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Exudativory in Primates: Interspecific Patterns

  • Andrew C. Smith
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

This chapter reviews the extent of primate gummivory, identifies phylogentic patterns in the degree of gummivory across primates, and examines overlap in the plant species whose exudates are consumed. Plant exudates are exploited both routinely and opportunistically by at least 69 species of strepsirrhine, platyrrhine, and catarrhine primates. Gummivory is particularly prevalent among the callitrichids, cheirogaleids, and galagos in terms of the number of species reported to consume gum, its contribution to their diet, and the number of plant species they exploit for it. While some marmosets, galagos and the fork-marked lemur are thought of as gum specialists, exudates may account for more than 10% of the diet in many other species. Gum feeding may increase further during periods of dry season resource scarcity with some, most notably Parkia pod gums, acting as a keystone resource for many New World monkeys. Exudates from at least 250 plant species in 170 genera and 63 families are eaten, with Fabaceae and Anacardiaceae being the most frequently exploited. The Callitrichidae were examined for patterns in the amount of gum they consumed. Differences in the prevalence of gummivory were linked to morphological adaptations, particularly dentition, and habitat seasonality. Cluster analysis of the plant families exploited by different primate genera revealed similarities based on the number of families they exploited for gums.

Keywords

Plant Family Mouse Lemur Lion Tamarin Grey Mouse Lemur Yellow Baboon 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

I thank Dr Anne Burrows for inviting me to participate in the symposium on the evolution of exudativory in primates at the XXIIth Congress of the International Primatological Society. This chapter benefited from Anne’s comments and those of Leanne Nash and two anonymous reviewers. Dr Philip Pugh conducted the cluster analysis and provided comments on an early draft of this manuscript. Financial support was provided by Anglia Ruskin University’s Animal and Environmental Research Group and Central Sabbatical Scheme.

References

  1. Adrian J, Assoumani M (1983) Gums and hydrocolloids in nutrition. In Reicheigl M (ed) CRC handbook of nutritional supplements: Vol. II agricultural use CRC Press, Boca RotanGoogle Scholar
  2. Albernaz ALKM (1997) Home range size and habitat use in the black lion tamarin (Leontopithecus chrysopygus). Int J Primatol 18: 877–887CrossRefGoogle Scholar
  3. Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, ChicagoGoogle Scholar
  4. Anderson DMW, de Pinto LG (1985) Gum polysaccharides from three Parkia species. Phytochemistry 24: 77–79CrossRefGoogle Scholar
  5. anon (2008) http://www.tropicos.org/ Missouri Botanical Garden
  6. Bearder SK, Martin RD (1980) Acacia gum and its use by lesser bushbabies, Galago senegalensis (Primates; Lorisidae). Int J Primatol 1: 103–128CrossRefGoogle Scholar
  7. Bentley-Condit VK (2009) Food choices and habitat use by the Tana River yellow baboons (Papio cynocephalus): a preliminary report on five years of data. Am J Primatol 71: 432–436PubMedCrossRefGoogle Scholar
  8. Biebouw K (2009) Home range size and use in Allocebus trichotis in Analamazaotra Special Reserve, Central Eastern Madagascar. Int J Primatol 30: 367–386CrossRefGoogle Scholar
  9. Bonvicino CR (1989) Ecologia e comportamento de Alouatta belzebul (Primates: Cebidae) na mata atlântica. Rev Nordestina Biol 6: 149–179Google Scholar
  10. Brandon-Jones D, Eudey AA, Geissmann T, Groves CP, Melnick DJ, Morales JC, Shekelle M, Stewart C-B (2004) Asian primate classification. Int J Primatol 23: 97–164CrossRefGoogle Scholar
  11. Buchanan-Smith HM (1991) A field study on the red-bellied tamarin, Saguinus l. labiatus, in Bolivia. Int J Primatol 12: 259–276CrossRefGoogle Scholar
  12. Burrows AM, Smith TD (2005) Three-dimesional analysis of mandibular morphology in Otolemur. Am J Phys Anthropol 127: 219–230PubMedCrossRefGoogle Scholar
  13. Carvalho CT, Carvalho CF (1989) A organização social dos savins-pretos, Leontopithecus chrysopygus (Mikan, 1823), Na reserva em Teodoro Sampaio, São Paulo (Primates, Callitrichidae). Rev Bras Zool 6: 707–717CrossRefGoogle Scholar
  14. Castro NR (1991) Behavioural ecology of two co-existing tamarin species (Saguinus fuscicolis nigrifrons and Saguinus mystax mystax, Callitrichidae, Primates) in Amazonian Peru. PhD thesis, Washington University, St. LouisGoogle Scholar
  15. Chapman CA, Chapman LJ, Cords M, Gauthua M, Gautier-Hion A, Lambert JE, Rode KD, Tutin CEG, White LTJ (2002) Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. In Glenn M, Cords M (eds) The guenons: Diversity and adaptation in African monkeys. Plenum Press, New YorkGoogle Scholar
  16. Charles-Dominique P (1977) Ecology and behaviour of nocturnal primates. Columbia University Press, New YorkGoogle Scholar
  17. Charles-Dominique P, Bearder SK (1979) Field studies of lorisid behaviour: methodological aspects. In GA Doyle, Martin RD (eds) The study of prosimian behavior Academic Press, New YorkGoogle Scholar
  18. Charles-Dominique P, Hladik CM (1971) Le Lepilemur du Sud de Madagascar: ecologie, alimentation et vie sociale. Terre Vie 25: 3–66Google Scholar
  19. Charles-Dominique P, Petter JJ (1980) Ecology and social life of Phaner furcifer. In Charles-Dominique P, Coper HM, Hladik CM, Petter J-J, Peter-Rousseaux A (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour Academic Press, New YorkGoogle Scholar
  20. Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166: 337–386PubMedCrossRefGoogle Scholar
  21. Clark AB (1978) Olfactory communication, Galago crassicaudatus, and the social life of prosimians. In Chivers DJ, Lane-Petter W (eds) Recent advances in primatology Academic Press, LondonGoogle Scholar
  22. Coimbra-Filho AF, Aldrighi AD, Martins HF (1973) Nova contribuição ao restabelecimento da fauna do Parque Nacional de Tijuca. Bras Florestal 4: 7–25Google Scholar
  23. Coimbra-Filho AF, Da Cruz Rocha N, Pissinatti A (1980) Morfofisiologia de ceco e sua correlacao com o tipo odontologico em Callitrichidae (Platyrrhini, Primates). Rev Bras Biol 40: 177–185PubMedGoogle Scholar
  24. Coimbra-Filho AF, Mittermeier RA (1976) Exudate-eating and tree-gouging in marmosets. Nature 262: 630CrossRefGoogle Scholar
  25. Coimbra-Filho AF, Mittermeier RA (1977) Exudate-eating, and the “short-tusked” condition in Callithrix and Cebuella. In Kleiman DG (ed) The biology and conservation of the Callitrichdae Smithsonain Institution Press, Washington, DCGoogle Scholar
  26. Coimbra-Filho AF, Mittermeier RA, Constable ID (1981) Callithrix flaviceps (Thomas, 1903) recorded from Minas Gerais, Brazil (Callitrichidae, Primates). Rev Bras Biol 41: 141–147Google Scholar
  27. Cords M (1986) Interspecific and intraspecific variation in the diet of two forest guenons, Cercopithecus ascanius and Cercopithecus mitis. J Anim Ecol 55: 811–827CrossRefGoogle Scholar
  28. Corrêa HKM, Coutinho PEG, Ferrari SF (2000) Between-year differences in the feeding ecology of highland marmosets (Callithrix aurita and Callithrix flaviceps) in south-eastern Brazil. J Zool (Lond) 252: 421–427Google Scholar
  29. Crompton RH (1984) Foraging, habitat structure and locomotion of two species of Galago. In Cant JGH, Rodman PS (eds) Adaptations for foraging in non-human primates Columbia University Press, New YorkGoogle Scholar
  30. Dammhahn M, Kappeler PM (2008b) Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29: 1567–1589CrossRefGoogle Scholar
  31. Dammhahn M, Kappeler PM (2008a) Small-scale coexistence of two mouse lemur species (Microcebus berthae and M. murinus) within a homogeneous competitive environment. Oecologia 157: 473–483PubMedCrossRefGoogle Scholar
  32. Defler TR, Defler SB (1996) The diet of a group of woolly monkeys (Lagothrix lagothricha lagothricha) in southeastern Colombia. Int J Primatol 17: 161–190CrossRefGoogle Scholar
  33. Dietz JM, Peres CA, Pinder L (1997) Foraging ecology and the use of space in wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol 41: 289–305PubMedCrossRefGoogle Scholar
  34. Doyle GA, Bearder SK (1977) The galagines of South Africa. In Rainier III (Grimaldi) Prince of Monaco, Bourne GH (eds) Primate conservation Academic Press, New YorkGoogle Scholar
  35. Egler SG (1992) Feeding ecology of Saguinus bicolor bicolor (Callitrichidae: Primates) in a relict forest in Manaus, Brazilian Amazon. Folia Primatol 59: 61–76PubMedCrossRefGoogle Scholar
  36. Ferrari SF (1988) The behaviour and ecology of the buffy-headed marmoset Callithrix flaviceps (O. Thomas 1903). PhD thesis, University College London, LondonGoogle Scholar
  37. Ferrari SF (1993) Ecological differentiation in the Callitrichidae. In Rylands AB (ed) Marmosets and tamarins: systematics, ecology and behaviour Oxford University Press, OxfordGoogle Scholar
  38. Ferrari SF, Corrêa HKM, Coutinho PEG (1996) Ecology of the “Southern” marmosets (Callithrix aurita and Callithrix flaviceps). In Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of neotropical primates Plenum Press, New YorkCrossRefGoogle Scholar
  39. Ferrari SF, Digby L (1996) Wild Callithrix groups: stable extended families? Am J Primatol 38: 19–27CrossRefGoogle Scholar
  40. Ferrari SF, Lopes Ferrari MA (1989) A re-evaluation of the social organisation of the Callitrichidae, with special reference to the ecological differences between genera. Folia Primatol 52: 132–147PubMedCrossRefGoogle Scholar
  41. Ferrari SF, Lopes, MA, Krause EAK (1993) Gut morphology of Callithrix nigriceps and Saguinus labiatus from western Brazilian Amazonia. Am J Phys Anthropol 90: 487–493PubMedCrossRefGoogle Scholar
  42. Ferrari SF, Martins ES (1992) Gummivory and gut morphology in two sympatric callitrichids (Callithrix emiliae and Saguinus fuscicollis weddelli) from western Brazilian Amazonia. Am J Phys Anthropol 88: 97–103PubMedCrossRefGoogle Scholar
  43. Ferrari SF, Rylands AB (1994) Activity budgets and differential visibility in field studies of three marmosets (Callithrix spp.). Folia Primatol 63: 78–83CrossRefGoogle Scholar
  44. Fonseca GAB, Lacher TE (1984) Exudate feeding by Callithrix jacchus penicillata in semideciduous woodland (cerradao) in central Brazil. Primates 25: 441–450CrossRefGoogle Scholar
  45. Fonseca GAB, Lacher TE, Alves C, Magalhães Castro B (1980) Some ecological aspects of free-living black tufted-ear marmosets (Callithrix jacchus penicillata). Antropol Contemp 3: 197Google Scholar
  46. Garber PA (1980) Locomotor behaviour and feeding ecology of the Panamanian tamarin, Saguinus oedipus geoffroyi (Callitrichidae, Primates). Int J Primatol 1: 185–201CrossRefGoogle Scholar
  47. Garber PA (1984) Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. Int J Primatol 5: 1–15CrossRefGoogle Scholar
  48. Garber PA (1988) Diet, foraging patterns and resource defence in a mixed species troop of species Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour 105: 18–34CrossRefGoogle Scholar
  49. Garber PA (1993a) Feeding ecology and behaviour of the Genus Saguinus. In Rylands AB (ed) Marmosets and tamarins: Systematics, ecology and behaviour (pp. 273–295). Oxford University Press, OxfordGoogle Scholar
  50. Garber PA (1993b) Seasonal patterns of diet and ranging in two species of tamarin monkeys: stability versus variability. Int J Primatol 14: 145–166CrossRefGoogle Scholar
  51. Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur Microcebus murinus. Rev Ecol (Terre Vie) 58: 397–410Google Scholar
  52. Génin F. (2008). Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Primatol 29: 303–322.CrossRefGoogle Scholar
  53. Glaser D (1978) Special effects of taste stimuli in Callitrichidae. In Rothe H, Wolters HJ, Hearn JP (eds) The biology and behaviour of marmosets Göttingen, EigenverlagGoogle Scholar
  54. Glicksman M (1969) Gum technology in the food industry. Academic Press, New YorkGoogle Scholar
  55. Grubb P, Butynski TM, Oates JF, Bearder SK, Disotell TR, Groves C, Struhsaker T (2003) Assessment of the diversity of African primates. Int J Primatol 24: 1301–1357CrossRefGoogle Scholar
  56. Guimarães A (1998) Ecologia, comportamento reprodutivo e marcação de cheiro em um grupo de Callithrix flaviceps (Callitrichidae, Primates), na Estação Biológica de Caratinga, Minas Gerais. Dissertação de Mestrado, Universidade Federal de Minas Gerais, Belo HorizonteGoogle Scholar
  57. Harcourt C (1986) Seasonal variation in the diet of South African galagos. Int J Primatol 7: 491–506CrossRefGoogle Scholar
  58. Harcourt C, Bearder SK (1989) A comparison of Galago moholi in South Africa with Galago zanzibaricus in Kenya. Int J Primatol 10: 41–52CrossRefGoogle Scholar
  59. Harcourt CS (1980) Behavioural adaptations in South African galagos. MS dissertation, University of the Witwatersrand, JohannesburgGoogle Scholar
  60. Hardie SM (1995) The behaviour of mixed-species tamarin groups (Saguinus labiatus and Saguinus fuscicollis). Unpublished PhD thesis, University of Stirling, StirlingGoogle Scholar
  61. Harrison ML, Tardif SD (1994) Social implications of gummivory in marmosets. Am J Phys Anthropol 95: 399–408PubMedCrossRefGoogle Scholar
  62. Hausfater G, Bearce WH (1976) Acacia tree exudates: their composition and use as a food source by baboons. East Afr Wildl J 14: 241–243Google Scholar
  63. Hernandez-Camacho J, Cooper RW (1976) The nonhuman primates of Colombia. In Thorington RW, Heltne PG (eds) Neotropical primates, field studies and conservation National Academy of Sciences Press, Washington, DCGoogle Scholar
  64. Hershkovitz, P (1977) Living new world monkeys, Part 1. (Platyrrhini) with an introduction to primates. Chicago University Press, ChicagoGoogle Scholar
  65. Heymann EW, Smith AC (1999) When to feed on gums: temporal patterns of gummivory in wild tamarins, Saguinus mystax and Saguinus fuscicollis (Callitrichinae). Zoo Biol 18: 459–471CrossRefGoogle Scholar
  66. Heymann EW (1990) Further field notes on red uacaris, Cacajao calvus ucayalii, from the Quebrada Blanco, Amazonian Peru. Primate Conserv 11: 7–8Google Scholar
  67. Hizukuri S (1999) Nutritional and physiological functions and uses of L-Arabinose. J Appl Glycosci 46: 159–165CrossRefGoogle Scholar
  68. Hladik A, Hladik CM (1969) Rapports trophiques entre vegetation et primates dans la foret de Barro Colorado (Panama). Terre Vie 1: 25–117Google Scholar
  69. Hladik CM (1979) Diet and ecology of prosimians. In Doyle GA, Martin RD (eds) The study of prosimian behavior Academic Press, New YorkGoogle Scholar
  70. Hladik CM, Charles-Dominique P, Peter J-J (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In Charles-Dominique P, Coper HM, Hladik CM, Petter J-J, Peter-Rousseaux A (eds) Nocturnal Malagasy primates: Ecology, physiology and behaviour Academic Press, New YorkGoogle Scholar
  71. Hopkins HC (1983) The taxomony, reproductive biology and economic potential of Parkia (Leguminosae: Mimosoideae) in Africa and Madagascar. Bot J Linn Soc 87: 135–167CrossRefGoogle Scholar
  72. Hrdy SB (1977) The langurs of Abu. Harvard University Press, Cambridge, MAGoogle Scholar
  73. Hubrecht RC (1985) Home-range size and use and territorial behavior in the common marmoset, Callithrix jacchus jacchus, at the Tapacura field station, Recife, Brazil. Int J Primatol 6: 533–550CrossRefGoogle Scholar
  74. Isbell LA (1998) Diet for a small primate: insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45: 381–398PubMedCrossRefGoogle Scholar
  75. Izawa K (1975) Foods and feeding behaviour of monkeys in the upper Amzon basin. Primates 16: 295–316CrossRefGoogle Scholar
  76. Izawa K (1978) A field study of the the ecology and behaviour of the black mantled tamarin (Saguinus nigricollis). Primates 19: 241–274CrossRefGoogle Scholar
  77. Johns T, Nagarajan M, Parkipuny ML, Jones PJH (2000) Maasai gummivory: implications for Paleolithic diets and contemporary health. Curr Anthropol 41: 453–459PubMedCrossRefGoogle Scholar
  78. Kierulff MC, Raboy BE, de Oliveira PP, Miller K, Passos FC, Prado F (2002) Behavioral ecology of lion tamarins. In Kleiman DG, Rylands AB (eds) Lion tamarins Smithsonian Institution Press, Washington, DCGoogle Scholar
  79. Kinzey WG, Rosenberger AL, Ramirez M (1975) Vertical clinging and leaping in a Neotropical anthropoid. Nature 255: 327–328PubMedCrossRefGoogle Scholar
  80. Knogge C (1998) Zur Vkologie der Samenausbreitung durch zwei Krallenaffenarten (Saguinus mystax, Saguinus fuscicollis) in Amazonien, Nordost-Peru. Unpublished PhD thesis, University of Bielefeld, BielefeldGoogle Scholar
  81. Kovach WL (1999) MVSP – A multi-variate statistical package for Windows, version 3.1. Kovach Computing Services, PentraethGoogle Scholar
  82. Krebs CJ (1989) Ecological methodology. Harper Collins Publishers Inc., New YorkGoogle Scholar
  83. Lacher TE, Fonseca GAB, Alves Jr C, Magalhães-Castro B (1984) Parasitism of trees by marmosets in a Central Brazilian gallery forest. Biotropica 16: 202–209CrossRefGoogle Scholar
  84. Lahann P (2007) Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. J Zool 271: 88–98CrossRefGoogle Scholar
  85. Lopes MA, Ferrari SF (1994) Foraging behaviour of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae). Int J Primatol 15(3): 373–387CrossRefGoogle Scholar
  86. Maier W, Alonso C, Langguth A (1982) Field observations on Callithrix jacchus jacchus. Z Saugetierkd 47: 334–346Google Scholar
  87. Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Phil Trans Soc Lond Biol 264: 295–353CrossRefGoogle Scholar
  88. Martin RD (1973) A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus J.F. Miller 1777). In Michael RP, Crook JH (eds) Comparative ecology and behaviour of primates Academic Press, London and New YorkGoogle Scholar
  89. Martin RD (1979) In Doyle GA, Martin RD (eds) Phylogenetic aspects of prosimian behavior. The study of prosimian behavior Academic Press, New YorkGoogle Scholar
  90. Martin RD, Chivers DJ, Maclarnon AM, Hladik CM (1985) Gastrointestinal allometry in primates and other mammals. In Jungers WL (ed) Size and scaling in primate biology Plenum Press, New York.Google Scholar
  91. Martins MM, Setz EZF (2000) Diet of buffy tufted-eared marmosets (Callithrix aurita) in a forest fragment in southeastern Brazil. Int J Primatol 21: 467–476CrossRefGoogle Scholar
  92. Meer W (1980) Gum arabic. In Davidson RL (ed) Handbook of water soluble gums and resins McGraw-Hill Book Co., New YorkGoogle Scholar
  93. Miranda GHB, de Faria DS (2001) Ecological aspects of black-pincelled marmoset (Callithrix penicillata) in the cerradão and dense cerrado of the Brazillian central plateau. Braz J Biol 61: 397–404PubMedCrossRefGoogle Scholar
  94. Monge TGF (1987) Importanica de los frutos en la dieta de Sanguinus mystax y S. fuscicollis (Primates, Callitrichidae) en el Rio Tayuayo, Loreto – Peru. MSc dissertation, Universidad Nacional de la Amazonia Peruana, IquitosGoogle Scholar
  95. Moynihan M (1976) Notes on the ecology and behaviour of the pygmy marmoset, Cebuella pygmaea, in Amazonian Colombia. In Thorington RW, Heltne PG (eds) Neotropical primates, field studies and conservation National Academy of Sciences Press, Washington, DCGoogle Scholar
  96. Muskin A (1984) Field notes and geographic distribution of Callithrix aurita in Eastern Brazil. Am J Primatol 7: 377–380CrossRefGoogle Scholar
  97. Nash LT (1986) Dietary, behavioural and morphological aspects of gummivory in primates. Yearb Phys Anthrop 29: 113–137CrossRefGoogle Scholar
  98. Nash LT, Whitten PL (1989) Preliminary observations on the role of Acacia gum chemistry in Acacia utilization by Galago senegalensis in Kenya. Am J Primatol 17: 27–39CrossRefGoogle Scholar
  99. Natori M (1986) Interspecific relationships of Callithrix based on the dental characters. Primates 27: 321–336CrossRefGoogle Scholar
  100. Natori M, Hanihara T (1992) Variations in dental measurements between Saguinus species and their systematic relationships. Folia Primatol 258: 84–92CrossRefGoogle Scholar
  101. Newton P (1984) The ecology and social organisation of Hanuman langurs (Presbytis entellus Dufresne, 1797) in Kanha tiger reserve, Central Indian Highlands. PhD thesis, University of Oxford, OxfordGoogle Scholar
  102. Newton P (1992) Feeding and ranging patterns of forest Hanuman langurs (Presbytis entellus). Int J Primatol 13: 245–285CrossRefGoogle Scholar
  103. Neyman PF (1978) Aspects of the ecology and social organisation of free ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. In Kleiman DG (ed) The biology and conservation of the Callitrichdae Smithsonain Institution Press, Washington, DCGoogle Scholar
  104. Nishida T, Uehara S (1983) Natural diet of chimpanzees (Pan troglodytes schweinfurthii): long term record from the Mahale mountains, Tanzania. Afr Study Monogr 3: 109–130Google Scholar
  105. Norconk MA (1986) Interactions between primate species in a neotropical forest: mixed species troops of Saguinus mystax and S. fuscicollis (Callitrichidae). PhD thesis, University of California, Los AngelesGoogle Scholar
  106. Norton GW, Rhine RJ, Wynn GW, Wynn RD (1987) Baboon diet: a five-year study of stability and variability in the plant feeding and habitat of the yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. Folia Primatol 48: 78–120PubMedCrossRefGoogle Scholar
  107. O’Brien TG, Kinnaird MF, Dierenfeld ES, Conklin-Brittain NL, Wrangham RW, Silver SC (1998) What’s so special about figs? Nature 392: 668CrossRefGoogle Scholar
  108. Oliveira ACM, Ferrari SF (2000) Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): implications for regeneration of degraded forest habitats in eastern Amazonia. J Trop Ecol 16: 709–716CrossRefGoogle Scholar
  109. Olson DK (1985) Gum exudates as a dietary staple of patas monkeys. Am J Phys Anthropol 66: 210–211Google Scholar
  110. Oppenheimer JR (1977) Presbytis entellus, the hanuman langur. In Rainier III (Grimaldi) Prince of Monaco, Bourne GH (eds) Primate conservation Academic Press, New YorkGoogle Scholar
  111. Pages E (1980) Ethoecology of Microcebus coquereli during the dry season. In Charles-Dominique P, Coper HM, Hladik CM, Petter J-J, Peter-Rousseaux A (eds) Nocturnal Malagasy primates: Ecology, physiology and behaviour Academic Press, New YorkGoogle Scholar
  112. Passamani M (1996) Ecologia e comportamento de um grupo de sagüi-de-cara-branca (Callithrix geoffroyi) em um fragmento de Mata Atlântica no Espírito Santo. Master thesis, Universidade federal de Minas Gerais, Belo HorizonteGoogle Scholar
  113. Passamani M (1998) Activity budget of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest in southeastern Brazil. Am J Primatol 46: 333–340PubMedCrossRefGoogle Scholar
  114. Passos FC (1997) Padráo de atividades, dieta e uso de espace em um grupo de micoleâo-preto (Leontopithecus chrysopygus) na Estaçao Ecológica dos Caetetus, SP. PhD dissertation, Universidade Federal de Säo Carlos, Säo CarlosGoogle Scholar
  115. Passos FC, de Carvalho CD (1991) Importancia de exsudatos na alimentação do micoleâo-preto Leontopithecus chrysopygus (Callithricidae, Primates). In Resumos XVIII Congresso Brasileiro de Zoologica Universidade Federal da Bahia, SalvadorGoogle Scholar
  116. Passos FC. 1999. Dieta de um grupo de micoleâo-preto, Leontopithecus chrysopygus (Mikan) (Mammalia, Callitrichidae), na Estaçao Ecología dos Caetetus, Sao Paulo. Rev Bras Zool 16: 269–278CrossRefGoogle Scholar
  117. Peres CA (1986) Costs and benefits of territorial defense in golden lion tamarins, Leontopithecus rosalia. Unpublished MSc dissertation, University of Florida, GainsvilleGoogle Scholar
  118. Peres CA (1989) Exudate-eating by wild golden lion tamarins, Leontopithecus rosalia. Biotropica 21: 287–288CrossRefGoogle Scholar
  119. Peres CA (1991) Ecology of mixed-species groups of tamarins in Amazonian terra firme forests. Unpublished PhD thesis, University of Cambridge, CambridgeGoogle Scholar
  120. Peres CA (1993a) Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and mustached (S. mystax) tamarins in an Amazonian terra firme forest. J Zool (Lond) 230: 567–592CrossRefGoogle Scholar
  121. Peres CA (1993b) Notes on the ecology of buffy saki monkeys (Pithecia albicans, Gray 1860): a canopy seed-predator. Am J Primatol 31: 129–140CrossRefGoogle Scholar
  122. Peres CA (1994a) Primate responses to phenological changes in an Amazonian terra firme forest. Biotropica 26: 98–112CrossRefGoogle Scholar
  123. Peres CA (1994b) Diet and feeding ecology of gray woolly monkeys (Lagothrix lagotricha cana) in central Amazonia: comparisons with other atelines. Int J Primatol 15: 333–372CrossRefGoogle Scholar
  124. Peres CA (2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16: 287–317CrossRefGoogle Scholar
  125. Petter JJ (1977) The aye-aye. In Rainier III Prince of Monaco, Bourne G (eds) Primate conservation Academic Press, New YorkGoogle Scholar
  126. Pook AG, Pook G (1981) A field study of the socio-ecology of the Goeldi’s monkey (Callimico goeldii) in Northern Bolivia. Folia Primatol 35: 288–312PubMedCrossRefGoogle Scholar
  127. Porter LM (2000) The behavior and ecology of the Goeldi’s monkey (Callimico goeldii) in northern Bolivia. PhD dissertation, SUNY-Stony Brook, New YorkGoogle Scholar
  128. Porter LM (2001) Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicolis and S. labiatus. Int J Primatol 22: 961–992CrossRefGoogle Scholar
  129. Porter LM, Garber PA, Nacimento E (2009) Exudates as a fallback food for Callimico goeldii. Am J Primatol 71: 120–129PubMedCrossRefGoogle Scholar
  130. Porter LM, Sterr SM, Garber PA (2007) Habitat use and ranging behaviour of Callimico goeldii. Int J Primatol 28: 1035–1058CrossRefGoogle Scholar
  131. Post DG (1982) Feeding behaviour of yellow baboons (Papio cynocephalus) in the Amboseli National Park, Kenya. Int J Primatol 3: 403–430CrossRefGoogle Scholar
  132. Power ML (1991) Digestive function, energy intake and the response to dietary gum in captive Callitrichids. PhD thesis, University of California, BerkeleyGoogle Scholar
  133. Power ML, Oftedal OT (1996) Differences among captive callitrichids in the digestive responses to dietary gum. Am J Primatol 40: 131–141CrossRefGoogle Scholar
  134. Prado F (1999) Ecologia, comportamento e conservação do mico-leão-da-cara-preta (Leontopithecus caissara) no Parque Nacional do Superagüi, Guaraqueçaba, Paraná. Master thesis, Universidade Estudal Paulista, BotucatuGoogle Scholar
  135. Pugh PJA, Convey P (2008) Surviving out in the cold: Antarctic endemic invertebrates and their refugia. J Biogeogr 35: 2176–2186CrossRefGoogle Scholar
  136. Raboy BE, Canale GR, Dietz JM (2008) Ecology of Callithrix kuhlii and a review of eastern Brazilian Marmosets. Int J Primatol 29: 449–467CrossRefGoogle Scholar
  137. Raboy BE, Dietz JM (2004) Diet, foraging, and use of space in wild golden-headed lion tamarins. Am J Primatol 63: 1–15PubMedCrossRefGoogle Scholar
  138. Radespiel U, Reimann W, Rahelinirina M, Zimmermann E (2006) Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. Int J Primatol 27: 311–321.CrossRefGoogle Scholar
  139. Rahaman H, Parthasarathy MD (1969) Studies on the social behaviour of bonnet monkeys. Primates 10: 149–162CrossRefGoogle Scholar
  140. Ramirez M (1985) Exudate feeding in upper Amazonian Saguinus and Cebuella. Am J Phys Anthropol 66: 216Google Scholar
  141. Ramirez M (1989) Ecology and demography of the mustached tamarin, Saguinus mystax in ­northeastern Peru. PhD thesis, City University of New York, New YorkGoogle Scholar
  142. Ramirez MF, Freese CH, Revilla CJ (1978) Feeding ecology of the pygmy marmoset (Cebuella pygmaea) in northeastern Peru. In Kleiman DG (ed) The biology and conservation of the Callitrichidae Smithsonian Institution Press, Washington, DCGoogle Scholar
  143. Ratsimbazafy JH, Ramarosandratana HV, Zaonarivelo RJ (2002) How do black-and-white ruffed lemurs still survive in highly disturbed habitat? Lemur News 7: 7–10Google Scholar
  144. Ripley S (1970) Leaves and leaf monkeys: the social organisation of foraging in gray ­langurs (Presbytis entellus thersites). In Napier JR, Napier PH (eds) Old World monkeys (pp. 489–509). Academic Press, New YorkGoogle Scholar
  145. Rizzini CT, Coimbra-Filho AF(1981) Lesões produzidas pelo sagüi, Callithrix penicillata penicillata (E.Geoffroy 1912), em árvores do cerrado (Callitrichidae, Primates). Rev Bras Biol 41: 579–583Google Scholar
  146. Rosenberger AL, Strasser ME, Delson E (1985) Anterior dentition of Notharctus and the adapid-anthropoid hypothesis. Folia Primatol 44: 15–39CrossRefGoogle Scholar
  147. Rylands AB (1981) Preliminary field observations on the marmoset, Callithrix humeralifer intermedius (Hershkovitz, 1977), at Dardanelos, Rio Aripuanã, Mato Grosso. Primates 22: 46–59CrossRefGoogle Scholar
  148. Rylands AB (1982) The behaviour and ecology of three species of marmosets and tamarins (Callitrichidae, Primates) in Brazil. PhD thesis, University of Cambridge, CambridgeGoogle Scholar
  149. Rylands AB (1984) Exudate-eating and tree-gouging by marmosets (Callitrichindae, Primates). In Chadwick AC, Sutton SL (eds) Tropical rain forest: The Leeds Symposium Leeds Philosophical and Literary Society, LeedsGoogle Scholar
  150. Rylands AB (1989) Sympatric Brazillian callitrichids: the black tufted-ear marmoset, Callithrix kuhlii, and the golden-headed lion tamarin, Leontopithecus chrysomelas. J Hum Evol 18: 679–695CrossRefGoogle Scholar
  151. Rylands AB (1993) The ecology of the lion tamarins, Leontopithecus: some intrageneric differences and comparisons with other callitrichids. In Rylands AB (ed) Marmosets and tamarins: Systematics, Behaviour and Ecology (pp. 296–313). Oxford University Press, OxfordGoogle Scholar
  152. Rylands AB, Faria D (1993) Habitats, Feeding Ecology, and Home Range Size in the genus Callithrix. In Rylands AB (ed) Marmosets and Tamarins: Systematics, Behaviour, and Ecology Oxford University Press, OxfordGoogle Scholar
  153. Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodríguez-Luna, E (2000) An assessment of the diversity of New World primates. Neotrop Primates 8: 61–93Google Scholar
  154. Scanlon CE, Chalmers NR, Monteiro da Cruz MAO (1989) Home range use and the exploitation of gum in the marmoset Callithrix jacchus jacchus. Int J Primatol 10: 123–136CrossRefGoogle Scholar
  155. Schülke O (2003) To breed or not to breed-food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behav Ecol Sociobiol 55: 11–21CrossRefGoogle Scholar
  156. Simmen B (1994) Taste discrimination and diet differentiation among New World primates. In Chivers DJ, Langer P (eds) The digestive system in mammals: Food, form and function Cambridge University Press, OxfordCrossRefGoogle Scholar
  157. Simmen B, Bayart F, Marez A, Hladik A (2007) Diet, nutritional ecology, and birth season of Eulemur macaco in an anthropogenic forest in Madagascar. Int J Primatol 28: 1253–1266CrossRefGoogle Scholar
  158. Smith AC (1997) Comparative ecology of saddleback (Saguinus fuscicollis) and moustached (Saguinus mystax) tamarins. PhD dissertation, University of Reading, ReadingGoogle Scholar
  159. Smith AC (1999) Potential competitors for exudates eaten by saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Neotrop Primates 7: 73–75Google Scholar
  160. Smith AC (2000) Composition and proposed nutritional importance of exudates eaten by saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Int J Primatol 21: 69–83CrossRefGoogle Scholar
  161. Snowdon CT, Soini P (1988) The tamarins, genus Saguinus. In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behaviour of neotropical primates World Wildlife Fund, Washington, DCGoogle Scholar
  162. Soini P (1982) Ecology and population dynamics of the pygmy marmoset, Cebuella pygmaea. Folia Primatol 39: 1–21PubMedCrossRefGoogle Scholar
  163. Soini P (1987) Ecology of the saddle-back tamarin Saguinus fuscicollis illigeri on the Rio Pacaya, northeastern Peru. Folia Primatol 49: 11–32CrossRefGoogle Scholar
  164. Soini P (1988) The pygmy marmosets, genus Cebuella. In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behaviour of neotropical primates World Wildlife Fund, Washington, DCGoogle Scholar
  165. Solanki GS, Kumar A, Sharma BK (2008) Winter food selection and diet composition of capped langur (Trachypithecus pileatus) in Arunachal Pradesh, India. Trop Ecol 49: 157–166Google Scholar
  166. Starin ED (1978) A preliminary investigation of home range use in the Gir Forest langur. Primates 19: 551–567CrossRefGoogle Scholar
  167. Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two New World monkeys. Biol Lett 1: 223–226PubMedCrossRefGoogle Scholar
  168. Stevenson MF, Rylands AD (1988) The marmosets, genus Callithrix. In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behaviour of neotropical primates World Wildlife Fund, Washington, DCGoogle Scholar
  169. Stone AI (2007) Responses of squirrel monkeys to seasonal changes in food availability in an eastern amazonian forest. Am J Primatol 69: 142–157PubMedCrossRefGoogle Scholar
  170. Sugiyama Y, Koman J (1987) A preliminary list of chimpanzees alimentation at Bossou, Guinea. Primates 28: 391–400CrossRefGoogle Scholar
  171. Sugiyama Y, Koman J (1992) The floara of Bossou: its utilization by chimpanzees and humans. Afr Study Monogr 13: 127–169.Google Scholar
  172. Sussman RW (1974) Ecological distinctions in sympatric species of Lemur. Ecology and feeding behaviour of five sympatric lorisids in Gabon. In Martin RD, Doyle GA, Walker AC (eds) Prosimian biology Duckworth, LondonGoogle Scholar
  173. Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: a review. Am J Phys Anthropol 64: 419–449PubMedCrossRefGoogle Scholar
  174. Swedell L, Hailemeskal G, Schreier A (2008) Composition and seasonality of diet in wild hamadryas baboons: preliminary finding from Filoha. Folia Primatol 79: 476–490PubMedCrossRefGoogle Scholar
  175. Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72: 37–39PubMedCrossRefGoogle Scholar
  176. Taylor AB, Vinyard J (2004) Comparative analysis of masseter fibre architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) Callitrichids. J Morph 261: 276–285PubMedCrossRefGoogle Scholar
  177. Terborgh J, Janson CH (1983) The ecology of primates in southeastern Peru. Nat Geogr Soc Res Rep 15: 655–662.Google Scholar
  178. Torres de Assumpção C (1983) An ecological study of primates in south-eastern Brazil, with a reappraisal of Cebus apella races. Unpublished PhD thesis, University of Edinburgh, EdinburghGoogle Scholar
  179. Ushida K, Fujita S, Ohasgi G (2006) Nutritional significance of the selective ingestion of Albizia zygia gum exudate by wild chimpanzees in Bossou, Guinea. Am J Primatol 68: 143–151PubMedCrossRefGoogle Scholar
  180. Valladares-Padua C (1993) The ecology, behavior and conservation of the black lion tamarins (Leontopithecus chrysopygus, Mikan 1823). PhD dissertation, University of Florida, GainesvilleGoogle Scholar
  181. van Roosmalen MGM (1985a) Habitat preferences, diet, feeding strategy and social organisation of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Suriname. Sup Acta Amazon 15(3/4, suppl): 1–238Google Scholar
  182. van Roosmalen MGM (1985b) Fruits of the Guianan flora. Institute of Systematic Botany, Utrecht University, UtrechtGoogle Scholar
  183. Vermes E, Weidholz A (1930) Zur vergleichenden Anatomie des Magen-Darmkanals der Primaten im Hinblick auf die Ernährungsfrage. Zool Gart 3: 28–34Google Scholar
  184. Viguier B (2004) Functional adaptations in the craniofacial morphology of Malagasy primates: shape variations associated with gummivory in the family Cheirogaleidae. Ann Anat 186: 495–501PubMedCrossRefGoogle Scholar
  185. Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5: 139–159CrossRefGoogle Scholar
  186. Wiens F, Zitzmann A, Hussein NA (2006) Fast food for slow lorises: is low metabolism related to secondary compounds in high-energy plant diet? J Mammal 87: 790–798CrossRefGoogle Scholar
  187. Wrangham RW, Waterman PG (1981) Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. J Anim Ecol 50: 715–731CrossRefGoogle Scholar
  188. Yamakoshi G (1998) Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol 106: 283–295PubMedCrossRefGoogle Scholar
  189. Yépez P, de la Torre S, Snowdon CT (2005) Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am J Primatol 66: 145–158PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Animal and Environmental Research Group, Department of Life SciencesAnglia Ruskin UniversityCambridgeUK

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