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Biology

By day, lorises are known to sleep curled up in the fork of a tree (2), but during the night, these animals can be seen moving slowly and deliberately through the trees on all fours (2) (5). They walk and climb along tree limbs, and stretch between terminal branches to cross to a neighbouring tree (5). Pygmy lorises feed on insects, seizing flying insects in their hands whilst they grip a branch with both hindfeet (2). This protein-rich food is supplemented with fruit, as well as gum from trees (3). To digest these gums, lorises possess unusually large cecums, a bag joining the large intestine that houses bacteria which enables these sugary gums to be broken down (5). It is thought that this ability to feed on gum helps pygmy lorises survive times when there is a shortage of other food sources (3). The pygmy loris gives birth to just a single young each year, after a gestation period of 184 to 200 days. The young are weaned at the age of 123 to 146 days (3), but generally stay within their mother's territory until they are sexually mature and establish a range of their own (5). The life span of the pygmy loris is believed to be about 20 years (3).
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Description

This nocturnal, tree-dwelling Asian primate has short, thick, woolly hair that is light brownish-grey to deep reddish-brown in colour. The individual hairs often have silvery tips giving a 'frosted' appearance and a darker stripe runs along the spine. The underparts are lighter in colour, being almost white or greyish (2) (3). The large eyes of the pygmy loris, which provide good vision at night (5), are encircled with dark rings and separated by a streak of light fur (2). Like other lorises, each digit on the hands and feet bears a nail, except for the second digit on each foot which instead has what is known as a 'toilet' claw, used for grooming (5). Unlike many other primates, lorises do not possess a tail to assist with moving through their forest habitat, but instead a special arrangement of muscles in the hands and feet enable an effortless and powerful grasp, allowing the pygmy loris to grip tightly to a branch at lofty heights all day (2) (5).
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Pygmy slow loris (Nycticebus pygmaeus)

The pygmy slow loris was described by J. Lewis Bonhote, from a juvenile male collected from Vietnam in 1905 (3). In 1939, Pocock placed all slow lorises in one species, N. coucang (4). Osman Hill (5) listed the pygmy slow loris as N. c. pygmaeus, but said that it could be deemed "specific rank". In 1960, Dao Van Tien called a species from Hòa Bình Province, Vietnam, N. intermedius (7), but his specimens were adult pygmy slow lorises (8,9). Colin Groves said the pygmy slow loris was morphologically unique enough to be a distinct species (8,11). This was supported by studies of chromosomal structure (12), genetic distance determined by protein variation at polymorphic loci (13) and mitochondrial DNA restriction enzyme analysis (14,15). N. pygmaeus diverged earlier than other species (16), perhaps 2.7 million years ago (15). Analysis of nucleotide sequence diversity from lorises from boundary areas between southern China and Vietnam (an area of sympatry between the pygmy and Bengal species) show that the former is not subject to the same introgressive hybridization as the latter. The study's authors suggest that the low polymorphism of pygmy slow lorises may be due to a founder effect and the individuals they studied originate from an ancestor that lived in middle or southern Vietnam 1860-7350 years ago (18). The pygmy slow loris shares a common ancestor with the Bengal slow loris (N. bengalensis) and its smaller body size may be due to character displacement, the accentuation of differences between similar species sharing the same geographic distribution. The two species differ in the banding patterns on the chromosomes (12). J.L. Harrison said the pygmy slow loris is "rather like a child's teddy-bear." The loris has short, thick, light brownish-grey to deep reddish-brown woolly hair. The pattern of light and dark facial markings often includes brown rings around the eyes, which are lighter in older individuals. A white stripe runs from the nose to the forehead, there are silvery hairs at the sides, black ears, lacking furry tips, and dorsal stripes from the crown down the back (9,20) . In winter, the markings become more prominent and gain silver tips or "frosting" (20). This may camouflage and protect the loris, which sits in exposed areas such as dense scrub or in the upper branches of trees that lack foliage in winter. The lighter underparts are almost white or greyish (2,3). The black ears are about 23 mm (0.91 in) long (9) and lack fur on the tips (5). The presence or absence of a dorsal stripe and silvery hair tips seems to be seasonal and not a separate species, N. intermedius (28-30). The buff legs have silvery white hands and feet (31) and yellowish-white nails (5). The large, forward-facing eyes provide good stereoscopic vision at night (5). The tapetum lucidum, a reflective layer in the eye, improves night vision (26). The rhinarium is a moist naked surface around the nostrils. The upper lip is split. The dental formula is 2.1.3.3/2.1.3.3. The lower incisors and canines tilt forward and form a toothcomb for grooming and feeding (25). The triangular third molar is only slightly smaller than the first molar; the second molar is largest (3). Each digit on the hands and feet has a nail, except the second digit on each foot which has a 'toilet' claw for grooming (5). The hand has a reduced second digit. A special arrangement of muscles in the hands and feet enables an effortless and powerful grasp, so a loris can grip tightly to a branch at lofty heights all day (2,5). The loris can grow to around 19-23 cm (7.5-9.1 in) long and has about a 1.8 cm (0.71 in) tail (9). It weighs 360-580 g (13- 20 oz) (22). Males tend to be slightly larger than females (9). Some individuals retard their growth in unfavourable environmental conditions. If the diet is restricted, they lose their juvenile fur and attain adult dentition before attaining adult size. There are large seasonal variations in weight and individuals may weigh up to 700 g (25 oz), being about 50% heavier in winter than the lowest weight in summer. Weight gains, due largely by increased feeding, are triggered by changes in the length of the day and night. This may help ensure survival in winter when food resources are scarce (23).

The loris occurs east of the Mekong River in eastern Cambodia, southernmost China (southeastern Yunnan), Lao PDR, and Vietnam (2,25,37,43,56). It seems to be absent or very scarce in the extreme west of the Mekong plain. It is unclear if lorises in southeast Yunnan are wild animals or captured animals brought into China from Viet Nam. The loris lives in various forest habitats, including primary evergreen and semi-evergreen rain forests, tropical dry forests, forests on limestone, secondary and highly degraded habitats, mixed deciduous forests and bamboo thickets (2,3,25,43,56,62,67,68). It is found up to 1,500 m (64). The loris is nocturnal and arboreal. It is least active on cold, moonlit nights and is generally active on dark nights, despite temperature (33). It conserves energy in colder winter months by reducing movement, often being inactive (23). It lives in trees at heights of 3-12 m in the canopy. By day, it leeps curled up in the fork of a tree (2). At night, it forages alone, walking and climbing slowly and deliberately on all fours along branches (2,5). It stretches between terminal branches to cross to a neighbouring tree and does not leap (5). It produces an aprocrine secretion from brachial scent glands (modified sweat glands) near inside of the elbows. The clear, oily secretion has over 200 volatile and semi-volatile components, such as a secretoglobin protein, similar to an allergenic protein in cat dander (38). When startled or alarmed, the loris licks the secretion from the glands, so it is mixed with its saliva, creating a volatile, noxious toxin, which it applies to its head (38). The toxic bite can be dangerous to humans; a loris bit a woman and she entered anaphylactic shock (42). The loris uses various verbal calls, such as a short whistle; it issues a rising tone during general contact. When disturbed, it growls and hisses. It may live in groups of 2-4, usually with young, but often occurs alone (34). Males use scent marking to defend territories and mark their boundaries. The loris is omnivorous, eating fruits, protein-rich termites, ants and other insects, geckos, small arboreal mammals, eggs and chicks, tree sap and floral nectar (24,25,27,32,58,62). It may be more insectivorous than N. coucang, which may help it survive better in secondary habitat lacking big fruiting trees (62). It uses its toothcomb to scrape resin from tree bark. It seizes flying insects in its hands whilst it grips a branch with both hindfeet (2), while standing or hanging upside down from a branch. It usually consumes insects at heights below 10 m (33 ft) (57). It uses its toothcomb to clean an area of lichens and fungi before gouging trees to eat the released exudates (22,60). It scratches and breaks bark and licks gum from trees (3), preferably flowering trees (25). It feeds on gum for 1-20 minutes at heights over 8 m (26 ft) (57). This involves intense licking, sometimes with scratching and bark-breaking sounds. Seasonal colour variation in the dorsal stripe may be linked to exudate feeding (22). It eats insects exposed by its bamboo-gouging activities. The very large caecum houses bacteria that break down and digest sugary gum (5) and this may help the loris survive times when other food sources are scarce (3). It develops fat stores by feeding more on energy-rich foods in the last few weeks of autumn to help it during the food scarce winter months. Tree gum is less nutrient-rich than its preferred diet, but is available year-round (22,23,60). Despite its high-sugar diet and small body mass, the loris has a very low metabolism, perhaps because it must detoxify toxic secondary compounds in its food (57). As the loris may eat a lot of fruit, it may aid seed dispersal. It may be a host tovarious protozoans, nematodes and other parasites. There are reports of predation by Sumatran orang-utans and reticulated pythons (6), but the ranges of orangs and pygmy slow lorises do not overlap. The loris blends in well with its surroundings, which may lead to low non-human predation rates. Humans are the primary predators of the loris, which is sold in Cambodian and Vietnamese markets (25). The tapetum lucidum glows when a spotlight is shone in its direction and this may incapacitate the loris. The loris seems to be a seasonal, polygynous breeder. It reproduces every 12-18 months. A male's territory typically includes several females with whom he mates. The loris may whistle to the opposite sex and use olfactory cues to find mates during oestrus (July-October) (44), when the female vagina and male testes enlarge. Testosterone peaks of males coincide with female oestrogen peaks (45). The loris is monoestrous with one 4-5 day period of reproductive activity (49). Females are more likely to approach others and engage in lunging; males are more likely to sniff and lick a female's genitals and mount them. Males spread their scent through urination and produce more urine than females. Urine scent markings have a strong characteristic odour and are communicate information about social relationships. Males that spread their scent over a large area have a competitive advantage, as marking territory indicates health, persistence, and energy. Females prefer males with a familiar odour to males they have not previously met, which may be related to infrequent contact between the sexes (35,36). Males countermark, over or next to another individual's mark, to advertise competitive ability to females (36). Females actively prefer countermarking males to males whose odours have been countermarked (36). If there is only one male's scent in an area, he can defend the area and/or prevent rival males from marking (52). An oestrous female is mildly aggressive to her suitors and often lunges at males, usually after a long period of being approached and followed. Vocalizations during mating include whistling, most commonly by the oestrous female, as well as chittering and growling. The female gives birth to 1-2 young in early February to mid-March (45) after a gestation period of 184-200 days (62). Birthing occurs in the open and the fully formed infants have fur and open eyes and weigh @ 23 g. The birth sex ratio is 1 female to 1.68 males (18). As mothers of twins must divide time equally between offspring, they spend less time engaging in social grooming and play with their young (54), which may lead to a lower infant survival rate (18). The newborn infant clings to its mother's belly. When the young are a week old, their mothers show "parking" behaviour, leaving them in a safe location while they forage for food. This lets the mothers gather food more efficiently for themselves and their young. The young follow their mothers at about 2 weeks (54). Mothers softly chirp to their infants, which respond with rapid clicks and squeaks when in distress (43). Compared to other lorises, the mothers spend more time close to their young, tending to huddle, sit or stand within 0.3 m of their young more than do other species. Mothers and infants primarily establish closeness through passive ventral contact. While mothers do not seem to directly defend their young, they tolerate older young following them. Older infants engage more often in adult social behaviour, such as grooming and play and less often in huddling and ventral contact. The young are weaned at 4-6 months (3,18,45), but weaning may take 8 months. The young tend to stay in their mother's territory until they are sexually mature and establish a range of their own (5). Females become sexually mature at 9-16 months and males at 18-20 months. The loris can conceive by 18 months and give birth by 2 years (46); captives may still breed at 14 years. The life span is thought to be @ 20 years (3,21,56). The loris is listed as Vulnerable on the IUCN Red List 2007 (1) and is on Appendix I of CITES (2,4,17,64). This gives it some protection from the devastating effects of trade as international commercial trade is prohibited (4); capture and transport are illegal in all countries in its range (56,66,69). There is little enforcement of these laws and penalties are too low to deter others (3,66). It declined by 30% in 3 generations (24 years) from 1984-2008, due mainly to hunting for food and trade (22,28,43,53,55,56,68-70), but also habitat loss (3,10,19,56,62) and gold mine development (43). It may warrant listing in a higher category of threat if the rate of decline is @ 50%. Populations fell drastically during the Vietnam War, as bombing, burningland clearing. Agent Orange, other defoliants and napalm destroyed much of their habitat (2,4,5,21). Some people kill the loris as they think it is a crop pest (43). Laos exports lorises to Vietnam (70). Ratajszczak (88) said hundreds of lorises were traded as pets and for medicine in markets (56,62,63,68), but fewer are now found in Viet Namese markets, so populations are probably in major decline (25,66). The low reproduction rate cannot keep pace with these large-scale off-takes (56,66). The loris is used in traditional Khmer medicine in Cambodia (17,22,56) and is exported to Laos, Thailand and Vietnam and eventually China and Taiwan and Europe (50,56,59,63). In Phnom Penh, local markets roast, dry and make lorises into pre-mixed medicines with rice-wine, alcohol, honey or charcoal; this loris is the most commonly requested animal in the traditional medicine shops (51). Doctors say these medicines treat "women after childbirth, stomach problems, wounds, broken bones and sexually transmitted diseases" (51). In Vietnam, medicine such as bone glue of monkey, is mainly produced by local people, but some is used in restaurants or sold to visitors (55,56). The hair is assumed to have medicinal value (56). In the 1950s, the fur was used to dress wounds and cuts due to its blood clotting properties. Increased protection of the loris led to the market price rising. Traders in live lorises do not distinguish among species (94) and there may be hybridization, improper care and health problems; confiscared animals may be reintroduced into improper habitat. Transport in small containers stresses lorises and threatens their health. Mortality rates are high, due to trauma, disease, malnutrition and close proximity to other lorises (56). The loris is represented by about 175 individuals in at least 50 captive collections (39) and reported in at least 24 national parks and nature reserves (1,3,56,68,70). A pygmy slow loris in North America was kept at Honolulu Zoo in 1968. In 1986, about 37 pygmy lorises were exported from Vietnam and Laos to Sweden. In 1987, several wild-caught pairs were transferred to zoos in Cincinnati, San Diego and the Duke Lemur Center (48). In 1994, the Association of Zoos and Aquariums established a Species Survival Plan for the species, after a proposal by the Global Captive Action Plan for Primates to create a breeding program to maintain its genetic diversity (48). Up to 2008, most captives were born at the San Diego Zoo (41). In 2013, the species is the most common lorisid in North American zoos (40).
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  • 52. Gosling, L. M. (1982). "A reassessment of the function of scent marking in territories". Zeitschrift für Tierpsychologie 60 (2): 89–118. doi:10.1111/j.1439-0310.1982.tb00492.x+ (inactive 2012-01-19). Ivanova, E., S. Spiridonov, O. Bain. 2007. Ocular oxyspirurosis of primates in zoos: intermediate probable origin of ht infection in the Moscow zoo. Parasite, 14(4): 287-298.
  • 53. Nguyen, V. S. (2003). "Wildlife trading in Vietnam: why it flourishes" (Word document). 2003-RR6 (Economy and Environment Program for Southeast Asia (EEPSEA)).
  • 54. Fitch-Snyder, H. and A. Ehrlich (2003). "Mother-infant interactions in slow lorises (Nycticebus bengalensis) and pygmy lorises (Nycticebus pygmaeus)". Folia Primatologica 74 (5–6): 259–271. doi:10.1159/000073313.
  • 55. Nguyen, Q. T.; V.S. Nguyen; X.T. Ngo and T.S. Nguyen (2003). "Evaluation of the wildlife trade in Na Hang District" (PDF). PARC Project VIE/95/G31&031 (Government of Viet Nam (FPD) /UNOPS/UNDP/Scott Wilson Asia-Pacific Ltd.).
  • 56. CITES Management Authority of Cambodia (3–15 June 2007). "Notification to Parties: Consideration of Proposals for Amendment of Appendices I and II" (PDF). Netherlands: Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). p. 31.
  • 57. Streicher, U. (2009). "Diet and feeding behaviour of pygmy lorises (Nycticebus pygmaeus) in Vietnam" (PDF). Vietnamese Journal of Primatology 3: 37–44.
  • 58. Swapna, N. (2008). Assessing the feeding ecology of the Bengal slow loris (Nycticebus bengalensis) in Trishna Wildlife Sanctuary, Tripura (M.Sc. thesis). Post-Graduate Program in Wildlife Biology & Conservation Centre for Wildlife Studies and National Centre for Biological Sciences UAS-GKVK Campus Bangalore. http://msc.wcsindia.org/PDF/14_Swapna%20N.pdf. Retrieved 2013-02-22.
  • 59. Schulze, H. and C.P. Groves (2004). "Asian Lorises: taxonomic problems caused by illegal trade". In Nadler, T.; Streicher, U.; Hà, T. L. Conservation of Primates in Vietnam. Hanoi, Vietnam: Frankfurt Zoological Society. OCLC 60527537.
  • 60. Tan, C. L. and J.H. Drake (2001). "Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus)". Folia Primatologica 72 (1): 37–39. doi:10.1159/000049918.
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  • 62. Ratajszczak, R. 1998. Taxonomy, Distribution and Status of the Lesser Slow Loris Nycticebus pygmaeus and Their Implications for Captive Management. Folia Primatologica, 69(1): 171-174. doi:10.1159/000052710.
  • 63. "Lorises and pottos: species, subspecies, local populations. Table 14 b: Threat due to predation, poaching and similar causes" (PDF). Conservation database for lorises (Loris, Nycticebus) and pottos (Arctocebus, Perodicticus), prosimian primates. www.loris-conservation.org. 4 February 2003.
  • 64. MacKinnon, J. and K. MacKinnon (1987). "Conservation status of the primates of the Indo-Chinese sub-region" (PDF). Primate Conservation 8: 187–195.
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  • 66. Streicher, U. and T. Nadler (2003). "Re-introduction of pygmy lorises in Vietnam" (PDF). Reintroduction News, Newsletter of the IUCN Reintroduction Specialist Group 23: 37–40. ISSN 1560-3709.
  • 67. Polet, G. and S. Ling (2004). "Protecting mammal diversity: Opportunities and constraints for pragmatic conservation management in Cat Tien National Park, Vietnam" (PDF). Oryx 38 (2): 186–196. doi:10.1017/S003060530400033X.
  • 68. Dang, H. H. (1998). "Ecology, biology and conservation status of prosimian species in Vietnam". Folia Primatologica 69 (suppl 1): 101–108. doi:10.1159/000052702.
  • 69. Li, W. and H. Wang (1999). "Wildlife trade in Yunnan Province, China, at the Border with Vietnam" (PDF). Traffic Bulletin 18 (1): 21–30.
  • 70. Duckworth, J.; R.E. Salter and K. Khounboline (1999). "Wildlife in Lao PDR, 1999 Status Report" (PDF). Vientiane: IUCN-The World Conservation Union, Wildlife Conservation Society, Centre for Protected Areas and Watershed Management.
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  • Other references
  • Dasgupta, S., U. Deichmann, C. Meisner and D. Wheeler (2005). Where is the poverty-environment nexus? Evidence form Cambodia, Lao PDR, and Vietnam. World Development, 33: 617-638.
  • Fayer, R. and L. Xiao (2008). Cryptosporidium and Cryptosporidiosis, 2nd ed. Boca Raton, FL: CRC Press.
  • Fitch-Snyder, H., M. Jurke, S. Jurke and N. Tornatore (1999). Behavioral and physiological correlates of a breeding colony of pygmy lorises Nycticebus pygmaeus. American Journal of Primatology, 49: 52.
  • Liu, D., ed. (2003). Rehabilitation of Degraded Forests to Improve Livelihoods of Poor Farmers in South China. Bogor, Indonesia: Center for International Forestry Research. ISBN 979-8764-98-6.
  • "Loris, Lesser Slow" (2011). Cleveland Metroparks Zoo. http://www.clemetzoo.com/animals/?action=details&animals_id=1066. MacKinnon, K. (1987). "Conservation status of primates in Malesia, with special reference to Indonesia" (PDF). Primate Conservation 8: 175–183.
  • Nekaris, K. and S. Jaffe. (2007). Unexpected diversity of slow lorises (Nycticebus spp.) within the Javan pet trade: implications for slow loris taxonomy. Contributions to Zoology, 76(3): 187-196.
  • Nekaris, K. A. I and V. Nijman (2007). "CITES proposal highlights rarity of Asian nocturnal primates (Lorisidae: Nycticebus)". Folia Primatologia 78: 211–214. doi:10.1159/000102316.
  • Nekaris, K. A. I.; Shepherd, C. R.; Starr, C. R.; Nijman, V. (2010). "Exploring cultural drivers for wildlife trade via an ethnoprimatological approach: a case study of slender and slow lorises (Loris and Nycticebus) in South and Southeast Asia". American Journal of Primatology 72 (10): 877–886. doi:10.1002/ajp.20842. PMID 20806336.
  • Nijman, V. and K. Nekaris (2010). Checkerboard Patterns, Interspecific Competition, and Extinction: Lessons from Distribution Patters of Tarsiers (Tarsius) and Slow Lorises (Nycticebus) in Insular Southeast Asia. International Journal of Primatology, 31: 1147-1160.
  • Ravosa, M. (1998). Cranial Allometry and Geographic Variation in Slow Lorises. American Journal of Primatology, 45: 225-243.
  • Schulze, H. (2005). "Health database for lorises (Loris, Nycticebus) and pottos (Arctocebus, Perodicticus), prosimian primates" (On-line). Loris Conservation. Accessed May 03, 2011 at http://www.loris-conservation.org/database/disease/index.htm.
  • UNEP-WCMC Species Database: CITES-Listed Species" (2011). http://www.unep-wcmc-apps.org/isdb/CITES/Taxonomy/tax-species-result.cfm/isdb/CITES/Taxonomy/tax-species-result.cfm?Genus=Nycticebus&Species=pygmaeus&source=animals&tabname=legal.
  • Wiens, F., A. Zitzmann, N. Hussein. 2006. Fast Food for Slow Lorises: Is Low Metabolism Related to Secondary Compounds in High-Energy Plant Diet?. Journal of Mammology, 87(4): 790-798.
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Distribution

Range Description

This species is found east of the Mekong River in eastern Cambodia, southernmost China (southeastern Yunnan), Lao PDR, and Viet Nam (Streicher 2004). The western limit of distribution in Lao PDR and Cambodia is uncertain, but it appears to be absent or at least naturally very scarce in the extreme west of the Mekong plain. In China, the species has only been recorded in southeast Yunnan, although it is not clear if these are wild animals or captured animals brought into China from Viet Nam (MacKinnon 2008).
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Geographic Range

Pygmy slow lorises, Nycticebus pygmaeus, are found in Vietnam, Laos, eastern Cambodia, and neighboring regions of southern China (southeast Yunnan province). It is unclear whether populations in China are native or introduced.

Biogeographic Regions: oriental (Native )

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Historic Range:
Indochina

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Range

The pygmy loris occurs in Laos, Vietnam, Cambodia and the Yunnan Province of China (2).
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Physical Description

Morphology

Physical Description

Zoologist J.L. Harrison describes pygmy slow lorises as "rather like a child's teddy-bear." They have thick light brown to deep reddish brown fur with a white or gray underside. Individuals have a unique pattern of lighter and darker colored markings on their face, which commonly include circles around the eyes and dorsal stripes starting at their crown and continuing down their back. During the winter, these markings become more prominent, and they acquire silver tips or "frosting." This seasonal coloration is thought to camouflage and protect the animals, as, during the winter, they must sit in exposed areas such as dense scrub or in the upper branches of trees that lack foliage.

Like other strepsirhine primates and members of the family Lorisidae, pygmy slow lorises have: forward-facing eyes with stereoscopic vision; a rhinarium, the moist naked surface around the nostrils; a tapetum lucidum, the reflective layer in the eye that improves night vision; a split upper lip; nails on all digits except for a grooming claw on the second digit of their feet; a dental formula of 2.1.3.3/2.1.3.3 with the lower incisors and canines forming a toothcomb; no tail; and reduced second digits on their hands.

Pygmy slow lorises and Bengal slow lorises evolved from a common ancestor and are similiar in appearance. The smaller body size in pygmy slow lorises is thought to be the result of character displacement, the accentuation of differences between similar species that share the same geographic distribution.

Pygmy slow lorises measure 15 to 25 cm in length and weigh from 120 to over 500 g (average 400 g). Males are generally larger than females. Members of this species can retard their growth if environmental conditions are not favorable. If their diet is restricted, they lose their juvenile fur and attain adult dentition before attaining adult size.

Pygmy slow lorises produce a toxin from modified sweat glands located near their elbows. They have been observed licking theses glands when alarmed. Their bite can be dangerous to humans; the only account of a pygmy slow loris biting a human resulted in an adult woman entering anaphylactic shock.

Range mass: 120 to 500+ g.

Average mass: 400 g.

Range length: 15 to 25 cm.

Other Physical Features: endothermic ; bilateral symmetry ; venomous

Sexual Dimorphism: male larger

  • Fleagle, J. 1999. Primate Adaptation and Evolution. San Diego, CA: Academic Press.
  • Harrison, J. 1955. The Apes and Monkeys of Malaya (including the Slow Loris). Singapore: Malayan Museum Pamphlets, Government Printing Office.
  • Kalimullah, E., S. Schmidt, M. Schmidt, J. Lu. 2008. Beware the Pygmy Slow Loris? in Abstracts of the 2008 North American Congress of Toxicology Annual Meeting. Clinical Toxicology, 46: 591-645.
  • Ravosa, M. 1998. Cranial Allometry and Geographic Variation in Slow Lorises. American Journal of Primatology, 45: 225-243.
  • Streicher, U. 2004. Aspects of Ecology and Conservation of the Pygmy Loris Nycticebus pygmaeus in Vietnam. Munich, Germany: Dissertation, Ludwig-Maximillans Universitat.
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Ecology

Habitat

Habitat and Ecology

Habitat and Ecology
This species has been sighted in a wide variety of habitats, including primary evergreen and semi-evergreen forest, forest on limestone, secondary and highly degraded habitats, and bamboo thickets (Ratajszczak 1998; Streicher 2004). It is found up to 1,500 m (MacKinnon and MacKinnon 1987).

Nycticebus pygmaeus is nocturnal and forages alone. Its feeding habits have not been well studied in the wild, but it is known that the species is omnivorous in natural conditions. A study of released pygmy loris food choices showed insectivory 40% of the time, gummivory 30% of the time, and feeding on unidentified plant exudates the rest of the time. Flowering trees are most attractive to these animals (Streicher 2004). This species appears to be more insectivorous than Nycticebus coucang, which may explain its ability to survive better in secondary habitat that lack big fruiting trees (Ratajszczak 1998). They may also take geckos, small arboreal mammals, eggs, and chicks (Ratajszczak 1998). This species appears to be a seasonal breeder, giving birth in the winter months (Ratajszczak 1998).

Systems
  • Terrestrial
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Pygmy slow lorises reside in rainforests and degraded habitats as well as bamboo thickets in Vietnam and evergreen forest in Laos. They have been observed at altitudes as great as 1500 m.

Locals in the Mondulkiri province of Cambodia suggest that pygmy slow lorises prefer thick, complex forested areas with bamboo to dry dipterocarp forest, and observations confirm their preference of mixed deciduous to semi-evergreen forests. Individuals of this species are usually seen at heights of 3 to 12 m in the canopy.

Range elevation: 1500 (high) m.

Habitat Regions: tropical

Terrestrial Biomes: forest ; rainforest

  • Ratajszczak, R. 1998. Taxonomy, Distribution and Status of the Lesser Slow Loris Nycticebus pygmaeus and Their Implications for Captive Management. Folia Primatologica, 69(1): 171-174.
  • Starr, C., K. Nekaris, U. Streicher, L. Leung. 2011. Field surveys of the Vulnerable pygmy slow loris Nycticebus pygmaeus using local knowledge in Mondulkiri Province, Cambodia. Fauna & Flora International, Oryx, 45(1): 135-142.
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This tree-dwelling primate inhabits primary and secondary forests (2) (3).
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Trophic Strategy

Food Habits

Reports from local people of Cambodia suggest pygmy slow lorises eat mostly termites, tree parts, fruit, and bamboo. Though surveys confirm they do eat this variety of foods, the absolute preference for termites over the other foods is not clear. There is also great debate over the degree of insectivory in this species. Some suggest that insects make up approximately 33% of their diet (Duke Lemur Center 2011), while others state that they are frugivorous (Fleagle 1999). Although early accounts of the species (Harrison 1955) indicate that members of this species eat insects, lizards, eggs, and "anything edible" in addition to fruit, recent studies do not corroborate these observations.

At the Endangered Primate Rescue Center, captive pygmy slow lorises are offered fruit, vegetables, boiled eggs, milk powder, and insects, and the insects are the most readily accepted food item. However, this finding cannot be used to assert they are not frugivorous, because the cultivated fruit offered to them may not be what they prefer in the wild.

Captive animals also gouge fresh tree branches, indicating a preference for exudates. They have been observed licking Saraca dives, Sapindus and Vernicia montana trees for periods between 1 and 20 minutes. Pygmy slow loris scratch and break the bark of other species of trees, feeding on the gum.

Pygmy slow lorises develop fat stores by increasing their feeding and choosing more energy-rich foods in the last few weeks of autumn. These fat stores are useful during the food scarce winter months.

Despite the high-sugar diet and small body mass of close relatives Sunda slow lorises, they have a very low metabolism. This may be due to a need to detoxify the toxic secondary compounds in their food matter.

Animal Foods: eggs; insects

Plant Foods: fruit; nectar; flowers; sap or other plant fluids

Other Foods: fungus

Primary Diet: carnivore (Insectivore ); herbivore (Frugivore ); omnivore

  • Wiens, F., A. Zitzmann, N. Hussein. 2006. Fast Food for Slow Lorises: Is Low Metabolism Related to Secondary Compounds in High-Energy Plant Diet?. Journal of Mammology, 87(4): 790-798.
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Associations

Ecosystem Roles

Because they may consume a considerable amount of fruit, pygmy slow lorises may play a role in seed dispersal.

In Polish zoos, oocytes of the parasitic protozoan Cryptosporidium, "crypto", have been found in the feces of pygmy slow lorises, indicating infection. Crypto is not typically studied in non-domesticated non-human primates, and little information is available regarding its prevalence.

An outbreak of ocular oxyspirurosis in a Moscow zoo was attributed to a pygmy slow loris from Vietnam. This condition is caused by the parasitic nematode Oxyspirura.

Pygmy slow lorises also act as hosts to some protozoan parasites (Entamoeba histoytica, Blantidium coli, Toxoplasma gondii, Giardia, Blastocystis hominis) and nematodes (Enterobius, Oxyrus, Trichuris).

Commensal/Parasitic Species:

  • Fayer, R., L. Xiao. 2008. Cryptosporidium and Cryptosporidiosis, 2nd ed. Boca Raton, FL: CRC Press.
  • Ivanova, E., S. Spiridonov, O. Bain. 2007. Ocular oxyspirurosis of primates in zoos: intermediate probable origin of ht infection in the Moscow zoo. Parasite, 14(4): 287-298.
  • Schulze, H. 2005. "Health database for lorises (Loris, Nycticebus) and pottos (Arctocebus, Perodicticus), prosimian primates" (On-line). Loris Conservation. Accessed May 03, 2011 at http://www.loris-conservation.org/database/disease/index.htm.
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Predation

Little is known regarding non-human predation of pygmy slow lorises. Although predation by Sumatran orangutans has been reported, the habitats of Sumatran orangutans and pygmy slow lorises do not overlap. Predation by reticulated pythons has also been reported. Pygmy slow lorises are cryptic, blending in well with their surroundings. This may contribute to low non-human predation rates.

Humans are the primary predators of pygmy slow lorises. Their prevalence in Cambodian and Vietnamese markets testifies to the intense hunting pressure on this species. Camobodian locals report hunting pygmy slow loris as a "non-target species," suggesting that the rate of hunting is not affected by abundance and will continue even as these animals become more scarce.

Pygmy slow lorises are easy prey because of their tapetum lucidum, the reflective layer in the eye that improves night vision, which glows when a spotlight is shone in their direction and by some accounts incapacitates them. This makes this species an easy target for night hunters.

Known Predators:

Anti-predator Adaptations: cryptic

  • Wiens, F., A. Zitzmann. 1999. Predation on Wild Slow Loris (Nycticebus coucang) by Reticulated Python (Python reticulatus). Folia Primatologia, 70: 362-364.
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Life History and Behavior

Behavior

Communication and Perception

Pygmy slow lorises utilize a variety of verbal communications. When disturbed, they growl and hiss. They issue a rising tone during general contact and may whistle to the opposite sex during estrus. Mothers softly chirp to their infants, who respond with rapid clicks and squeaks when they are in distress.

Males mark their territory with urine, which also affects mating behavior (See Reproduction: Mating Systems).

Communication Channels: acoustic ; chemical

Other Communication Modes: scent marks

Perception Channels: visual ; acoustic

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Life Expectancy

Lifespan/Longevity

In captivity, pygmy slow lorises are capable of reproduction as old as 14 years of age. They have been known to live 20 years in captivity.

Range lifespan

Status: captivity:
20 (high) years.

Average lifespan

Status: captivity:
17.1 years.

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Lifespan, longevity, and ageing

Maximum longevity: 17.1 years (captivity) Observations: It has been reported that these animals live up to 20 years (Lindenfors 2002), which is possible but has not been confirmed. Record longevity for this species belongs to one male specimen that was at least 17.1 year old, but probably older, when it died in captivity (Richard Weigl 2005).
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Reproduction

Although mating has been observed in captivity, little to nothing is known about mating of pygmy slow lorises in the wild.

Female pygmy slow lorises enter estrus between July and October. During this period, the female vagina and male testes become enlarged. Behavior also differs during this period; females are more likely to approach others and engage in lunging, while males are more likely to sniff and lick a female's genitals and mount them.

Pygmy slow lorises are polygynous. A male's territory typically includes several females with whom he mates. Males and females communicate with one another through whistles. Olfactory cues are also used to find mates. Males spread their scent through urination, and males thus produce more urine than females. Males that spread their scent over a large area have a competitive advantage, because marking territory is an indication of health, persistence, and energy. Females prefer males with a familiar odor to males they have not previously encountered, which may be related to infrequent contact between the sexes.

Mating System: polygynous

Pygmy slow lorises reproduce once every 12 to 18 months. Females enter estrus between July and October. After about 6 months, females give birth to 1 to 2 offspring, generally during the winter months. Twinning is common among this species. Birthing occurs in the open, and infants are born fully formed with fur and open eyes. Offspring are nursed for an average of 4.5 months, though in some cases weaning may take as long as 8 months. Females reach sexual maturity at about 9 months of age, while males reach sexual maturity at 18 to 20 months of age.

Breeding interval: Pygmy slow lorises breed once every 12 to 18 months.

Breeding season: Pygmy slow lorises generally breed from end of July to the beginning of October.

Range number of offspring: 1 to 2.

Average gestation period: 6 months.

Range weaning age: 4 to 8 months.

Average weaning age: 4.5 months.

Average age at sexual or reproductive maturity (female): 9 months.

Range age at sexual or reproductive maturity (male): 18 to 20 months.

Key Reproductive Features: seasonal breeding ; gonochoric/gonochoristic/dioecious (sexes separate); viviparous

Average birth mass: 23 g.

Average gestation period: 188 days.

Average number of offspring: 2.

Average age at sexual or reproductive maturity (female)

Sex: female:
273 days.

Immediately after birth, pygmy slow lorises cling to their mother's underside. Later, mothers exhibit "parking" behavior, leaving their infants in a safe location while they leave to forage for food. Without the burden of a dependent, mothers can more efficiently gather food for themselves and their offspring.

Individuals in the San Diego Zoo have a similiar parenting style to that of other species of slow lorises. However, pygmy slow lorises spend more time in close proximity to their young, tending to huddle, sit or stand within 0.3 m of their offspring more than other species. Mothers and infants primarily establish closeness through passive ventral contact. Although mothers do not appear to directly defend their young, they tolerate the following behavior of their young as they get older. As infants age, they engage more often in adult social behaviors such as grooming and play, and less often in huddling and ventral contact.

Parental Investment: female parental care ; pre-hatching/birth (Provisioning: Female, Protecting: Female); pre-weaning/fledging (Provisioning: Female, Protecting: Female)

  • 2011. "Loris, Lesser Slow" (On-line). Cleveland Metroparks Zoo. Accessed April 27, 2011 at http://www.clemetzoo.com/animals/?action=details&animals_id=1066.
  • Duke Lemur Center. 2011. "Pygmy Slow Loris" (On-line). Duke Lemur Center: Studying and Caring for Lemurs. Accessed April 26, 2011 at http://lemur.duke.edu/category/nocturnal-lemurs/pygmy-slow-loris/.
  • Fisher, H., R. Swaisgood, H. Fitch-Snyder. 2003. Odor familiarity and female preferences for males in a threatened primate, the pygmy loris Nycticebus pygmaeus: applications for genetic management of small populations. Naturwissenchaften, 90: 509-512.
  • Fitch-Snyder, H., A. Ehrlich. 2003. Mother-Infant Interactions in Slow Lorises (Nycticebus bengalensis) and Pygmy Lorises (Nycticbus pygmaeus). Folia Primatologia, 74: 259-271.
  • Fitch-Snyder, H., M. Jurke, S. Jurke, N. Tornatore. 1999. Behavioral and physiological correlates of a breeding colony of pygmy lorises Nycticebus pygmaeus. American Journal of Primatology, 49: 52.
  • Nijman, V., K. Nekaris. 2010. Checkerboard Patterns, Interspecific Competition, and Extinction: Lessons from Distribution Patters of Tarsiers (Tarsius) and Slow Lorises (Nycticebus) in Insular Southeast Asia. International Journal of Primatology, 31: 1147-1160.
  • Ratajszczak, R. 1998. Taxonomy, Distribution and Status of the Lesser Slow Loris Nycticebus pygmaeus and Their Implications for Captive Management. Folia Primatologica, 69(1): 171-174.
  • Streicher, U. 2004. Aspects of Ecology and Conservation of the Pygmy Loris Nycticebus pygmaeus in Vietnam. Munich, Germany: Dissertation, Ludwig-Maximillans Universitat.
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Conservation

Conservation Status

IUCN Red List Assessment


Red List Category
VU
Vulnerable

Red List Criteria
A2cd

Version
3.1

Year Assessed
2008

Assessor/s
Streicher, U., Ngoc Thanh,V., Nadler,T., Timmins, R.J. & Nekaris, A.

Reviewer/s
Mittermeier, R.A. & Rylands, A.B. (Primate Red List Authority)

Contributor/s

Justification
Nycticebus pygmaeus is listed as Vulnerable as the species is believed to have undergone a decline of more than 30% over the last three generations (24 years, given a generation length of 8 years) due primarily to hunting, but also as a result of habitat loss. This species may warrant listing in a higher category of threat if it subsequently shown that the rate of decline is on the order of 50%.

History
  • 2000
    Vulnerable
  • 1996
    Vulnerable
  • 1994
    Vulnerable
    (Groombridge 1994)
  • 1990
    Vulnerable
    (IUCN 1990)
  • 1988
    Vulnerable
    (IUCN Conservation Monitoring Centre 1988)
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Current Listing Status Summary

Status: Threatened
Date Listed: 10/19/1976
Lead Region: Foreign (Region 10) 
Where Listed: Entire


Population detail:

Population location: Entire
Listing status: T

For most current information and documents related to the conservation status and management of Nycticebus pygmaeus , see its USFWS Species Profile

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Pygmy slow lorises are considered threatened by the IUCN. Populations decreased by 30% between 1984 and 2008, and they continue to decline.

Populations of pygmy slow lorises drastically declined during the Vietnam War, as bombing, land clearing by Rome plows, and use of Agent Orange (2,4,5-T), other defoliants, and napalm destroyed the majority of their native habitat in Vietnam, Laos, and Cambodia. Bombing is estimated to have damaged 40% of Vietnamese forests, and herbicides affected 43% of the cultivated area. Prior to the Vietnam War, broad-leafed tropical forests with stands of bamboo and mangroves covered approximately one-half of the land area in these countries.

The use of pygmy slow lorises in traditional medicine, as well as the reluctance of consumers and doctors of traditional medicine to use alternatives, threatens the future of this species.

Lorises are frequently killed by logging and slash and burn agriculture. If they are not killed in the fire, they face habitat destruction, which may lead to their eventual disappearance from the area. The resulting fragmentation of forests further threatens the species.

Pygmy slow lorises were listed in Appendix II by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) in February 1977. They were promoted to Appendix I in September 2007, which indicates trade of this species has not been properly controlled in the last few decades.

Although trade is restricted and capture and transport of pygmy slow lorises is illegal in all countries in their range, their small size makes slow lorises easy to traffic in boxes, baskets, and sacks from country to country. This process is physically stressful for the animals and also threatens their health. Rescue centers have been developed for confiscated slow lorises, but mortality rates remain high. These deaths are attributed to trauma, disease, and atypically close proximity to conspecifics.

US Federal List: threatened

CITES: appendix i

IUCN Red List of Threatened Species: vulnerable

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Status

Classified as Vulnerable (VU) on the IUCN Red List 2007 (1) and listed on Appendix I of CITES (4).
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Population

Population
Ratajszczak (1998) mentioned that hundreds of this species were being traded in markets, but based on the smaller numbers of pygmy lorises now found in Viet Namese markets, as well as the increased difficulty noted in making field encounters, researchers have concluded that wild populations are probably in major decline (Fitch-Snyder and Vu 2002; Streicher 2004). In Phong Nha-Ke Bang National Park, 90 survey nights returned only seven sightings of this species; in Ben En National Park, only eight animals were encountered over ten night walks by four teams, each covering several kilometers per night. In Lao PDR, Duckworth (1994) recorded only four individuals during a survey in Phou Xang He protected area (about 0.05-0.10 individuals/km). It is possible that this species was under-recorded, however, as villagers claimed that this species was common throughout the area, and their accounts may also be historical (Duckworth 1994). The species is widespread in forested areas in Lao PDR, where exploitation of lorises is lower than in neighboring Viet Nam.

Population Trend
Decreasing
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Threats

Major Threats
In Viet Nam, the pygmy slow loris is heavily exploited for traditional “medicine” as well as for the pet trade (Nekaris and Nijman 2007), including international trade, at levels that are not sustainable; it is also used as a food source by many (Streicher 2004). Some hunting involves the use of elaborate traps, as well as snares. In Cambodia, it is generally used for so-called “medicinal” purposes. Levels of exploitation in Lao PDR are significantly lower. Habitat loss, due to agriculture (cashew plantations, corn, rice paddies and so forth), and human settlement, may be resulting in localized declines.
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Although, due to unstable political situations throughout its range, data on the pygmy loris are scarce (3), it is likely that it is threatened by the severe habitat degradation that is occurring in certain areas (3). For example, in Yunnan, China, forest cover has been reduced by 42 percent since the mid-1990s, while in Vietnam, only 30 percent of the original forest cover is left. The threat of habitat loss (the result of logging, military activities and defoliant spraying), is compounded by the impact of hunting. The pygmy loris is hunted for food, the pet trade, and is used in traditional medicines of the Khmer people (the predominant ethnic group in Cambodia). A dramatic increase in trade in recent years has been attributed to human population growth and improving economic situations in the countries in which this vulnerable primate occurs (3).
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Management

Conservation Actions

Conservation Actions
In Viet Nam this species is protected at the highest possible level (Appendix IB, Decree 32, 2006); in China, it is listed as Class 1 protected (involving potentially severe penalties); and in Cambodia it is listed on the Ministry of Forestry and Fisheries Species List as prohibited to hunt from 08 January 1994. The species has been recently transfer from Appendix II to Appendix I of CITES (Nekaris and Nijman 2007). There is a need for close monitoring of harvesting rates of this species, not only in Viet Nam, but also in Cambodia and Lao PDR where rates of take could increase in future.
Pygmy lorises are represented in at least 50 captive collections, and reported in at least two-dozen protected areas, but these reports need to be ground-sourced with systematic surveys (Nekaris et al. 2008).
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Conservation

Hunting and capture of the pygmy loris is illegal in Cambodia, China and Vietnam, although unfortunately, enforcement of these laws is lacking, and the penalties for those breaking the law are too low to deter others (3). Internationally, the pygmy loris receives some protection from the devastating effects of trade by being listed on Appendix I of the Convention on International Trade in Endangered Species (CITES), which prohibits any international commercial trade in this species (4). In addition, the pygmy loris occurs in a number of national parks and nature reserves throughout its range (3), which should hopefully protect some populations from the threat of habitat loss.
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Relevance to Humans and Ecosystems

Benefits

Economic Importance for Humans: Negative

Pygmy slow lorises may produce a toxin from modified sweat glands located near their elbows. They have a toxic bite which is dangerous to humans. The only account of a pygmy slow loris biting a human resulted in the adult woman entering anaphylactic shock.

Negative Impacts: injures humans (bites or stings, poisonous )

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Economic Importance for Humans: Positive

Pygmy slow lorises are commonly used in medicines in Cambodia. In Phnom Penh, they are found in local markets roasted, dried, and made into pre-mixed medicines with rice-wine, alcohol, honey, or charcoal. Doctors of traditional medicine reported in questionnaires that these medicines are primarily used to treat "women after childbirth, stomach problems, wounds, broken bones, and sexually transmitted diseases" (Starr et al. 2010). In the 1950s from Burma to Borneo, the fur of slow lorises was used to dress wounds and cuts because of its blood clotting properties, and it may still be used as such in some localities. Some researchers attribute the popularity of loris medicine to the lack of access to or education about biomedical alternatives and high levels of poverty.

Due to increased protection of this species, market price is increasing. Veteran hunters able to distinguish different species of loris and know species distributions in local forests yield high profits. Trade is driven by wealthy city dwellers who are able and willing to pay rural hunters for their illegal product.

Live trade of slow lorises occurs in high levels in the Mondulkiri, Ratanakiri, and Phnom Penh provinces of Cambodia. As many as 204 lorises were found in a single store in Phnom Penh. Slow lorises are the most popular pets that are listed on CITES Appendix I. They are primarily traded in Borneo, Java, Sumatra, and the surrounding islands. Live trade of slow lorises most commonly affects Sunda slow lorises, Bornean slow lorises, and Javan slow lorises, but traders do not distinguish among species, and other slow lorises such as pygmy slow lorises are sometimes traded as well. This lack of differentiation among species leads to hybridization, improper care and health problems, as well as reintroduction of confiscated animals into improper habitat.

Positive Impacts: pet trade ; source of medicine or drug

  • Dasgupta, S., U. Deichmann, C. Meisner, D. Wheeler. 2005. Where is the poverty-environment nexus? Evidence form Cambodia, Lao PDR, and Vietnam. World Development, 33: 617-638.
  • Nekaris, K., S. Jaffe. 2007. Unexpected diversity of slow lorises (Nycticebus spp.) within the Javan pet trade: implications for slow loris taxonomy. Contributions to Zoology, 76(3): 187-196.
  • Nekaris, K., C. Shepherd, C. Starr, V. Nijman. 2010. Exploring Cultural Drivers for Wildlife Trade via Ethnoprimatological Approach: A Case Study of Slender and Slow Lorises (Loris and Nycticebus) in South and Southeast Asia. American Journal of Primatology, 72: 877-886.
  • Starr, C., K. Nekaris, U. Streicher, L. Leung. 2010. Traditional use of slow lorises Nycticebus bengalensis and N. pygmaeus in Cambodia: an impediment to their conservation. Endangered Species Research, 12: 17-23.
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Wikipedia

Pygmy slow loris

The pygmy slow loris (Nycticebus pygmaeus) is a species of slow loris found east of the Mekong River in Vietnam, Laos, eastern Cambodia, and China. It occurs in a variety of forest habitats, including tropical dry forests, semi-evergreen, and evergreen forests. The animal is nocturnal and arboreal, crawling along branches using slow movements in search of prey. Unlike other primates, it does not leap. It lives together in small groups usually with one or two offspring. An adult can grow to around 19 to 23 cm (7.5 to 9.1 in) long and has a very short tail. It weighs about 450 g (1.0 lb). Its diet consists of fruits, insects, small fauna, tree sap, and floral nectar. The animal has a toxic bite, which it gets by licking a toxic secretion from glands on the inside of its elbows. The teeth in its lower jaw form a comb-like structure called a toothcomb that is used for scraping resin from tree bark.

The pygmy slow loris mates once every 12–18 months and has one or two offspring after an average gestation period of six months. For the first few days, the young loris clings to the belly of its mother. After six months the baby will be weaned, the females reach sexual maturity by 16 months, while the male reaches maturity by about 18 months. The pygmy slow loris is seasonally fertile during the months of July and August. Chemical signals play a role in the reproductive behavior of female pygmy slow lorises. Urine scent markings have a strong characteristic odor and are used to communication information about social relationships.

The habitat of the pygmy slow loris in Vietnam was greatly reduced due to extensive burning, clearing, and defoliating of forests during the Vietnam War. Extensive hunting for traditional medicines is currently putting severe pressure on Cambodian populations. The pygmy slow loris is seriously threatened by hunting, trade, and habitat destruction; consequently, it is listed in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), and in 2006 the International Union for Conservation of Nature (IUCN) classified it as "Vulnerable".

History, taxonomy, and phylogeny[edit]

The pygmy slow loris as illustrated in Bonhote's 1907 description of the species

The pygmy slow loris was first described scientifically by J. Lewis Bonhote in 1907. The description was based on a male specimen sent to him by J. Vassal, a French physician who had collected the specimen from Nha Trang, Vietnam (then called Annam, a French Protectorate) in 1905.[3] In 1939, Reginald Innes Pocock combined all slow lorises into a single species, Nycticebus coucang.[4]

In an influential 1953 publication, primatologist William Charles Osman Hill also consolidated all the slow lorises in one species, Nycticebus coucang, and considered other forms distinct at the subspecies level. Osman Hill thus listed Nycticebus coucang pygmaeus,[5] while acknowledging that "it may be deemed necessary to accede this form specific rank."[6] In 1960, Dao Van Tien reported a species from Hòa Bình Province, Vietnam, that he called N. intermedius,[7] but it turned out that his specimens were merely adults of the pygmy slow loris, which had originally been described on the basis of a juvenile.[8][9] After studying slow lorises from Indochina, primatologist Colin Groves proposed that the pygmy slow loris was morphologically unique enough to be considered a distinct species.[10][11] The validity of this opinion was later corroborated by studies of chromosomal structure,[12] genetic distance determined by protein variation at polymorphic loci,[13] and mitochondrial DNA restriction enzyme analysis.[14][15]

The phylogenetic relationships within the genus Nycticebus have been studied with modern molecular techniques, using DNA sequences derived from the mitochondrial DNA markers D-loop and cytochrome b from 22 slow loris individuals. In this analysis, most of the recognized lineages of Nycticebus, including the pygmy slow loris, were shown to be genetically distinct, and the species was shown to have diverged earlier than the other slow loris species,[16] beginning perhaps 2.7 million years ago.[17] Analysis of nucleotide sequence diversity from individuals taken from the boundary areas between southern China and Vietnam (a region of sympatry between the pygmy slow loris and the Bengal slow loris) show that the pygmy slow loris is not subject to the same introgressive hybridization as the Bengal slow loris (N. bengalensis). The authors of the study suggest that the low polymorphism of pygmy slow lorises may be due to a founder effect, and that the individuals they used in the study originate from an ancestor that lived in middle or southern Vietnam between 1860 and 7350 years ago.[18]

Anatomy and physiology[edit]

Typical facial features include the overall rufous color, brown rings encircling large eyes, a white stripe from the nose to the forehead, and silvery gray hair at the sides of the head.

The pygmy slow loris has a head and body length (measured from the top of the head to the base of the tail) of 195–230 mm (7.7–9.1 in); there is no significant difference in size between the sexes.[19] The length of the skull is less than 55 mm (2.2 in).[20] The tail is short, averaging 1.8 cm (0.71 in) in length.[21] The bodyweight ranges between 360 and 580 grams (13 and 20 oz),[22] with an average mass of 420 grams (15 oz) for males and 428 grams (15.1 oz) for females. There are, however, large seasonal variations in bodyweight, and individuals up to 700 grams (25 oz) have been recorded. The animal tends to have significantly higher bodyweights during the winter months, about 50 percent higher than the lowest values in the summer. The weight gains, achieved largely by increasing food intake, are triggered by changes in the length of the day and night. This seasonal change in bodyweight occurs in both sexes, in both pregnant and non-pregnant females—an adaptation thought to help ensure survival during winter when food resources become scarce.[23] The species has distinctive teeth morphology: its third molar is triangular in outline and only slightly smaller than the first molar; its second molar is the largest.[24] The incisors and canines on its lower jaw are procumbent (tilt forward) and together form a toothcomb that is used in grooming and feeding.[25]

Palatal (left) and lateral (right) views of a pygmy slow loris skull

Like other prosimians, the pygmy slow loris has tapeta lucida in its eyes to assist with night vision.[26] In adults, the rings circling the eyes are seal brown; they are darker in young individuals. There is a white stripe extending from the nose to the forehead, and the sides of the head and upper lip are silvery gray, while the rest of the face and top of the head is rufous.[20] It has small black ears, typically about 23 mm (0.91 in) long,[19] which do not have fur on the tips.[27] On the dorsal side of the animal, a rufous to brownish-black stripe runs from the nape to the middle of the lower back. The upper parts, including the shoulders and upper back, are russet to reddish-buff to brownish, and are sometimes "frosted" with silvery gray white hairs.[20] The presence or absence of a dorsal stripe and silvery hair tips appear to be a seasonal variation and have led some to postulate the existence of an additional species, N. intermedius,[28][29] although DNA analysis has since confirmed this to be an adult version of the pygmy slow loris.[30] The pygmy slow loris has buffy flanks, paler than the back. The upper sides of the arms are ochraceous, and have silvery hairs mingled with the darker ones. The buff legs are also tipped with silvery white hairs. The underparts are plumbeous (lead-colored) at the base, with ochraceous apical portions. The hands and feet are silvery white,[31] with yellowish-white nails.[27] Foot length is relatively consistent, averaging about 45 mm (1.8 in).[32]

The pygmy slow loris has a diploid chromosome number of 2n=50. Although the banding patterns on the chromosomes of all slow lorises are similar, this species may be distinguished from the Bengal slow loris (N. bengalensis) by distinct differences in the number and location of nucleolus organizer regions.[12]

Behavior[edit]

The pygmy slow loris is nocturnal, although it is least active on cold, moonlit nights and is generally active on dark nights, regardless of temperature.[33] In the wild, it is normally encountered alone, or in small groups of two to four individuals.[34] Males use scent marking to defend territories and mark their boundaries. Females prefer to mate with males whose scent is familiar.[35] Males will also countermark—mark over or adjacent to another individual's mark deposited earlier—to advertise competitive ability to females.[36] Females actively prefer countermarking males to males whose odors have been countermarked.[37]

The pygmy slow loris produces an apocrine secretion on scent glands near their elbow (brachial glands). This clear liquid, when mixed with its saliva, creates a volatile, noxious toxin. When startled, the slow loris licks its brachial glands and applies the secretion to its heads.[38] The oily secretion contains a complex mixture of volatile and semi-volatile components; one chemical analysis indicated over 200 components were present.[39] One of the components is a member of the secretoglobin family of proteins,[40] and similar to an allergenic protein found in cat dander.[41] The similarity between the brachial gland secretions and domestic cat allergens may account for anaphylaxis in susceptible individuals.[42]

Vocalizations of the pygmy slow loris include a short whistle, mother-infant contact calls,[43] and a whistling sound produced during estrus.[44]

Reproduction[edit]

The female is mildly aggressive to her suitors during estrus, and will often lunge at males, usually after a long period of being approached and followed. Vocalizations during mating include a whistling sound, most commonly by the female, usually during June and August, coinciding with female estrus. Other vocalizations recorded during estrus include chittering and growling. The testosterone levels of the males are seasonal, with peaks coinciding with female estrogen peaks.[45]

The pygmy slow loris can conceive by 18 months and give birth to its first offspring by two years of age. Studbook records show that the youngest male to sire offspring was around 18 months of age, and the youngest female conceived at 16 months.[46] Gestation length is 184–200 days, and the lactation period lasts 123–146 days.[47] Offspring are weaned at about 24 weeks of age.[48] The pygmy slow loris is monoestrous, experiencing a single four- to five-day period of reproductive activity between late July and early October in captivity,[49] with births occurring from early February to mid-March.[50] As a result, opportunities for mating are rare, and females rely heavily on scent to assess mate quality. Females show a strong preference for familiar-smelling males over novel-smelling males.[51] Research on the process of sexual selection in primates suggests that the exclusive presence of one male's scent in the area is a reliable cue that he is capable of defending the area and/or preventing rival males from marking.[52] Pygmy slow lorises usually have a litter size of one or two; separate studies have reported frequencies of twinning as either 50% or 100% of births.[53] Data collected from a seven-year captive breeding program indicates that they have a skewed birth sex ratio of 1 female to 1.68 males.[18] Because they must divide time equally between offspring, mothers of twins spend less time engaging in social grooming and play with their young,[54] which may lead to a lower infant survival rate.[18] Mothers will "park" their young at one week of age while foraging, and the young begin following their mothers at about two weeks.[55] The life span of the pygmy slow loris is about 20 years.[56]

Diet[edit]

Insect prey can be captured while hanging upside-down from a branch.

The pygmy slow loris is omnivorous, feeding on ants, insects, and fruit. Insects are captured with one or both hands while standing or hanging upside-down from a branch. Insect prey is typically consumed at heights less than 10 m (33 ft).[57] A Vietnamese study concluded that the diet of the pygmy slow loris consists largely of tree exudates (gum) (63%) and animal prey (33%), with other food types making up the remainder.[58] A study on recently reintroduced individuals found similar results—40% insects, 30% gum, and 30% other exudates.[59] The pygmy slow loris will gouge trees to feed on the released exudates.[60] Although tree gum is not as nutrient-rich as its preferred diet, it is available year-round. The pygmy slow loris is a specialized gummivore,[60] a trait that helps it overcome difficulties in finding food during times of shortage. Unable to leap from tree to tree, the pygmy slow loris has a restricted range from which it may obtain food sources. Having generalist dietary preferences allows them to overcome difficult environmental conditions; gum allows them to live at a low energy level with a reduced metabolism.[61] Trees from which exudates are eaten are from the following families: Sapindaceae (Sapindus), Euphorbiaceae (Vernicia), Fabaceae (Saraca), Anacardiaceae (Spondias), and Burseraceae.[22] Feeding on gum takes place over a time period ranging from one to twenty minutes and involves intense licking, sometimes accompanied by audible scratching and bark-breaking sounds. Feeding on exudates usually occurs at heights over 8 m (26 ft).[62] The seasonal color variation that occur in the dorsal stripe of Vietnamese individuals may be related to the need to engage in exudate feeding.[63]

The diet of the pygmy slow loris is seasonal. In north Vietnam, for example, the winter is characterized by low rainfalls and temperatures as low as 5 °C (41 °F), when there is little growth of vegetation in forests, few insects, and limited food resources.[64] The pygmy slow loris will also consume insects that have been exposed by its bamboo-gouging activities. It will use its toothcomb to clean an area of lichens and fungi prior to gouging.[65] The animals conserve energy in the colder winter months by reducing movement, often to the point of complete inactivity.[66]

Habitat and distribution[edit]

The pygmy slow loris is nocturnal and arboreal, and is most commonly found in semi-evergreen, secondary,[67][68][69] and mixed deciduous forests.[70] It is distributed east of the Mekong River in Vietnam, eastern Cambodia, Laos, and Yunnan province in southern China.[71][2] In China it has been recorded only from Pingbian, Hekou, Jinping, and Lüchun counties of Yunnan.[69] In Vietnam, the pygmy slow loris is widespread throughout the country.[72] In Laos, populations have been recorded in Phou Khaokhoay, Nam Kading, Nam Theun, Nakai–Nam Theun, Khammouane Limestone, Dakchung Plateau, and Bolaven Northeast.[69] Its encounter rate, determined from two field studies from Laos and Vietnam combined, was 0.05–0.08 lorises/km.[73] In Cambodia, this value ranged from 0 in Mondulkiri Protected Forest to 0.10 in Phnom Prich Wildlife Sanctuary.[74]

Conservation[edit]

The pygmy slow loris has declined in numbers as a result of extensive habitat degradation throughout its range, including north-eastern Cambodia, the Yunnan Province of China, and Vietnam. In Yunnan province, nearly all primary evergreen forests have vanished and secondary forests have been heavily degraded;[75][76] as of 2005, forest cover has been reduced by 42% since the mid-1990s.[56] The use of defoliants, such as Agent Orange, during the Vietnam War and the ongoing clearing of forests in Vietnam have resulted in a considerable loss of habitat.[77] As of 2003, the forest cover had been reduced to 30% of its original area, with only 10% of the remaining forest consisting of the closed-canopy forests preferred by the pygmy slow loris.[56]

The pygmy slow loris is captured for use in traditional medicine throughout its range.

Due to a combination of unstable political situations in its range, and its nocturnal, arboreal lifestyle, population data for the pygmy slow loris are scarce. The population in China has been estimated at less than 500 individuals.[56] In the 1980s, one estimate placed the population at roughly 72,000 individuals,[78] while another estimate from the same period placed the number around 600–700 individuals.[79] This enormous discrepancy underlines the difficulty to calculate population size without detailed field studies.[56] In Laos, the wildlife status report of 1999 describes the species as "little known" and "common",[80] based on availability of potential habitat. In 2000 the IUCN classified the pygmy slow loris as "Vulnerable",[1] as did the Vietnam Red Data Book the same year. The European Union (EU) (2005) describes the population status in Laos as "apparently widespread, but not common anywhere".[56]

In addition to habitat destruction, the pygmy slow loris is seriously threatened by hunting and trade.[81][79] Within its geographic range and neighbor countries, the trade in the pygmy slow loris has recently increased due to economic changes and human population growth,[82] and the trend is expected to continue.[69] Decreased sightings in the field and at animal markets indicate that wild populations are being depleted since the low reproduction rate of the pygmy slow loris cannot keep pace with these large-scale off-takes.[83][84] Accordingly, conservationists and field biologists fear local extinctions in the near future.[79] Between 1998 and 2006, 70% of pygmy slow lorises seized by authorities died before reaching a sheltering zoo, resulting in replacement demand and additional captures from the wild.[85]

Within the whole Indochinese region, populations of the pygmy slow loris have drastically decreased as a result of military activities, defoliant spraying, logging, and massive off-takes,[86] especially in Vietnam. It has been extirpated in the northern part of this country due to the belief that it is a crop pest.[70] The demand of the pet and the medicinal markets is further aggravating the situation, which is reflected by its abundance in many local markets.[87][79] This demand has recently increased due to human population growth and improved economic conditions within the region. According to CITES, this activity is considered unsustainable.[84]

The population in southern China has been reduced to a few hundred individuals, and by another report, may be locally extinct. The decreasing number of pygmy slow lorises for sale corroborates reports of rapid declines in Vietnamese populations. By 2007, field sightings were becoming scarce, and there were reports that it had disappeared from large parts of its range,[84] particularly in areas with intense logging and agriculture.[88] In Cambodia, widespread declines have been associated with increases in hunting pressure during 2001 and 2002. In one field survey, three areas with high encounter rates in early 2008 were resurveyed in late 2008 and 2009, but no individuals were encountered. This change was thought to be due to both high hunting pressures and gold mine development.[70]

Both the Bengal slow loris and pygmy slow loris are found in more than 20 protected areas, although their populations are either low or insufficiently recorded.[89][1] The pygmy slow loris is protected in most of its range states: in Cambodia, China, and Vietnam. This makes hunting and capture illegal, and in China and Vietnam, possession and storage are also illegal.[90] Under Vietnamese law it has had the highest level of wildlife protection since 1992,[83] all exploitation and use of the pygmy slow loris is illegal.[91] However, enforcement is poor while minor penalties have little deterring effect.[83] In terms of international protection, the species was elevated to Appendix I of CITES in 2007.[2] In addition, since October 2001, the European Union prohibits imports for all wild specimens of pygmy slow loris from Laos and Cambodia for conservation reasons.[91]

The species has been recorded in at least 6 national parks and 12 nature reserves.[72] In China, Daweishan, Fenshuiling, and Huanglianshan Reserve maintained approximately 80% of that country's population of the species in 2007.[92] However, the species is still vulnerable to hunting, even in protected areas.[93] In Laos, the species has been recorded in seven National Biodiversity Conservation Areas.[80]

In Vietnam, confiscated pygmy lorises are usually taken to the Endangered Primate Rescue Centre in Cúc Phương National Park, to be reintroduced into the wild.[92] Non-experts may find it difficult to distinguish between the pygmy slow loris and the Sunda slow loris, as both have similarly reddish fur, which is variable in colors.[94] In international shipments, pygmy lorises may be even mixed up with pottos or lemurs.[92]

Trade[edit]

Pygmy slow lorises obtained from animal markets suffer from stress, neglect, malnutrition, and infection. As a consequence, they seldom live long.

The pygmy slow loris is traded mainly for its purported medicinal properties, for the pet trade, or, to a lesser extent, as food for local consumption.[80][28] According to a 2003 report, the animals were sold for 30,000–50,000 Vietnamese dong (US$1.50–2.50 or €1.10–1.80).[95] Other reports have found them to cost US$2–10.[84] In Cambodia, the species is used in Traditional Khmer Medicine. Surveys conducted at Cambodian markets showed that the species was the third most common mammal for sale, offered at prices ranging from US$0.85–6.25 (€0.65–4.70).[84] In Vietnam, the pygmy slow loris is used for food, medicine, and often as a pet[84] and is among the most frequently sold species. Formerly, hundreds of pygmy lorises were traded monthly in major markets,[88] but recently numbers seem to have decreased, due to shortages in supply.[83] In southern Vietnam, lorises are among the most popular wildlife dishes in wildlife meat restaurants.[96]

Exporting countries reported a total of 111 pygmy slow lorises traded internationally between 1977 and 2004, whereas importing countries reported 131 animals. In Laos, large numbers of native lorises are exported to Vietnam.[80] In Japan, pet shops occasionally offer pygmy slow lorises for US$2,000–3,800 (€1,500–2,800).[91]

There are also parts and derivatives of pygmy lorises in trade, such as the skin and the hair. All parts of the animal are used in traditional Khmer medicine.[84] In Vietnam, medicine such as bone glue of monkey, is mainly produced by local people, but a smaller portion is also destined for restaurants or sold to visitors.[91][95] The species is especially used for the assumed medicinal value of its hair.[91] Traders have reported that they have difficulty keeping pace with demand—one trader claimed to have sold nearly 1,200 pygmy slow lorises during 2001–2002.[97] In Cambodia, the deeply rooted tradition of using the Bengal and pygmy slow loris in traditional medicine is widespread,[98] and the pygmy slow loris is the most commonly requested animal in traditional medicine shops in Cambodia's capital, Phnom Penh.[99]

Illegal trade routes are known to exist from Cambodia, to Laos, Thailand, and Vietnam, with much of this trade destined for China.[87] Surveys from 1998 and 1999 show that 80 to 90 animals were imported from Vietnam though Hekou Port into Yunnan province, making it the most commonly recorded animal in the surveys.[91] China is the primary destination of most Vietnamese slow lorises, although they are also smuggled to other countries,[94] including Taiwan. In one noted incident, 102 animals were confiscated during transit to Ho Chi Minh City in August 1993; of these, only four survived.[100] Pygmy lorises may cost up to US$400 on the Taiwanese pet market. In the USA, occasionally, pygmy lorises smuggled from Vietnam have been confiscated. The Endangered Primate Rescue Centre reports that the pygmy slow loris is the most often rescued species,[91] which reflects their abundance in trade. In Europe, illegal purchases have been reported from Germany, the Netherlands, Poland, and Moscow.[91][87]

In captivity[edit]

The first documented pygmy slow loris in North America was kept at Hawaii's Honolulu Zoo in 1968. In 1986, about 37 pygmy lorises were exported from Vietnam and Laos to Sweden. A year later, several pairs caught from the wild were transferred to zoos in Cincinnati, San Diego, and the Duke Lemur Center.[101] In 1994, the Association of Zoos and Aquariums established a Species Survival Plan for the species, following a proposal by the Global Captive Action Plan for Primates to create a breeding program to maintain its genetic diversity.[102] As of 2008, the captive population in North America had grown to 74 individuals, with most of them born at the San Diego Zoo;[103] as of 2013, the species is the most common lorisid primate kept in North American zoos.[104] About 175 pygmy lorises live in breeding facilities worldwide.[105]

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Literature cited[edit]

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