Abstract
Craniomandibular variation characterizes the five species of Asian slow loris (Nycticebus), but until now, few ecological studies have been available to understand the factors that underpin it. Here, we review feeding ecology of Asian lorises and African pottos, with emphasis on the importance of exudate feeding, including several new studies. We then present novel data on this behavior based on a 10-week study of N. coucang at Pusat Penyelamatan Satwa, Lampung, Sumatra, Indonesia. Lorises and pottos range in body size from 100 g (Loris tardigradus) to more than 2 kg (N. bengalensis). Three of the smallest species (Arctocebus calabarensis, A. aureus, L. tardigradus) rely mainly on insects and small invertebrates as dietary staples. Although Perodicticus is known to eat gum only from already open wounds, active gouging of bark to extract exudates or consumption of plant sap has now been observed in all other lorises. Five species (P. potto, N. coucang, N. bengalensis, N. javanicus, N. pygmaeus) rely on exudates as a key food source. Although at all field sites, exudates are eaten all year round, at some, they become a key resource in times of food scarcity. Exudates have been extracted from 14 different plant families; Fabaceae is possibly the most important, currently consumed by all exudativorous species. Despite the lack of keeled nails, gouging behavior of lorises closely resembles that of marmosets and fork-marked lemurs, and involves active breaking of the plant surface; the audible nature of this behavior, as well as the characteristic marks left behind, makes it useful for determining the presence of Nycticebus in a forest. The captive lorises in our study also gouged regularly, recorded 2.9 times per hour for both adults and juveniles. Urine and facial marking accompanied the majority of gouges, a behavior recorded before only for marmosets. The functions of this behavior as a resource sharing strategy are explored. The importance of providing opportunity for gouging for captive lorises is also discussed, as a way to mitigate the periodontal diseases, which plague Nycticebus in captivity. We conclude by discussing the importance of a better understanding of this relatively unique behavior to improve our knowledge of morphological correlates to loris taxonomy and ecology, and captive management via dietary changes and enrichment.
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Altmann J (1974) Observational study of behaviour: sampling methods. Behavior 49: 227–267
Ambrose L (1999) Species diversity in West and Central African galagos (Primates, Galagonidae): the use of acoustic analysis. PhD thesis, Oxford Brookes University, Oxford
Barrett E (1984) The ecology of some nocturnal, arboreal mammals in the rainforests of peninsular Malaysia. Unpub. Ph.D. dissertation, University of Cambridge, Cambridge
Bearder S, Martin RD (1980) Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1:103–128
Charles-Dominique P (1977) Ecology and Behaviour of the Nocturnal Primates. Prosimians of Equatorial West Africa. Duckworth, London
Chivers DL, Hladik CM (1980) Morphology of the gastrointestinal tracts in primates: comparisons with other animals in relation to diet. J Morphol 166:337–386
Coimbra-Filho AF, Mittermeier RA (1978) Tree-gouging, exudate-eating and the “short-tusked” condition in Callithrix and Cebuella. In: Kleimann DG (ed) The behaviour and conservation of the Callithrichidae. Smithsonian Institution Press, Washington
Collins RL (2007) Behavioural data of captive greater slow loris (Nycticebus coucang) & Javan slow loris (N. javanicus), and a survey of Javan slow loris in Mt. Salak, West Java, Java. Unpub. MSc dissertation. Oxford Brookes University, Oxford
Collins R, Nekaris KAI (2008) Release of greater slow lorises (Nycticebus coucang), confiscated from the pet trade, to Batutegi Protected Forest, Sumatra, Indonesia. In: Soorae PS (ed) IUCN global re-introduction perspectives: Re-introduction case studies from around the globe. IUCN/SSC Reintroduction Specialist Group, Abu Dabhi, UAE
Craig J, Reed C (2003) Diet-based enrichment ideas for small primates. Int Zoo News 50(1):16–20
Das N (2008) Comments on the feeding ecology of Nycticebus bengalensis in Gibbon Wildlife Sanctuary, Assam, India. Report submitted to the Nocturnal Primate Research Group, Oxford, UK, p. 1
Fitch-Snyder H, Schulze H, Larson L (eds) (2001) Management of lorises in captivity. A husbandry manual for Asian lorisines (Nycticebus & Loris ssp.). Center for Reproduction in Endangered Species (CRES), Zoological Society of San Diego, San Diego
Fleagle J (1999) Primate adaptation and evolution. Academic Press, San Diego
Groves C, Maryanto I (2008) Craniometry of slow lorises (genus Nycticebus) of insular Southeast Asia. In: Shekelle M (ed) Primates of the Oriental night. Treubia, Jakarta
Gutteridge RC, Shelton HM (1998) Forage tree legumes in tropical agriculture with case studies from Australia and Southeast Asia. CABI Publishing, Australia
Hladik CM (1979) Diet and ecology of prosimians. In: Doyle GA, Martin RD (eds) The study of prosimian behaviour. Academic Press, New York
Hylander WL (1985) Mandibular function and biomechanical stress and scaling. Am Zool 25:315–330
Kingdon J (1974) East African mammals. An atlas of evolution in Africa, Vol. 1. Academic Press, London
Kubota K, Iwamoto M (1966) Comparative anatomical and neurohistological observations on the tongue of slow loris (Nycticebus coucang). Anat Rec 158:163–176
Lehner PN (1996) Handbook of ethological methods. University Press, Cambridge
McGrew WC, Brennan JA, Russell J (1986) An artificial “gum-tree” for marmosets (Callithrix j. jacchus). Zoo Biol 5(1):45–50
Müller EF, Nieschalk U, Meier B (1985) Thermoregulation in the slender loris (Loris tardigradus). Folia Primatol 44:216–226
Nash L (1986) Dietary, behavioural, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137
Nash L (1989) Galagos and gummivory. Hum Evol 4(2–3):199–206
Nekaris KAI, Bearder SK (2007) The strepsirrhine primates of Asia and Mainland Africa: diversity shrouded in darkness. In: Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford
Nekaris KAI, Jaffe S (2007) Unexpected diversity within the Javan slow loris trade: implications for slow loris taxonomy. Contrib Zool 76:187–196
Nekaris KAI, Jayewardene J (2003) Pilot study and conservation status of the slender loris (Loris tardigradus and Loris lydekkerianus) in Sri Lanka. Primate Conserv 19:83–90
Nekaris KAI, Nijman V (2007) Survey on the abundance and conservation of Sumatran slow lorises (Nycticebus coucang hilleri) in Aceh, Northern Sumatra. Proceedings of the European Federation of Primatology, Charles University, Prague, p. 47
Nekaris KAI, Rasmussen DT (2003) Diet and feeding behaviour of the Mysore slender loris. Int J Primatol 24(1):33–46
Nekaris KAI, Blackham GV, Nijman V (2008) Implications of low encounter rates in five nocturnal species (Nycticebus spp). Biodivers Conserv 17(4):733–747
Nekaris KAI, Munds R (2010) Using facial markings to unmask diversity: the slow lorises (Primates: Lorisidae: Nycticebus) of Indonesia. In (Gursky S & Supriatna J, eds) The Primates of Indonesia. Springer: New York. Pp. 383–396
Oates JF (1984) The niche of the potto, Perodicticus potto. Int J Primatol 5(1):51–61
Osman Hill WC (1953) Primates. Comparative anatomy and taxonomy. I. Strepsirhini. Edinburgh University Press, Edinburgh
Petter JJ, Schilling A, Pariente G (1971) Observations eco-ethologiques sur deux lemuriens malgaches nocturnes: Phaner furcifer et Microcebus coquereli. Terre Vie 118:287–327
Pimley ER (2002) The behavioural ecology and genetics of the potto (Perodicticus potto edwardsi) and Allen’s bushbaby (Schiurocheirus alleni cameronensis). Unpub. Ph.D. thesis, University of Cambridge, Cambridge
Pliosoengeon M, Savini T (2008) Spatial and feeding behavior of the endangered Bengal slow loris, Nycticebus bengalensis in Khao Angrunai Wildlife Sanctuary, Thailand. Unpublished report to the Primate Society of Great Britain, p. 8
Rahm U (1960) Quelques notes sur le potto de Bosman. Bull Inst Fr d’Afr Noire, Ser A 22:331–341
Ratajszczak R (1998) Taxonomy, distribution and status of the lesser slow loris Nycticebus pygmaeus and their implications for captive management. Folia Primatol 69(1):171–174
Ravosa MJ (1998) Cranial allometry and geographic variation in slow lorises (Nycticebus). Am J Primatol 45:225–243
Rhadakrishna S (2001) The social behavior of the Mysore slender loris (Loris tardigradus lydekkerianus). Unpub. Ph.D. thesis, University of Mysore, Manasagangotri
Roos C (2003) Molekulare Phylogenie der Halbaffen, Schlankaffen, und Gibbons. Unpub. Ph.D. thesis, Technische Universität München
Rylands AB (1984) Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In: Chadwick AC, Sutton SL (eds) Tropical rain forest. The Leeds Symposium. Leeds Philosophical and Literary Society, Leeds
Rylands AB (1985) Tree-gouging and scent-marking by marmosets. Anim Behav 33(4):1365–1367
Rylands AB (1990) Scent-marking behaviour of wild marmosets, Callithrix humeralifer (Callitrichidae, Primates). In: Macdonald DW, Müller-Schwarze D, Natynczuk SE (eds) Chemical signals in vertebrates 5. Oxford University Press, Oxford
Schein L (2008) Species diversity of the enigmatic nocturnal primates in the secondary Rhoko forest, Cross River State, Nigeria: Preliminary findings on densities, abundance estimates, and methods comparisons using DISTANCE. MSc Primate Conservation. Oxford Brookes University, UK
Schwartz JH, Beutel JC (1995) Species diversity in lorisids: a preliminary analysis of Arctocebus, Perodicticus and Nycticebus. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: The nocturnal prosimians. Plenum Press, New York
Starr CR, Streicher U, Nekaris KAI (2008) The distribution and conservation of the pygmy loris (Nycticebus pygmaeus) in Eastern Cambodia. XXIIth Congress International Primatological Society Abstracts, Primate Eye:116
Streicher, U (2004) Aspects of the ecology and conservation of the pygmy loris Nycticebus pygmaeus in Vietnam. Dissertation. Ludwig-Maximilians Universität, Germany
Streicher U, Collins R, Navarro-Montes A, Nekaris KAI (in review) Observations on the feeding preferences of slow lorises (N. pygmaeus, N. javanicus, N. coucang) confiscated from the trade. In: Masters J, Crompton R, Genin F (eds) Prosimians. Springer, New York
Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39
Vinyard CJ, Wall CE, Williams SH, Hylander WL (2003) Comparative functional analysis of skull morphology of tree-gouging in primates. Am J Phys Anthropol 120:153–170
Wiens F (2002) Behaviour and ecology of wild slow lorises (Nycticebus coucang): social organisation, infant care system, and diet. Dissertation. Faculty of Biology, Chemistry and Geosciences, Bayreuth University, Germany
Wiens F, Zitzmann A (2003) Social dependence of infant slow lorises to learn diet. Int J Primatol 24(5):1008–1021
Wiens F, Zitzmann A, Hussein NA (2006) Fast food for slow lorises: is low metabolism related to secondary 5 compounds in high-energy plant diet? J Mammal 87(4):790–798
Williams SH, Wall CE, Vinyard CJ, Hylander WL (2001) A biomechanical analysis of skull form in gum-harvesting galagids. Folia Primatol 73:197–109
Winarti I (2008) Field research on Javan slow loris’ population in Sukakerta Ciamis and Kawungsari Tasikmalaya, West Java, Indonesia. Report to IAR Indonesia, Ciapus, Bogor, Indonesia, p. 7
Zimmermann E (1989) Reproduction, physical growth and behavioural development in slow loris (Nycticebus coucang, Lorisidae). Hum Evol 4(2–3):171–179
Acknowledgments
We thank Annie Burrows and Leanne Nash for organizing the symposium at the International Primatology Conference in Edinburgh and for inviting us to participate in this volume. We are extremely grateful to N. Das, M. Pliosoengeon, and I. Winarti for sharing unpublished accounts of loris exudativory; to J. Oates, L. Schein, and E. Pimley for unpublished accounts on the lack of this behavior in pottos and angwantibos; and to A. Rylands and S. Bearder for sharing their observations on exudate feeding in marmosets and galagos. For the Sumatran study, we thank the staff at PPS and IAR, especially to P. Agus, F. den Haas, A. Knight, E. Rahadian, K. Sanchez, and K. Sudaryatmo. International Animal Rescue, International Primate Protection League, Primate Conservation Inc., and Oxford Brookes University provided financial support.
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Nekaris, K.AI., Starr, C.R., Collins, R.L., Wilson, A. (2010). Comparative Ecology of Exudate Feeding by Lorises (Nycticebus, Loris) and Pottos (Perodicticus, Arctocebus). 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_8
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