Abstract
Five species of slow lorises were once considered to comprise a single strongly polymorphic species, Nycticebus coucang, ranging throughout South and Southeast Asia. The cryptic nature of these nocturnal primates has led to a lack of understanding of their distribution patterns and abundance. In short surveys, often few if any lorises are detected, meaning that the few available density estimates are from long-term studies. Based on new research in Sebangau National Park, Borneo, and compilation of survey data from other areas, we provide the first comparative abundance estimates for all five slow loris species: N. coucang occurred in significantly higher abundances (median encounter rate 0.80/km: n = 15), than N. bengalensis (0.26/km; n = 12), or N. javanicus (0.11/km: n = 2), N. menagensis (0.02/km: n = 3), and N. pygmaeus (0.13/km: n = 4). Abundance estimates in Sebangau (0.19/km) did not increase with increasing survey effort, but for all species and studies combined, study duration was positively correlated with abundance estimates. We did not find a relation between abundance and body mass, nor between abundance and latitude. Long-term studies are more likely to be conducted at sites where the species of interest is particularly plentiful. The data suggest that slow lorises occur at low abundances throughout much of their range, and some in larger social groups than previously assumed. We recommend taking into account the species’ heterogeneous distribution (potentially requiring larger survey effort), their social structure, the use of red lights as opposed to white lights whilst surveying, and to make use of their vocalisations when surveying slow lorises.
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References
Andelman SJ, Fagan WF (2000) Umbrellas and flagships: efficient conservation surrogates or expensive mistakes. Proc Natl Acad Sci USA 97(11):5954–5959
Barrett E (1981) The present distribution and status of the slow loris in peninsular Malaysia. Malays Appl Biol 10:205–211
Barrett E (1984) The ecology of some nocturnal, arboreal mammals in the rainforests of peninsular Malaysia. Dissertation, Cambridge University
Bearder SK, Doyle GA (1974) Ecology of bushbabies Galago senegalensis and Galago crassicaudatus, with some notes on their behaviour in the field. In: Martin RD, Doyle GA, Walker AC (eds) Prosimian biology. Duckworth Press, London, pp 109–130
Brandon-Jones D, Eudey AA, Geissmann T et al (2004) Asian primate classification. Int J Primatol 25(1):97–164
Brooks TM, Mittermeier RA, Mittermeier CG et al (2000) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16(4):909–923
Buckley C, Nekaris KAI, Husson SJ (2006) Survey of Hylobates agilis albibarbis in a logged peat-swamp forest: Sabangau catchment, Central Kalimantan. Primates 47(4):327–335
Caro T, Engilis A, Fitzherbert E et al (2004) Preliminary assessment of the flagship species concept on a small scale. Anim Conserv 7:63–70
Charles-Dominique P (1977) Ecology and behaviour of nocturnal primates. Duckworth Press, London
Charles-Dominique P, Bearder SK (1979) Field studies of lorisid behaviour: methodological aspects. In: Doyle GA, Martin RD (eds) The study of prosimian behaviour. Academic Press, New York, pp 567–629
Chen JH, Pan D, Groves CP et al (2006) Molecular phylogeny of Nycticebus inferred from mitochondrial genes. Int J Primatol 27(4):1187–1200
Chivers DJ (1992) Socio-ecology and conservation of gibbons in Southeast Asia with special reference to Borneo In: Ismail G, Mohamed M, Omar S (eds) Forest biology and conservation in Borneo. Centre for Borneo Studies Publication No 2, Sabah Foundation, Kota Kinabalu, pp 230–244
Chivers DJ, Burton KM (1988) Some observations on the primates of Kalimantan Tengah, Indonesia. Primate Conserv 9:138–146
Choudhury A (1998) Mammals, birds and reptiles of Dibru-Saikhowa sanctuary, Assam, India. Oryx 32(3):192–200
Choudhury A (1999) Primates in gibbon sanctuary Assam, India. Asian Primates 7:4–6
Collins R (2007) Preliminary study of behaviour and population densities of Nycticebus coucang and N. javanicus in Sumatra and Java, Indonesia. MSc Thesis, Oxford Brookes University, Oxford
Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, Oxford
Duckworth JW (1994) Field sighting of the pygmy loris (Nycticebus pygmaeus) in Laos. Folia Primatol 63:99–101
Duckworth JW (1997) Mammals in Similajau National Park, Sarawak, in 1995. Sarawak Mus J 51:171–192
Duckworth JW (1998a) A survey of large mammals in the central Annamite mountains of Laos. Z Säugetierk 63:239–250
Duckworth JW (1998b) The difficulty of estimating population densities of nocturnal forest mammals from line transect counts. J Zool 246:466–468
Duckworth JW, Timmins RJ, Thewlis RCM et al (1994) Field observations of mammals in Laos, 1992–1993. Nat His Bull Siam Soc 42:177–205
Elliot O, Elliot M (1967) Field notes on the slow loris in Malaya. J Mammol 48:497–498
Entwistle AC, Stephenson PJ (2000) Small mammals and the conservation agenda. In: Entwistle AC, Dunstone N (eds) Priorities for the conservation of mammalian diversity: has the panda had its day? Cambridge University Press, Cambridge, pp 369–387
Evans TD, Duckworth JW, Timmins RJ (2000) Field observations of larger mammals in Laos, 1994–1995. Mammalia 64:55–100
Fitch-Snyder H, Vu NT (2002) A preliminary survey of lorises (Nycticebus spp.) in northern Vietnam. Asian Primates 8:1–3
Geissmann T, Bohlen-Eyring S, Heuck A (2005) The male song of the Javan silvery gibbon (Hylobates moloch). Contrib Zool 74:1–25
Groves CP (1971) Systematics of the genus Nycticebus. In: Biegert J, Leutenegger W (eds) Taxonomy, anatomy, reproduction. Proceedings of the third international congress of primatology, vol 1. S Karger, Basel, pp 44–53
Groves CP (1998) Systematics of tarsiers and lorises. Primates 39:13–27
Groves C, Maryanto I (in press) Craniometry of slow lorises (Genus Nycticebus) of insular Southeast Asia. Primates of the Oriental Night, Treubia (Shekelle M, ed)
Gupta AK (1994) Status and conservation of non-human primates in Tripura, India. In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N (eds) Current primatology, vol I: ecology and evolution. Uni Louis Pasteur, Strasbourg, pp 101–111
Gursky S (1998) Conservation status of the spectral tarsier, Tarsius spectrum: population density and home range size. Folia Primatol 69:191–203
Haydon MJ (1994) The ecology and management of rain forest ungulates in Sabah, Malaysia: implications of forest disturbance. Final Report to the Institute of Tropical Biology, University of Aberdeen, UK
Hilton-Taylor C (2002) 2002 IUCN Red List of Threatened Species. The World Conservation Union (IUCN), Species Survival Commission (SSC), Gland, Switzerland and Cambridge, UK
Hunyh DH (1998) Ecology, biology and conservation status of prosimians species in Vietnam. Folia Primatol 69:101–108
Indrawan M, Rangkuti F (2001) Development, biodiversity and the conservation status of banded langur in Natuna Islands, Indonesia. Trop Biodiv 7:151–163
IUCN (2007) Website: www.redlist.org
Jenkins DV (1971) Animal life of Kinabalu National Park. Malay Nat J 24:177–183
Jewell PA, Oates JF (1969) Ecological observations of the lorisoid primates of African lowland forest. Zool Afr 4:231–248
Johns AD (1983) Ecological effects of selective logging in a West Malaysian rain forest. PhD Thesis, Cambridge University, Cambridge, UK
Johns AD (1986) Effects of selective logging on the behavioral ecology of West Malaysian primates. Ecology 67(3):684–694
Koenig A, Larney E, Kreetiyutanont K et al (2004) The primates of Phu Khieo Wildlife Sanctuary. Am J Phys Anth 123(suppl 38):127
Liat LB (1969) Distribution of the primates of West Malaysia. Proc 2nd Int Cong Primat 1968, vol 2. Karger, Basel, pp 121–130
Liat LB, Muul I, Langham NPE (1971) Preliminary studies of small mammals collected from Penang Island, Malaysia. Fed Museum J 16:61–74
Malone N, Purnama AR, Wedana M et al (2002) Assessment of the sale of primates at Indonesian bird markets. Asian Primates 8:7–11
Meijaard E, Sheil D, Nasi R et al (2005) Life after logging: reconciling wildlife conservation and production forestry in Indonesian Borneo, CIFOR and UNESCO, Bogor
Merker S, Yustian I, Muhlenberg M (2005) Responding to forest degradation: altered habitat use by Dian’s tarsier Tarsius dianae in Sulawesi, Indonesia. Oryx 39:189–195
Merker S (2006) Habitat-specific ranging patterns of Dian’s tarsiers (Tarsius dianae) as revealed by radiotracking. Am J Primatol 68:111–125
Molur S, Brandon-Jones D, Dittus W et al (2003) The status of South Asian primates: conservation assessment and management plan (C.A.M.P) workshop report. Zoo Outreach Organisation/CBSG-South Asia, Coimbatore, pp:viii, 432
Momberg F, Weiler H (1999) Conservation status of the Cardamom Mountains in Southwestern Cambodia: preliminary studies. Fauna and Flora International Indochina Programme, Hanoi, pp 63
Morrogh-Bernard H, Husson S, Page SE et al (2003) Population status of the Bornean orang-utan (Pongo pygmaeus) in the Sebangau peat swamp forest, Central Kalimantan, Indonesia. Biol Conserv 110:141–152
Nekaris KAI (2003) Spacing system of the Mysore slender loris (Loris lydekkerianus lydekkerianus). Am J Phys Anthropol 121:86–96
Nekaris KAI (2006) The social lives of Mysore slender lorises. Am J Primatol 68:1–12
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, pp 24–45
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 (2004) Distribution of slender lorises in four ecological zones in Sri Lanka. J Zool 262:1–12
Nekaris KAI, Nijman V (2007) CITES proposal highlights threat to nocturnal primates (Nycticebus: Lorisidae). Folia Primatol 78:211–214
Nekaris KAI, Liyanage WKDD, Gamage S (2005) Relationship between forest structure and floristic composition and population density of the Southwestern Ceylon slender loris (Loris tardigradus tardigradus) in Masmullah Forest, Sri Lanka. Mammalia 69:1–10
Nekaris KAI, Pimley ER, Ablard K (2006) Anti-predator behaviour of lorises and pottos. In: Gursky SG, Nekaris KAI (eds) Primates and their predators. Springer Press: New York, pp 220–238
Nijman V (2003) Species management plan for the primates of Kayan Mentarang National Park. WWF Indonesia, Tarakan, pp 159
Nijman V (2006) In situ and ex situ status of the Javan gibbon and the role of zoos in conservation of the species. Contrib Zool 75:161–168
Nijman V, van Balen S (1998) A faunal survey of the Dieng Mountains, Central Java, Indonesia: distribution and conservation of endemic primate taxa. Oryx 32:145–156
Pimley ER, Bearder SK, Dixson AF (2005) Home range analysis of Perodicticus potto and Sciurocheirus cameronensis. Int J Primatol 26:185–201
Rasmussen DT (1986) Life history and behaviour of slow and slender lorises: Implications for the lorisine-galagine divergence. PhD Thesis, Duke University, Durham, North Carolina
Rhadakrishna S, Sinha A (2004) Population survey and conservation of the Bengal slow loris in Assam and Meghalaya, Northeastern India. Technical Report 1–04 to Margot Marsh Biodiversity Foundation, USA, pp 31
Rhadakrishna S, Goswami AB, Sinha A (2006) Distribution and conservation of Nycticebus bengalensis in northeastern India. Int J Primatol 27:971–982
Ratajszczak R (1998) Taxonomy, distribution and status of the lesser slow loris Nycticebus pygmaeus and their implications for captive management. Folia Primatol 69:171–174
Ravosa MJ (1998) Cranial allometry and geographic variation in slow lorises (Nycticebus). Am J Primatol 45:225–243
Roos C (2003) Molekulare Phylogenie der Halbaffen, Schlankaffen, und Gibbons. Dissertation, Technische Universität München
Rudd RL, Stevens GL (1992–94) A long-term capture-mark-release (CMR) and removal study of small mammals in Malaysian sub-montane rain forest. Wasmann J Ecol 50:96–150
Shepherd CR, Sukumaran J, Wich SA (2005) Open season: an analysis of the pet trade in Medan, North Sumatra, 1997–2001. TRAFFIC Southeast Asia. Kuala Lumpur
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
Schulze H, Groves CP (2004) Asian lorises: taxonomic problems caused by illegal trade. In: Nadler T, Streicher U, Thang Long H (eds) Conservation of primates in Vietnam. Frankfurt Zoological Society, Frankfurt, pp 33–36
Singh M, Lindburg DG, Udhayan A, et al (1999) Status survey of slender loris Loris tardigradus lydekkerianus in Dindigul, Tamil Nadu, India. Oryx 33:31–37
Streicher U (2004) Aspects of the ecology and conservation of the pygmy loris Nycticebus pygmaeus in Vietnam. Dissertation. Ludwig-Maximilians-Universität, München
Steinmetz R, Chutpong W, Seuaturien N (2006) Collaborating to conserve large mammals in Southeast Asia. Cons Biol 20:1391–1401
Supriatna J, Manansang J, Tumbelaka L et al (eds) (2001) Conservation assessment and management plan for the primates of Indonesia. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley, MN, p 251
Sutherland WJ (2002) Mammals. In: Sutherland WJ (ed) Ecological censusing techniques. Cambridge University Press, Cambridge, pp 260–278
van Schaik CP, Ancrenaz M, Borgen G et al (2003) Orang-utan cultures and the evolution of material culture. Science 299:102–105
Webber C, Nekaris KAI (2004) Survey of primates and other mammals in markets of Indonesia, with an analysis of conditions and health of the animals. Folia Primatol 75:60
Wells K, Pfeiffer M, Lakim MB et al (2004) Use of arboreal and terrestrial space by a small mammal community in a tropical rain forest in Borneo, Malaysia. J Biog 31:641–652
Wiens F (2002) Behavior and ecology of wild slow lorises (Nycticebus coucang): social organisation, infant care system and diet. Dissertation, Bayreuth University
Wiens F, Zitzmann A (2003) Social structure of the solitary slow loris Nycticebus coucang (Lorisidae). J Zool 261:35–46
White L, Edwards A (2000) Methods for assessing the status of animal populations. In: White L, Edwards A (eds) Conservation research in the African rain forests: a technical handbook. Wildlife Conservation Society, New York, pp 91–201
Zar JH (1999) Biostatistical analysis. Prentice Hall, New Jersey
Zhang Y, Quan G, Zhao T et al (1992) Distribution of primates (except Macaca) in China. Acta Theriologica Sinica 12:81–95
Zimmerman E (1985) Vocalisations and associated behaviours in adult slow loris (Nycticebus coucang). Folia Primatol 44:52–64
Acknowledgements
We thank S Husson, H Morrogh-Bernard, L D’Arcy, S Cheyne, Suwido Limin and CIMTROP for their guidance in the field. We are also indebted to R Collins, W Duckworth, AD Grieser-Johns, S Gursky, A Miehs, C Starr, CR Shepherd and K Wells for providing details of unpublished data. This manuscript was greatly improved by comments from W. Duckworth and two anonymous reviewers. This project was supported by a grant from the Orang-utan Foundation UK to Blackham, and SYNTHESYS (NL-TAF-3491) and an Oxford Brookes University Research Strategy Fund Grant to Nekaris.
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Nekaris, K.A.I., Blackham, G.V. & Nijman, V. Conservation implications of low encounter rates of five nocturnal primate species (Nycticebus spp.) in Asia. Biodivers Conserv 17, 733–747 (2008). https://doi.org/10.1007/s10531-007-9308-x
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DOI: https://doi.org/10.1007/s10531-007-9308-x