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

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The Evolution of Exudativory in Primates

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR))

Abstract

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.

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References

  • Agrawal AA, Konno K (2009) Latex: A model for understanding mechanisms, ecology, and ­evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40:311–331

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behaviour: Sampling methods. Behaviour 49:227–267

    Article  PubMed  CAS  Google Scholar 

  • Altmann SA (1998) Foraging for survival: Yearling baboons in Africa. University of Chicago Press, Chicago

    Google Scholar 

  • Anderson MJ (1999) The use of hand morphology in the taxonomy of galagos. Primates 40:469–478

    Article  Google Scholar 

  • 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 21:537–556

    Article  Google Scholar 

  • 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 York

    Google Scholar 

  • Bearder SK, Martin RD (1980a) Acacia gum and its use by bushbabies, Galago senegalensis (Primates Lorisidae). Int J Primatol 1:103–128

    Article  Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Biebouw K (2009) Home range size and use in Allocebus trichotis in Analamazaotra Special Reserve, Central Eastern Madagascar. Int J Primatol 30:367–386

    Article  Google Scholar 

  • Burrows AM, Smith TD (2005) Three-dimensional analysis of mandibular morphology in Otolemur. Am J Phys Anthropol 127:219–230

    Article  PubMed  Google Scholar 

  • Burrows AM, Smith TD (2007) Histomorphology of the mandibular condylar cartilage in greater galagos (Otolemur spp.). Am J Primatol 69:36–45

    Article  PubMed  Google Scholar 

  • Campbell CJ, Fuentes A, Mackinnon KC et al (2007) Primates in perspective. Oxford University Press, New York

    Google Scholar 

  • Caton JM, Hill DM, Hume ID et al (1996) The digestive strategy of the common marmoset, Callithrix jacchus. Comp Biochem Phys A114:1–8

    Google Scholar 

  • Caton JM, Lawes M, Cunningham C (2000) Digestive strategy of the south-east African lesser bushbaby, Galago mohol. Comp Biochem Phys A127:39–48

    Google Scholar 

  • Charles-Dominique P (1977) Ecology and behaviour of nocturnal prosimians. Duckworth, London

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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 York

    Google Scholar 

  • Christianou M, Ebenman B (2005) Keystone species and vulnerable species in ecological communities: Strong or weak interactors? J Theor Biol 235:95–103

    Article  PubMed  Google Scholar 

  • Clark AB (1985) Sociality in a nocturnal “solitary” prosimian: Galago crassicaudatus. Int J Primatol 6:581–600

    Article  Google Scholar 

  • 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, NJ

    Google Scholar 

  • Committee on Animal Nutrition (2003) Nutrient requirements of nonhuman primates, 2nd rev. edn. National Academy Press, Washington, DC

    Google Scholar 

  • Constantino PJ, Wright BW (2009) The importance of fallback foods in primate ecology and evolution. Am J Phys Anthropol 140:599–602

    Article  PubMed  Google Scholar 

  • Copeland SR (2007) Vegetation and plant food reconstruction of lowermost bed II, Olduvai Gorge, using modern analogs. J Hum Evol 53:146–175

    Article  PubMed  Google Scholar 

  • Crompton RH (1983) Age differences in locomotion of two subtropical Galaginae. Primates 24:241–259

    Article  Google Scholar 

  • Davic RD (2003) Linking keystone species and functional groups: a new operational definition of the keystone species concept. Conserv Ecol 7:r11. [online] URL: http://www.consecol.org/vol7/iss1/resp11/

  • Dumont ER (1997) Cranial shape in fruit, nectar, and exudate feeders: Implications for interpreting the fossil record. Am J Phys Anthropol 102:187–202

    Article  PubMed  CAS  Google Scholar 

  • Fedor A, Vasas V (2009) The robustness of keystone indices in food webs. J Theor Biol 260:372–378

    Article  PubMed  Google Scholar 

  • 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 52:132–147

    Article  PubMed  CAS  Google Scholar 

  • Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests: Test of a hypothesis. Oecologia 91:540–547

    Article  Google Scholar 

  • Garber PA (1980) Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201

    Article  Google Scholar 

  • Garber PA (1984) Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. Int J Primatol 5:1–15

    Article  CAS  Google Scholar 

  • 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 York

    Google Scholar 

  • Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur. Rev Ecol – Terre Vie 58:397–410

    Google Scholar 

  • Génin F (2007) Energy-dependent plasticity of grey mouse lemur social systems: Lessons from field and captive studies. Rev Ecol – Terre Vie 62:245–256

    Google Scholar 

  • Génin F (2008) Life in unpredictable environments: First investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321

    Article  Google Scholar 

  • Génin F, Schilling A, Perret M (2005) Social inhibition of seasonal fattening in wild and captive gray mouse lemurs. Physiol Behav 86:185–194

    Article  PubMed  Google Scholar 

  • Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • 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, Baltimore

    Google Scholar 

  • Grubb P, Butynski TM, Oates JF et al (2003) An assessment of the diversity of African primates. Int J Primatol 24:1301–1357

    Article  Google Scholar 

  • Harcourt CS (1986) Seasonal variation in the diet of South African galagos. Int J Primatol 7:491–506

    Article  Google Scholar 

  • Harcourt CS, Bearder SK (1989) A comparison of Galago moholi in South Africa with Galago zanzibaricus in Kenya. Int J Primatol 10:35–45

    Article  Google Scholar 

  • Harcourt CS, Nash LT (1986a) Social organization of galagos in Kenyan coastal forests: I. Galago zanzibaricus. Am J Primatol 10:339–355

    Article  Google Scholar 

  • Harcourt CS, Nash LT (1986b) Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests. Primates 27:41–52

    Article  Google Scholar 

  • Harrison ML, Tardif SD (1994) Social implications of gummivory in marmosets. Am J Phys Anthropol 95:399–408

    Article  PubMed  CAS  Google Scholar 

  • 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 18:459–471

    Article  Google Scholar 

  • 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 York

    Google Scholar 

  • Hodges KE (2008) Defining the problem: Terminology and progress in ecology. Front Ecol Environ 6:35–42

    Article  Google Scholar 

  • Huber HF (2009a) Environmental enrichment for gummivorous primates. M.A. Thesis. Texas State University, San Marcos, San Marcos, TX

    Google Scholar 

  • 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:153

    Google Scholar 

  • Isbell LA (1998) Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45:381–398

    Article  PubMed  CAS  Google Scholar 

  • 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 42:123–133

    Article  Google Scholar 

  • Jordán F, Liu W-c, Mike Á (2009) Trophic field overlap: A new approach to quantify keystone species. Ecol Modell 220:2899–2907

    Article  Google Scholar 

  • Kelly K (1993) Environmental enrichment for captive wildlife through the simulation of gum feeding. Anim Welf Inf Cent Newsl 4:1–2, 5–10

    Google Scholar 

  • Lambert JE (1998) Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20

    Article  Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Lambert JE (2009) Summary to the symposium issue: Primate fallback strategies as adaptive phenotypic plasticity – scale, pattern, and process. Am J Phys Anthropol 140:759–766

    Article  PubMed  Google Scholar 

  • Marshall A, Wrangham R (2007) Evolutionary consequences of fallback foods. Int J Primatol 28:1219–1235

    Article  Google Scholar 

  • 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 140:603–614

    Article  PubMed  Google Scholar 

  • Masters JC, Brothers DJ (2002) Lack of congruence between morphological and molecular data in reconstructing the phylogeny of the Galagonidae. Am J Phys Anthropol 117:79–93

    Article  PubMed  Google Scholar 

  • Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137

    Article  Google Scholar 

  • Nash LT (1989) Galagos and gummivory. Hum Evol 4:199–206

    Article  Google Scholar 

  • 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 1:204–217

    Article  Google Scholar 

  • Nash LT, Harcourt CS (1986) Social organization of galagos in Kenyan coastal forests: II. Galago garnettii. Am J Primatol 10:357–369

    Article  Google Scholar 

  • 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 York

    Google Scholar 

  • Peres CA (2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317

    Article  Google Scholar 

  • Pimley E, Bearder SK, Dixson AF (2003) Patterns of ranging and social interactions in pottos (Perodicticus potto edwardsi) in Cameroon. Folia Primatol 74:367–368

    Article  Google Scholar 

  • Pimley ER, Bearder SK, Dixson AF (2005a) Home range analysis of Perodicticus potto edwardsi and Sciurocheirus cameronensis. Int J Primatol 26:191–206

    Article  Google Scholar 

  • Pimley ER, Bearder SK, Dixson AF (2005b) Social organization of the Milne-Edward’s potto. Am J Primatol 66:317–330

    Article  PubMed  Google Scholar 

  • Porter LM (2007) The behavioral ecology of callimicos and tamarins in northwestern Bolivia. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

  • Porter LM, Garber PA (2004) Goeldi’s monkeys: A primate paradox? Evol Anthropol 13:104–115

    Article  Google Scholar 

  • Porter LM, Garber PA, Nacimento E (2009) Exudates as a fallback food for Callimico goeldii. Am J Primatol 71:120–129

    Article  PubMed  CAS  Google Scholar 

  • Ray E (2007) Research questions. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New York

    Google Scholar 

  • Reed KE, Bidner LR (2004) Primate communities: Past, present, and possible future. Yearb Phys Anthropol 47:2–39

    Article  Google Scholar 

  • 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 55:11–21

    Article  Google Scholar 

  • 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 65:331–343

    Article  Google Scholar 

  • Schülke O, Ostner J (2005) Big times for dwarfs: Social organization, sexual selection, and cooperation in the Cheirogaleidae. Evol Anthropol 14:170–185

    Article  Google Scholar 

  • Simmen B, Hladik CM (1998) Sweet and bitter taste discrimination in primates: Scaling effects across species. Folia Primatol 69:129–138

    Article  PubMed  CAS  Google Scholar 

  • Smith AP (1982) Diet and feeding strategies of the marsupial sugar glider in temperate Australia. J Anim Ecol 51:149–166

    Article  Google Scholar 

  • Smith AP (1992) Sugar gliders, wattles and rural eucalypt dieback. Aust Netw Plant Conserv Newsl 1:7–10

    Google Scholar 

  • Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two New World monkeys. Biol Lett 1:223–226

    Article  PubMed  Google Scholar 

  • Suckling GC (1984) Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Wildl Res 11:49–75

    Google Scholar 

  • Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: A review. Am J Phys Anthropol 64:419–449

    Article  PubMed  CAS  Google Scholar 

  • Sussman RW, Raven PH (1978) Pollination by lemurs and marsupials: An archaic coevolutionary system. Science 200:731–736

    Article  PubMed  CAS  Google Scholar 

  • Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39

    Article  PubMed  CAS  Google Scholar 

  • 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 139:353–367

    Article  PubMed  Google Scholar 

  • 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 68:143–151

    Article  PubMed  CAS  Google Scholar 

  • Viguier B (2004) Functional adaptations in the craniofacial morphology of Malagasy primates: Shape variations associated with gummivory in the family Cheirogaleidae. Ann Anat 186:495–501

    Article  PubMed  Google Scholar 

  • Vinyard CJ, Wall CE, Williams SH et al (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170

    Article  PubMed  Google Scholar 

  • 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 87:790–798

    Article  Google Scholar 

  • Wright PC (1999) Lemur traits and Madagascar ecology: Coping with an island environment. Yearb Phys Anthropol 42:31–72

    Article  Google Scholar 

  • 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 139:368–381

    Article  PubMed  Google Scholar 

  • Yépez P, De La Torre S, Snowdon CT (2005) Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am J Primatol 66:145–158

    Article  PubMed  Google Scholar 

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Acknowledgments

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.

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  1. School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, 85287-2402, USA

    Leanne T. Nash

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  1. Leanne T. Nash
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Correspondence to Leanne T. Nash .

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  1. Dept. Physical Therapy, Duquesne University, Pittsburgh, 15282, Pennsylvania, USA

    Anne M. Burrows

  2. School of Human Evolution &, Social Change, Arizona State University, Tempe, 85287-2402, Arizona, USA

    Leanne T. Nash

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Nash, L.T., Burrows, A.M. (2010). Introduction: Advances and Remaining Sticky Issues in the Understanding of Exudativory in Primates. In: Burrows, A., Nash, L. (eds) The Evolution of Exudativory in Primates. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6661-2_1

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