Introduction: Advances and Remaining Sticky Issues in the Understanding of Exudativory in Primates

  • Leanne T. Nash
  • Anne M. Burrows
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


In the 25 years since the last synthesis on this topic was published, there has been a marked increase in the appreciation of exudativory as a primate dietary strategy and investigations of its morphological correlates that appear to be adaptations to exudates as food. At least 75 species of primates consume some exudates. Variability of diet among marmosets and tamarins precludes simple classifications of the former as year-round specialists vs. the latter as always facultative seasonal users of exudates. Differences in exudate use among callithrichines, now also including callimico as an exudativore, are associated with apparent adaptations in gut anatomy and functioning, a suite of dental and jaw features, and some features of socioecology and life-history. Among strepsirrhines, several Nycticebus species are newly known to gouge to eat gum, variability among mouse lemurs in gum use has been documented, but little added work has improved our knowledge of variation in exudate use in galagos. For these taxa, much less is understood about possible morphological, behavioral and life-history adaptations and detailed descriptions of behaviors associated with exudate acquisition are needed from the field. The ability to identify anatomical features that will clarify the role of exudates in the diets of fossil primates remains a major challenge.


Mouse Lemur Gray Mouse Lemur Patas Monkey Dietary Niche Fallback Food 
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.



First, we thank all of the authors whose hard work tackling the sticky issue of exudativory – and their patience with our nagging – make this an exciting volume. To all the reviewers of the chapters in the book, we are most grateful for the improvements they helped us make to the chapters. We are very grateful to Melissa Higgs at Springer for her endless advice and assistance. Michael Power and George Perry provided helpful comments on this chapter. We would also like to thank our families who put up with our rants and occasional absences as well as providing us with much needed support.


  1. Agrawal AA, Konno K (2009) Latex: A model for understanding mechanisms, ecology, and ­evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40:311–331CrossRefGoogle Scholar
  2. Altmann J (1974) Observational study of behaviour: Sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  3. Altmann SA (1998) Foraging for survival: Yearling baboons in Africa. University of Chicago Press, ChicagoGoogle Scholar
  4. Anderson MJ (1999) The use of hand morphology in the taxonomy of galagos. Primates 40:469–478CrossRefGoogle Scholar
  5. Anderson MJ, Ambrose L, Bearder SK et al (2000) Intraspecific variation in the vocalizations and hand pad morphology of southern lesser bush babies (Galago moholi): A comparison with G. senegalensis. Int J Primatol 21:537–556CrossRefGoogle Scholar
  6. Bearder SK, Honess PE, Ambrose L (1995) Species diversity among galagos with special reference to mate recognition. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: The nocturnal prosimians. Plenum Publishing Co., New YorkGoogle Scholar
  7. Bearder SK, Martin RD (1980a) Acacia gum and its use by bushbabies, Galago senegalensis (Primates Lorisidae). Int J Primatol 1:103–128CrossRefGoogle Scholar
  8. Bearder SK, Martin RD (1980b) The social organization of a nocturnal primate revealed by radio tracking. In: Amlaner CJ, MacDonald DW (eds) A handbook on biotelemetry and radio tracking. Pergamon Press, OxfordGoogle Scholar
  9. 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
  10. Burrows AM, Smith TD (2005) Three-dimensional analysis of mandibular morphology in Otolemur. Am J Phys Anthropol 127:219–230PubMedCrossRefGoogle Scholar
  11. Burrows AM, Smith TD (2007) Histomorphology of the mandibular condylar cartilage in greater galagos (Otolemur spp.). Am J Primatol 69:36–45PubMedCrossRefGoogle Scholar
  12. Campbell CJ, Fuentes A, Mackinnon KC et al (2007) Primates in perspective. Oxford University Press, New YorkGoogle Scholar
  13. Caton JM, Hill DM, Hume ID et al (1996) The digestive strategy of the common marmoset, Callithrix jacchus. Comp Biochem Phys A114:1–8Google Scholar
  14. Caton JM, Lawes M, Cunningham C (2000) Digestive strategy of the south-east African lesser bushbaby, Galago mohol. Comp Biochem Phys A127:39–48Google Scholar
  15. Charles-Dominique P (1977) Ecology and behaviour of nocturnal prosimians. Duckworth, LondonGoogle Scholar
  16. Charles-Dominique P, Bearder SK (1979) Field studies of lorisid behavior: Methodological aspects. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic Press, New YorkGoogle Scholar
  17. Charles-Dominique P, Petter JJ (1980) Ecology and social life of Phaner furcifer. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pagès E, Pariente GF, Petter-Rousseaux A, Petter J-J, Schilling A (eds) Nocturnal Malagasy primates: Ecology, physiology, and behavior. Academic Press, New YorkGoogle Scholar
  18. Christianou M, Ebenman B (2005) Keystone species and vulnerable species in ecological communities: Strong or weak interactors? J Theor Biol 235:95–103PubMedCrossRefGoogle Scholar
  19. Clark AB (1985) Sociality in a nocturnal “solitary” prosimian: Galago crassicaudatus. Int J Primatol 6:581–600CrossRefGoogle Scholar
  20. Collinge SK, Ray C, Cully JF, Jr. (2008) Effects of disease on keystone species, dominant species, and their communities In: Ostfeld RS, Keesing F, Eviner VT (eds) Infectious disease ecology: Effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, NJGoogle Scholar
  21. Committee on Animal Nutrition (2003) Nutrient requirements of nonhuman primates, 2nd rev. edn. National Academy Press, Washington, DCGoogle Scholar
  22. Constantino PJ, Wright BW (2009) The importance of fallback foods in primate ecology and evolution. Am J Phys Anthropol 140:599–602PubMedCrossRefGoogle Scholar
  23. Copeland SR (2007) Vegetation and plant food reconstruction of lowermost bed II, Olduvai Gorge, using modern analogs. J Hum Evol 53:146–175PubMedCrossRefGoogle Scholar
  24. Crompton RH (1983) Age differences in locomotion of two subtropical Galaginae. Primates 24:241–259CrossRefGoogle Scholar
  25. Davic RD (2003) Linking keystone species and functional groups: a new operational definition of the keystone species concept. Conserv Ecol 7:r11. [online] URL:
  26. Dumont ER (1997) Cranial shape in fruit, nectar, and exudate feeders: Implications for interpreting the fossil record. Am J Phys Anthropol 102:187–202PubMedCrossRefGoogle Scholar
  27. Fedor A, Vasas V (2009) The robustness of keystone indices in food webs. J Theor Biol 260:372–378PubMedCrossRefGoogle Scholar
  28. Ferrari SF, Lopes FMA (1989) A re-evaluation of the social organization of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatol 52:132–147PubMedCrossRefGoogle Scholar
  29. Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests: Test of a hypothesis. Oecologia 91:540–547CrossRefGoogle Scholar
  30. Garber PA (1980) Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201CrossRefGoogle Scholar
  31. 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
  32. Garber PA, Rosenberger AA, Norconk MA (1996) Marmoset misconceptions. In: Norconk MA, Rosenberger AA, Garber PA (eds) Adaptive radiations of neotropical primates. Plenum Press, New YorkGoogle Scholar
  33. Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur. Rev Ecol – Terre Vie 58:397–410Google Scholar
  34. Génin F (2007) Energy-dependent plasticity of grey mouse lemur social systems: Lessons from field and captive studies. Rev Ecol – Terre Vie 62:245–256Google Scholar
  35. Génin F (2008) Life in unpredictable environments: First investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321CrossRefGoogle Scholar
  36. Génin F, Schilling A, Perret M (2005) Social inhibition of seasonal fattening in wild and captive gray mouse lemurs. Physiol Behav 86:185–194PubMedCrossRefGoogle Scholar
  37. Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DCGoogle Scholar
  38. Groves CP (2005) Order primates. In: Wilson DE, Reeder DM (eds) Mammal species of the world: A taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  39. Grubb P, Butynski TM, Oates JF et al (2003) An assessment of the diversity of African primates. Int J Primatol 24:1301–1357CrossRefGoogle Scholar
  40. Harcourt CS (1986) Seasonal variation in the diet of South African galagos. Int J Primatol 7:491–506CrossRefGoogle Scholar
  41. Harcourt CS, Bearder SK (1989) A comparison of Galago moholi in South Africa with Galago zanzibaricus in Kenya. Int J Primatol 10:35–45CrossRefGoogle Scholar
  42. Harcourt CS, Nash LT (1986a) Social organization of galagos in Kenyan coastal forests: I. Galago zanzibaricus. Am J Primatol 10:339–355CrossRefGoogle Scholar
  43. Harcourt CS, Nash LT (1986b) Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests. Primates 27:41–52CrossRefGoogle Scholar
  44. Harrison ML, Tardif SD (1994) Social implications of gummivory in marmosets. Am J Phys Anthropol 95:399–408PubMedCrossRefGoogle Scholar
  45. 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
  46. Hladik CM, Charles-Dominique P, Petter J-J (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P (ed) Nocturnal Malagasy primates: ecology, physiology and behavior. Academic Press, New YorkGoogle Scholar
  47. Hodges KE (2008) Defining the problem: Terminology and progress in ecology. Front Ecol Environ 6:35–42CrossRefGoogle Scholar
  48. Huber HF (2009a) Environmental enrichment for gummivorous primates. M.A. Thesis. Texas State University, San Marcos, San Marcos, TXGoogle Scholar
  49. Huber HF (2009b) Gum’s the word: applying knowledge from the wild to improve environmental enrichment for captive gummivores. Am J Phys Anthropol S48, Suppl:153Google Scholar
  50. 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
  51. Isbell LA, Pruetz JD, Young TP (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density and distribution. Behav Ecol Sociobiol 42:123–133CrossRefGoogle Scholar
  52. Jordán F, Liu W-c, Mike Á (2009) Trophic field overlap: A new approach to quantify keystone species. Ecol Modell 220:2899–2907CrossRefGoogle Scholar
  53. Kelly K (1993) Environmental enrichment for captive wildlife through the simulation of gum feeding. Anim Welf Inf Cent Newsl 4:1–2, 5–10Google Scholar
  54. Lambert JE (1998) Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20CrossRefGoogle Scholar
  55. Lambert JE (2007) Seasonality, fallback strategies, and natural selection: a chimpanzee and cercopithecoid model for interpreting the evolution of the hominin diet. In: Ungar PS (ed) Evolution of the human diet: The known, the unknown, and the unknowable. Oxford University Press, OxfordGoogle Scholar
  56. Lambert JE (2009) Summary to the symposium issue: Primate fallback strategies as adaptive phenotypic plasticity – scale, pattern, and process. Am J Phys Anthropol 140:759–766PubMedCrossRefGoogle Scholar
  57. Marshall A, Wrangham R (2007) Evolutionary consequences of fallback foods. Int J Primatol 28:1219–1235CrossRefGoogle Scholar
  58. Marshall AJ, Boyko CM, Feilen KL et al (2009) Defining fallback foods and assessing their importance in primate ecology and evolution. Am J Phys Anthropol 140:603–614PubMedCrossRefGoogle Scholar
  59. Masters JC, Brothers DJ (2002) Lack of congruence between morphological and molecular data in reconstructing the phylogeny of the Galagonidae. Am J Phys Anthropol 117:79–93PubMedCrossRefGoogle Scholar
  60. Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137CrossRefGoogle Scholar
  61. Nash LT (1989) Galagos and gummivory. Hum Evol 4:199–206CrossRefGoogle Scholar
  62. Nash LT (1998) Vertical clingers and sleepers: Seasonal influences on the activities and substrate use of Lepilemur leucopus at Beza Mahafaly Special Reserve, Madagascar. Folia Primatol 69, Suppl 1:204–217CrossRefGoogle Scholar
  63. Nash LT, Harcourt CS (1986) Social organization of galagos in Kenyan coastal forests: II. Galago garnettii. Am J Primatol 10:357–369CrossRefGoogle Scholar
  64. Nekaris A, Bearder SK (2007) The lorisiform primates of Asia and mainland Africa: Diversity shrouded in darkness. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New YorkGoogle Scholar
  65. Peres CA (2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317CrossRefGoogle Scholar
  66. Pimley E, Bearder SK, Dixson AF (2003) Patterns of ranging and social interactions in pottos (Perodicticus potto edwardsi) in Cameroon. Folia Primatol 74:367–368CrossRefGoogle Scholar
  67. Pimley ER, Bearder SK, Dixson AF (2005a) Home range analysis of Perodicticus potto edwardsi and Sciurocheirus cameronensis. Int J Primatol 26:191–206CrossRefGoogle Scholar
  68. Pimley ER, Bearder SK, Dixson AF (2005b) Social organization of the Milne-Edward’s potto. Am J Primatol 66:317–330PubMedCrossRefGoogle Scholar
  69. Porter LM (2007) The behavioral ecology of callimicos and tamarins in northwestern Bolivia. Prentice Hall, Upper Saddle River, NJGoogle Scholar
  70. Porter LM, Garber PA (2004) Goeldi’s monkeys: A primate paradox? Evol Anthropol 13:104–115CrossRefGoogle Scholar
  71. Porter LM, Garber PA, Nacimento E (2009) Exudates as a fallback food for Callimico goeldii. Am J Primatol 71:120–129PubMedCrossRefGoogle Scholar
  72. Ray E (2007) Research questions. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New YorkGoogle Scholar
  73. Reed KE, Bidner LR (2004) Primate communities: Past, present, and possible future. Yearb Phys Anthropol 47:2–39CrossRefGoogle Scholar
  74. 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
  75. Schülke O, Kappeler PM (2003) So near and yet so far: Territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Anim Behav 65:331–343CrossRefGoogle Scholar
  76. Schülke O, Ostner J (2005) Big times for dwarfs: Social organization, sexual selection, and cooperation in the Cheirogaleidae. Evol Anthropol 14:170–185CrossRefGoogle Scholar
  77. Simmen B, Hladik CM (1998) Sweet and bitter taste discrimination in primates: Scaling effects across species. Folia Primatol 69:129–138PubMedCrossRefGoogle Scholar
  78. Smith AP (1982) Diet and feeding strategies of the marsupial sugar glider in temperate Australia. J Anim Ecol 51:149–166CrossRefGoogle Scholar
  79. Smith AP (1992) Sugar gliders, wattles and rural eucalypt dieback. Aust Netw Plant Conserv Newsl 1:7–10Google Scholar
  80. Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two New World monkeys. Biol Lett 1:223–226PubMedCrossRefGoogle Scholar
  81. Suckling GC (1984) Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Wildl Res 11:49–75Google Scholar
  82. Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: A review. Am J Phys Anthropol 64:419–449PubMedCrossRefGoogle Scholar
  83. Sussman RW, Raven PH (1978) Pollination by lemurs and marsupials: An archaic coevolutionary system. Science 200:731–736PubMedCrossRefGoogle Scholar
  84. Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39PubMedCrossRefGoogle Scholar
  85. Taylor AB, Eng CM, Anapol FC et al (2009) The functional correlates of jaw-muscle fiber architecture in tree-gouging and nongouging callitrichid monkeys. Am J Phys Anthropol 139:353–367PubMedCrossRefGoogle Scholar
  86. Ushida K, Fujita S, Ohashi 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
  87. 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
  88. Vinyard CJ, Wall CE, Williams SH et al (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170PubMedCrossRefGoogle Scholar
  89. 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
  90. Wright PC (1999) Lemur traits and Madagascar ecology: Coping with an island environment. Yearb Phys Anthropol 42:31–72CrossRefGoogle Scholar
  91. Yamashita N, Vinyard CJ, Tan CL (2009) Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. Am J Phys Anthropol 139:368–381PubMedCrossRefGoogle Scholar
  92. 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

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.School of Human Evolution and Social ChangeArizona State UniversityTempeUSA

Personalised recommendations