Bornean slow loris

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Bornean slow loris
Conservation status
CITES Appendix I (CITES)[2]
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primates
Family: Lorisidae
Genus: Nycticebus
Species: N. menagensis
Binomial name
Nycticebus menagensis
(Lydekker, 1893)
Bornean Slow Loris area.png
Range of the Bornean slow loris prior to being split into 4 species in 2013
Synonyms[3]
  • Lemur menagensis Lydekker, 1893
  • Nycticebus philippinus Cabrera, 1908
  • Nycticebus coucang menagensis: Groves, 1971

The Bornean slow loris (Nycticebus menagensis) or Philippine slow loris is a strepsirrhine primate and a species of slow loris that is native to the north and east coastal areas of the island of Borneo, as well as the Sulu Archipelago in the Philippines. The species was first named in 1892, but lumped into the widespread Sunda slow loris (N. coucang) in 1952. However, it was promoted to full species status based on molecular analysis in 2006. In 2013, two former subspecies of the Bornean slow loris were elevated to species status, and a new species—N. kayan—was recognized among the Bornean population.

Weighing 265–300 grams (9.3–10.6 oz), it is one of the smallest of the slow lorises, and can be distinguished from other slow lorises by its pale golden to red fur, the lack of markings on its head, and consistent absence of a second upper incisor. Like other slow lorises, it has a vestigial tail, round head, short ears, a curved grooming claw for grooming, and a gland that produces an oily toxin that the animal uses for defense. The Bornean slow loris is arboreal, nocturnal, and occurs in low densities, making it difficult to locate. It is also the least studied of Indonesia's slow lorises. It is found at elevations between 35–100 meters (115–328 ft) in primary and secondary lowland forest, gardens, and plantations. Information about its diet is limited, but it is suspected to be one of the more insectivorous slow loris species, and is also known to eat gum from woody plants.

The Bornean slow loris was classified as "Vulnerable" by the International Union for Conservation of Nature (IUCN) in 2008, is included in CITES Appendix I, which prevents international commercial trade, and is protected by Indonesian law. Prior to being divided into four distinct species in 2013, it was found in numerous protected areas within its range, making it the least threatened of the slow lorises. However, since the taxonomic split, it may face a higher risk of extinction. It is sparsely distributed throughout its range and is threatened by illegal wildlife trade, including the exotic pet trade, and habitat loss.

Taxonomy and phylogeny[edit]

The Bornean slow loris was first described based on specimens collected by Frank S. Bourns and Dean C. Worcester during the Menage Scientific Expedition to the Philippines and Borneo in the early 1890s. The original collection was made between 5 October and 5 November 1891 near Tataan, Tawi-Tawi Island, in the Philippines,[4] however this type specimen is missing as of 2013.[5] The specimens were given to Henry F. Nachtrieb, President of the Minnesota Academy of Sciences and Chairman of the Zoology Department at the University of Minnesota. Nachtrieb was the first to use the name menagensis in 1892, based on a description of the species sent to him by Worcester in 1891.[6] Worcester's progress report included a description of the specimen and an explanation on how they had obtained it:

I now come to the curious mammal of which I enclose description. Shortly before we left for Tawi Tawi the Jesuit priest here, Padre Marche, informed us that just before our arrival he had made a trip to Tawi Tawi, and had bought of the Moros there a curious animal. He said it has the face of a bear, the hands of a monkey, moved like a sloth, and was called "cocam" by the natives ... I believe nothing of this kind has been found in the Philippines before, and it makes an important addition to the rather meager list of Philippine mammals. It is evidently one of the Lemuridae, but as generic characteristics are not given in the book I have, I cannot go farther.

—Dean C. Worcester[7]

Nachtrieb did not assign the name to a specific genus, noting that it was "an undescribed member of the Lemuridae".[8] The following year, the English naturalist Richard Lydekker published the combination Lemur menagensis in The Zoological Record.[9] This makes Lydekker the authority of the species name menagensis, because he was the first to use the specific name in combination with the name of a genus, although some subsequent authors credited other workers.[10]

In his influential 1953 book Primates: Comparative Anatomy and Taxonomy, the primatologist William Charles Osman Hill placed all the slow lorises in one species, N. coucang.[11] In 1971, however, Colin Groves recognized the pygmy slow loris (N. pygmaeus) as a separate species, and divided N. coucang into four subspecies, including Nycticebus coucang menagensis.[12][13] The Bornean slow loris was elevated to the species level (as Nycticebus menagensis) in 2006 when molecular analysis of DNA sequences of the D-loop and the cytochrome b gene demonstrated it to be genetically distinct from N. coucang.[14] The genetic evidence was corroborated by both a previous study (1998) on morphology (based on craniodental measurements) that indicated distinct differences between the subspecies that were consistent with separation at the species level,[15] and a later study (2010) of facial markings.[16]

Early in its own taxonomic history, distinguishing coloration patterns and size differences resulted in the division of the Bornean slow loris into four subspecies: N. m. bancanus, N. m. borneanus, N. m. menagensis, and N. m. philippinus.[17] These later became taxonomic synonyms, although in 2013 N. bancanus and N. borneanus were elevated to species status based on unique facial markings. Furthermore, a new species—N. kayan—was also identified within the Bornean population.[18][19] The southern Philippine slow lorises (N. m. philippinus or N. philippinus) identified by Spanish zoologist Ángel Cabrera in 1908[20] remains a synonym since the 2013 study was unable to find its type specimen and found no distinguishable characteristics between the Philippine and northern Bornean populations. Additionally, the syntype for N. menagensis was collected by Lydekker in 1893 from the Philippine island of Tawi-Tawi, and Lydekker's species name has precedence under the Principle of Priority.[21]

Physical description[edit]

Like other slow lorises, the tail of the Bornean slow loris is vestigial and it has a round head and short ears.[22] It has a rhinarium (the moist, naked surface around the nostrils of the nose) and a broad, flat face with large eyes. On its front feet, the second digit is smaller than the rest; the big toe on its hind foot opposes the other toes, which enhances its gripping power. Its second toe on the hind foot has a curved grooming claw that the animal uses for scratching and grooming, while the other nails are straight.[23] It also possesses a specialized arrangement of lower front teeth, called a toothcomb, which is also used for grooming, as with other lemuriform primates.[24] It also has a small swelling on the ventral side of its elbow called the brachial gland, which secretes a pungent, clear oily toxin that the animal uses defensively by wiping it on its toothcomb.[25]

The body weight of for the species is typically in the range of 265–300 grams (9.3–10.6 oz),[26] although weights of up to 700 grams (25 oz) have been recorded.[27] One of the smallest of the slow lorises, it can be distinguished from the other species by its pale golden to red fur, light marks on its head, and the consistent lack of a second upper incisor.[15][28] The body length averages 274.2 mm (10.80 in).[29] Its skull length ranges between 54.5 and 56.5 mm (2.15 and 2.22 in),[30] roughly intermediate in size between the smaller pygmy slow loris and the larger Sunda slow loris.[31] The Bornean slow loris always has patches encircling the eye that end just below it. In contrast, the Sunda slow loris is characterized by medium width hair anterior to the opening of the ear, and the Javan slow loris always has a diamond stripe between the eyes.[16] In comparison to the other three species of slow lorises on Borneo, the N. menagensis has very light colored and contrasting facial markings. The rings around the eyes are either rounded or diffused-edged on top, while the bottom occasionally extends down below the zygomatic arch. The stripe between its eyes is narrow, the ears usually lack fur, the patch on the top of the head is mostly diffused, and the band of fur in front of the ears varies in width.[29]

Distribution[edit]

Following the taxonomic split in 2013 of the four species of slow loris in Borneo, N. menagensis is now restricted to the north and east coastal areas in the provinces of Brunei, Sabah, and East Kalimantan. It is also found on the southern Philippine Islands, known as the Sulu Archipelago,[29] and may be found on other nearby islands, such as the Banggi Island off Sabah.[32] In the Sulu Archipelago, it occurs in the Tawi-Tawi Group, in the west of the archipelago, including the islands of Tawi-Tawi, Bongao, Sanga-Sanga, Simunul, and possibly other small islands. It does not occur on the island of Jolo, further to the east, and although it has been recorded from Mindanao—a large island in the southern Philippines—the record was in error.[33] The species may be extinct on some Philippine islands, but is likely to persist on the smaller islands.[1] Because the species is so popular as a pet, zoologists Guy Musser and Lawrence Heaney suggested in 1985 that the Philippine populations may have been introduced there by humans.[34]

It is considered to be sympatric with N. kayan.[29] Fossils of this species have been found in the Late Pleistocene site of Niah in Sarawak.[35]

Habitat and ecology[edit]

The Bornean slow loris is the least studied of Indonesia's slow lorises.[36] In a field study at the Sabangau National Park in Central Kalimantan, only 12 slow loris sightings were made over a 75-day period.[37] All were seen in the trees at heights of 15–20 m (49–66 ft). They were encountered singly, as mother and offspring, or in adult trios. Of the two trios, both were on fruiting trees, Calophyllum hosei and Syzygium cf. nigricans. In another survey conducted at Wehea Forest, East Kalimantan, only one Bornean slow loris—seen at a height of 30 m (98 ft)—was encountered in an area of more than 30 km2.[1] Other surveys confirm that the animal is difficult to locate, and occurs in low densities.[38][39][40]

The species occurs in primary and secondary lowland forest, gardens, and plantations, at elevations between 35–100 m (115–328 ft). Interviews conducted with Philippines locals indicate that it is commonly seen in citrus trees (calamansi), and may be tolerant of a variety of habitats. It is nocturnal, and almost entirely arboreal.[1] Although data on diet is limited, based on cranial size and morphology, the Bornean slow loris is suspected to be one of the more insectivorous slow loris species.[41] It has also been observed feeding on the gum from an unidentified liana (a long-stemmed woody vine).[27]

Conservation[edit]

In a 2005 report on the effect of logging on wildlife conservation in Indonesia, the authors claimed the Bornean slow loris to be "common" throughout Borneo.[42] However, as pointed out by Nekaris and colleagues, this assessment was based on field research data and historic museum specimens, and cannot be considered reliable, as "loris ‘presence’ is usually not determined first-hand, and it also cannot be presumed that lorises still occur in areas from where they were once collected."[43] The species appears to be uncommon throughout its range, including a very limited distribution in the Philippines. Surveys have demonstrated that, compared to other slow loris species, the Bornean slow loris is rare, and sparsely distributed throughout its range.[44]

The Bornean slow loris is listed in CITES Appendix I, which prevents international commercial trade; it is also protected by Indonesian law. The species is often confused with other slow lorises in animal rescue centers, as it is not well-covered in field guides. The species occurs in a number of protected areas throughout its range, including some fragmented forests.[1] Threats to the species include the illegal local exotic pet trade[40][45] and habitat loss due to burning and conversion to palm oil plantations. Additionally, uncontrolled release of pets in some areas is also a threat to the species.[1]

Prior to being split into four species in 2013, the Bornean slow loris was among the least threatened of the slow lorises,[1] and its situation was considered to be good due to its presence in a high percentage of "low risk" areas on Borneo.[46] It was classified as "Vulnerable" by the IUCN, who consider there to have been a greater than 30% reduction in population between roughly 1984 and 2008, based on harvesting for the pet trade and extensive habitat loss.[1] Because that species has been divided into four distinct species since the 2008 IUCN assessment, each of the new species faces a higher risk of extinction. Accordingly, each of them are expected to be listed as "Vulnerable" at the least, with some of them likely to be assigned to a higher-risk category.[47]

References[edit]

  1. ^ a b c d e f g h Nekaris, A. & Streicher, U. (2008). "Nycticebus menagensis". IUCN Red List of Threatened Species. Version 2010.4. International Union for Conservation of Nature. Retrieved 23 January 2011. 
  2. ^ "Appendices I, II and III" (PDF). Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). 2010. 
  3. ^ Nekaris & Jaffe 2007, p. 188.
  4. ^ Timm & Birney 1992, p. 679.
  5. ^ Munds, Nekaris & Ford 2013, pp. 51 & 53.
  6. ^ Timm & Birney 1980, p. 680.
  7. ^ Worcester & Bourns 1905, p. 149.
  8. ^ Nachtrieb 1892.
  9. ^ Lydekker 1893, pp. 24–25.
  10. ^ Timm & Birney 1992, p. 682.
  11. ^ Osman Hill 1953, pp. 156–163.
  12. ^ Groves 1971.
  13. ^ Groves 2001, p. 99.
  14. ^ Chen et al. 2006, p. 1198.
  15. ^ a b Ravosa 1998.
  16. ^ a b Nekaris & Munds 2010.
  17. ^ Munds, Nekaris & Ford 2013, p. 47.
  18. ^ Munds, Nekaris & Ford 2013, p. 46.
  19. ^ Walker, M. (13 December 2012). "Primate species: new slow loris found in Borneo". BBC News. Archived from the original on 24 December 2012. 
  20. ^ Cabrera 1908, pp. 136–137.
  21. ^ Munds, Nekaris & Ford 2013, p. 49.
  22. ^ Management Authority of Cambodia (3–15 June 2007). "Notification to Parties: Consideration of Proposals for Amendment of Appendices I and II" (PDF). Netherlands: CITES. p. 31. Archived from the original on 8 January 2011. Retrieved 9 January 2011. 
  23. ^ Smith & Xie 2008, pp. 159–160.
  24. ^ Ankel-Simons 2007, p. 246.
  25. ^ Hagey, Fry & Fitch-Snyder 2007, p. 253.
  26. ^ Nekaris, Blackham & Nijman 2008, p. 734.
  27. ^ a b Nekaris et al. 2010, p. 157.
  28. ^ Chen et al. 2006.
  29. ^ a b c d Munds, Nekaris & Ford 2013, p. 53.
  30. ^ Groves 2001, p. 98.
  31. ^ Groves 1998, p. 24.
  32. ^ Nor 1996, p. 28.
  33. ^ Fooden 1991, p. 287.
  34. ^ Musser & Heaney 1985, p. 30.
  35. ^ Tougard 2001.
  36. ^ Nekaris & Munds 2010, p. 21.
  37. ^ Nekaris, Blackham & Nijman 2008, p. 737.
  38. ^ Wells et al. 2004.
  39. ^ Duckworth 1997.
  40. ^ a b Munds et al. 2008.
  41. ^ Ravosa 1998, p. 239.
  42. ^ Meijaard et al. 2005, p. 242.
  43. ^ Nekaris, Blackham & Nijman 2008, p. 735.
  44. ^ Nekaris, Blackham & Nijman 2008, p. 744.
  45. ^ Braun, D. (2010). "Love potions threaten survival of lorises". National Geographic. Archived from the original on 9 January 2011. Retrieved 9 January 2011. 
  46. ^ Thorn et al. 2009, p. 295.
  47. ^ Wall, T. (13 December 2012). "Three new species of venomous primate identified by MU researcher". Missouri University News Bureau. Archived from the original on 24 December 2012. Retrieved 19 December 2012. 

Literature cited[edit]