 18: 654–655.Google Scholar
  9. Crompton, D. W. T. (1970). An Ecological Approach to Acanthocephalan Physiology, Cambridge University Press, Cambridge.Google Scholar
  10. Dawson, G. A. (1976). Behavioral Ecology of the Panamanian Tamarin, Saguinus Oedipus Callitrichidae, Primates), Ph.D. thesis, Michigan State University, East Lansing.Google Scholar
  11. Dunn, F. L. (1963). Acanthocephalans and cestodes of South American monkeys and marmosets. J. Parasitol. 49: 717–722.Google Scholar
  12. Epple, G. (1970). Maintenance, breeding, and development of marmoset monkeys (Callitrichidae) in captivity. Folia Primatol. 12: 56–76.Google Scholar
  13. Estrada, A., and Coates-Estrada, R. (1984). Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxlas, Mexico. Am. J. Primatol. 7: 3–13.Google Scholar
  14. Ferrari, S. F., and Martins, E. S. (1992). Gummivory and gut morphology in two sympatric callitrichids (Callithrix emiliae and Saguinus fuscicollis weddelli) from Western Brazilian Amazonia. Am. J. Phys. Anthropol. 88: 97–103.Google Scholar
  15. Ferrari, S. F., Lopes, M. A., and Krause, E. A. K. (1993). Gut morphology of Callithrix nigriceps and Saguinus labiatus from Western Brazilian Amazonia. Am. J. Phys. Anthropol. 90: 487–493.Google Scholar
  16. Garber, P. A. (1986). The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). Am. J. Primatol. 10: 155–170.Google Scholar
  17. Garber, P. A. (1992). Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichidae. Am. J. Phys. Anthropol. 88: 69–482.Google Scholar
  18. Garber, P. A. (1993). Feeding ecology and behaviour of the genus Saguinus. In Rylands, A. B. (ed.), Marmosets and Tamarins: Systematics, Ecology and Behaviour, Oxford University Press, Oxford, pp. 273–295.Google Scholar
  19. Garber, P. A. (1994). Aspects of fruit eating and seed dispersal in Panamanian (Saguinus geoffroyi) and moustached tamarins (Saguinus mystax). 1994 Reg. Conf. Proc. Am. Zoo. Aquar. Assoc., pp. 364–369.Google Scholar
  20. Garber, P. A. (1997). One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy. Evol. Anthropol. (in press).Google Scholar
  21. Garber, P. A., and Preutz, J. D. (1995). Positional behavior in moustached tamarin monkeys: Effects of habitat on locomotor variability and stability. J. Hum. Evol. 28: 411–426.Google Scholar
  22. Garber, P. A., Encarnación, F., Moya, L., and Preutz, J. D. (1993). Demography, dispersal, and patterns of mating in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems. Am. J. Primatol. 29: 235–254.Google Scholar
  23. Gautier-Hion, A., Duplantier, J.-M, Quris, R., Feer, F., Sourd, C., Decoux, J.-P., Dubost, G., Emmons, L., Erard, C., Hecketsweiler, P., Roussilhon, C., and Thiollay, J.-M. (1995). Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324–337.Google Scholar
  24. Hampton, J. K., Hampton, S. H., and Landwehr, B. T. (1966). Observations on a successful breeding colony of the marmoset, Oedipomidas oedipus. Folia Primatol. 4: 265–287.Google Scholar
  25. Hershkovitz, P.H. (1977). Living New World Monkeys (Platyrrhini), Vol. 1, University of Chicago Press, Chicago.Google Scholar
  26. Hladik, A., and Hladik, C. M. (1969). Rapports trophiques entre vegetation et primates dans le foret de Barro Colorado (Panama). Terre Vie 116: 25–117.Google Scholar
  27. Howe, H. F. (1982). Fruit production and animal activity in two tropical trees. In Leigh, E. G., Rand, A. S., and Windsor, D.M. (eds.), The Ecology of a Tropical Forest: Seasonal Rhythms and Long-Term Changes, Smithsonian Institution Press, Washington, DC, pp. 189–199.Google Scholar
  28. Howe, H. F., and Smallwood, J. (1982). Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13: 201–228.Google Scholar
  29. Huffman, M. A., and Wrangham, R. W. (1994). Diversity of medicinal plant use by chimpanzees in the wild. In Wrangham, R. W., McGrew, W. C., de Wall, F. B. M., and Heltne, P. G. (eds.), Chimpanzee Cultures, Harvard University Press, Cambridge, MA, pp. 129–148.Google Scholar
  30. Hunt, R. D., Anderson, M. P., and Chalifoux, L. V. (1978). Spontaneous infectious diseases of marmosets. Primates Med. 10: 239–253.Google Scholar
  31. Janzen, D. H. (1978). Complications in interpreting the chemical defenses of trees against tropical arboreal plant-eating vertebrates. In Montgomery, G. G. (ed.), The Ecology of Arboreal Folivores, Smithsonian Institution Press, Washington, DC, pp. 73–84.Google Scholar
  32. Kim, J. C. S., and Wolf, R. H. (1980). Diseases of moustached marmosets. In Montali, R.J., and Migaki, G. (eds.), The Comparative Pathology of Zoo Animals, Smithsonian Institution Press, Washington, DC, pp. 431–436.Google Scholar
  33. Lambert, J. E. (1995). Feeding behavior of common chimpanzees and redtail monkeys: Seed dispersal in the Kibale Forest, Uganda. Am. J. Phys. Anthropol. (Suppl.) 20: 128.Google Scholar
  34. Lieberman, D., Hall, J. B., Swaine, M. D., and Leiberman, M. (1979). Seed dispersal by baboons in the Sha Hills, Ghana. Ecology 60: 65–75.Google Scholar
  35. Nelson, B., Cosgrove, G. E., and Gengozian, N. (1966). Diseases of an imported primate Tamarinus nigricollis. Lab. Anim. Care 16: 255–275.Google Scholar
  36. Page, J. E., Balza, F. F., Nishida, T., and Towers, G. H. N. (1992). Biologically active diterpenes from Aspilia mossambicensis, a chimpanzee medicinal plant. Phytochemistry 31: 3437–3439.Google Scholar
  37. Phillips-Conroy, J. E. (1986). Baboons, diet, and disease: Food plant selection and schistosomiasis. In Taub, D. M., and King, F. A. (eds.), Current Perspectives in Primate Social Dynamics, Van Nostrand Reinhold, New York, pp. 287–304.Google Scholar
  38. Rand, S. A., and Rand, W. M. (1982). Variation in rainfall on Barro Colorado Island. In Leigh, E. G., Rand, A. S., and Windsor, D. M. (eds.), The Ecology of a Tropical Forest: Seasonal Rhythms and Long-term Changes, Smithsonian Institution Press, Washington, DC, pp. 47–59.Google Scholar
  39. Rodgers, M. E., Williamson, E. A., Fernandez, M., and Tutin, C. E. G. (1990). The diet of gorillas in the Lopé Reserve, Gabon: A nutritional analysis. Oecologia 84: 326–339.Google Scholar
  40. Rodman, P. S. (1988). Diversity and consistency in ecology and behavior. In Schwartz, J. H. (ed.), Orang-utan Biology, Oxford University Press, Oxford, pp. 31–51.Google Scholar
  41. Rowell, T. E., and Mitchell, B. J. (1991). Comparison of seed dispersal by guenons in Kenya and capuchins in Panama. J. Trop. Ecol. 7: 269–274.Google Scholar
  42. Schmidt, G. D. (1972). Acanthocephala of captive primates. In Fiennes, R. N. T.-W. (ed.), Pathology of Simian Primates, Part II, S. Karger, Basel, pp. 144–156.Google Scholar
  43. Schmidt, G. D., and Roberts, L. S. (1981). Foundations of Parasitology, 2nd ed. Mosby, St. Louis.Google Scholar
  44. Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. In Fleming, T. H., and Estrada, A. (eds.), Frugivory and Seed Dispersal: Ecological and Evolutionary Aspects, Kluwer Academic, Dordrecht, pp. 15–29.Google Scholar
  45. Snowdon, C. T., and Soini, P. (1988). The tamarins, genus Saguinus. In Mittermeier, R. A., Rylands, A. B., Coimbra-Filho, A., and Fonseca, G. A. B. (eds.), Ecology and Behavior of Neotropical Primates, Vol. 2, World Wildlife Fund, Washington, DC, pp 223–298.Google Scholar
  46. Stuart, M. D., and Strier, K. (1995). Primates and parasites: A case for a multidisciplinary approach. Int. J. Primatol. 16: 577–594.Google Scholar
  47. Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology, Princeton University Press, Princeton, NJ.Google Scholar
  48. Terborgh, J. (1986). Community aspects of frugivory in tropical forests. In Estrada, A., and Fleming, T. H. (eds.), Frugivores and Seed Dispersal, Dr. W. Junk, Dordrecht, pp. 371–384.Google Scholar
  49. Thatcher, V. E., and Porter, J. A. (1968). Some helminth parasites of Panamanian primates. Trans. Am. Microsc. Soc. 87: 186–196.Google Scholar
  50. Tutin, C. E. G., Williamson, E. A., Rogers, M. E., and Fernandez, M. (1991). A case study of a plant-animal relationship: Cola lizae and lowland gorillas in the Lopé Reserve, Gabon. J. Trop. Ecol. 7: 181–199.Google Scholar
  51. van Cleave, H. J. (1953). Acanthocephala of North American Mammals. Ill. Biol. Monogr. 23: 1–179.Google Scholar
  52. van Roosmalen, M. G. M (1985). Habitat preferences, diet, feeding strategy and social organization of the black spider monkeys (Ateles paniscus paniscus Linnaeus 1758) in Suriman. Acta Amazon. 15: 1–238.Google Scholar
  53. Wrangham, R. W. (1995). Relationship of chimpanzee leaf-swallowing to a tapeworm infection. Am. J. Primatol. 37: 297–303.Google Scholar
  54. Wrangham, R. W., Chapman, C. A., and Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. J. Trop. Ecol. 10: 355–368.Google Scholar

Copyright information

© Plenum Publishing Corporation 1997

Authors and Affiliations

  • P. A. Garber
    • 1
  • U. Kitron
    • 2
  1. 1.Department of AnthropologyUniversity of IllinoisUrbana
  2. 2.College of Veterinary MedicineUniversity of IllinoisUrbana

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