Slow Loris

**Slow lorises** are a group of several species of nocturnal strepsirrhine primates which make up the genus ***Nycticebus***. Found in Southeast Asia and bordering areas, they range from Bangladesh and Northeast India in the west to the Sulu Archipelago in the Philippines in the east, and from Yunnanprovince in China in the north to the island of Java in the south. Although many previous classifications recognized as few as a single all-inclusive species, there are now at least eight that are considered valid: the Sunda slow loris (*N. coucang*), Bengal slow loris (*N. bengalensis*), pygmy slow loris(*N. pygmaeus*), Javan slow loris (*N. javanicus*), Philippine slow loris (*N. menagensis*), Bangka slow loris (*N. bancanus*), Bornean slow loris (*N. borneanus*), and Kayan River slow loris (*N. kayan*). The group's closest relatives are the slender lorises of southern India and Sri Lanka. Their next closest relatives are the African lorisids, the pottos, false pottos, and angwantibos. They are less closely related to the remaining lorisoids (the various types of galago), and more distantly to the lemurs of Madagascar. Their evolutionary history is uncertain since their fossil record is patchy and molecular clock studies have given inconsistent results.

Slow lorises have a round head, a narrow snout, large eyes, and a variety of distinctive coloration patterns that are species-dependent. Their arms and legs are nearly equal in length, and their trunk is long and flexible, allowing them to twist and extend to nearby branches. The hands and feet of slow lorises have several adaptations that give them a pincer-like grip and enable them to grasp branches for long periods of time. Slow lorises have a toxic bite, a trait rare among mammals and unique to lorisid primates. The toxin is obtained by licking a gland on their arm, and the secretion is activated by mixing with saliva. Their toxic bite is a deterrent to predators, and the toxin is also applied to the fur during grooming as a form of protection for their infants. The secretion from the arm contains a chemical related to cat allergen, but may be augmented by secondary toxins from the diet in wild individuals. Slow lorises move slowly and deliberately, making little or no noise, and when threatened, they stop moving and remain motionless. Their only documented predators—apart from humans—include snakes, changeable hawk-eagles and orangutans, although cats, civets and sun bears are suspected. Little is known about their social structure, but they are known to communicate by scent marking. Males are highly territorial. Slow lorises reproduce slowly, and the infants are initially parked on branches or carried by either parent. They are omnivores, eating small animals, fruit, tree gum, and other vegetation.

Each of the slow loris species that had been identified prior to 2012 is listed as either "Vulnerable" or "Endangered" on the IUCN Red List. The three newest species are yet to be evaluated, but they arise from (and further reduce the ranks of) what was thought to be a single "vulnerable" species. All four of these are expected to be listed with at least the same, if not a higher-risk, conservation status. All slow lorises are threatened by the wildlife trade and habitat loss. Their habitat is rapidly disappearing and becoming fragmented, making it nearly impossible for slow lorises to disperse between forest fragments; unsustainable demand from the exotic pet trade and from traditional medicine has been the greatest cause for their decline. Deep-rooted beliefs about the supernatural powers of slow lorises, such as their purported abilities to ward off evil spirits or to cure wounds, have popularized their use in traditional medicine. Despite local laws prohibiting trade in slow lorises and slow loris products, as well as protection from international commercial trade under Appendix I, slow lorises are openly sold in animal markets in Southeast Asia and smuggled to other countries, such as Japan. Due in part to the large eyes that are an adaptation to their nocturnal lifestyle, they have also been popularized as 'cute' pets in viral videos on YouTube. Slow lorises have their teeth cut or pulled out for the pet trade. They make poor pets that are difficult to care for, and often die from infection, blood loss, improper handling or inadequate nutrition.

## Anatomy and Physiology

Slow lorises have a round head because their skull is shorter than in other living strepsirrhine. Like other lorisids, its snout does not taper towards the front of the face as it does in lemurs, making the face appear less long and pointed. Compared to the slender lorises, the snout of the slow loris is even less pointed. As with other members of Lorisidae, its interorbital distance is shorter than in lemurs. The skull has prominent crests (ridges of bone). A distinguishing feature of the slow loris skull is that the occipital bone is flattened and faces backward. The foramen magnum (hole through which the spinal cord enters) faces directly backward. The brains of slow lorises have more folds (convolutions) than the brains of galagos.

The ears are small, sparsely covered in hair, and hidden in the fur. Similar to the slender lorises, the fur around and directly above the eyes is dark. Unlike the slender lorises, however, the white stripe that separates the eye rings broadens both on the tip of the nose and on the forehead while also fading out on the forehead. Like other strepsirrhine primates, the nose and lip are covered by a moist skin called the rhinarium ("wet nose"), which is a sense organ. The eyes of slow lorises are forward-facing, which gives stereo vision. Their eyes are large and possess a reflective layer, called the tapetum lucidum, that improves low-light vision. It is possible that this layer blurs the images they see, as the reflected light may interfere with the incoming light. Slow lorises have monochromatic vision, meaning they see in shades of only one color. They lack the opsin gene that would allow them to detect short wavelength light, which includes the colors blue and green.

The dental formula of slow lorises is 2.1.3.32.1.3.3 × 2 = 36, meaning that on each side of the mouth there are two upper (maxillary) and lower (mandibular) incisors, one upper and lower canine tooth, three upper and lower premolars, and three upper and lower molars, giving a total of 36 permanent teeth. As in all other crownstrepsirrhines, their lower incisors and canine are procumbent (lie down and face outwards), forming a toothcomb, which is used for personal and social groomingand feeding. The toothcomb is kept clean by the sublingua or "under-tongue", a specialized structure that acts like a toothbrush to remove hair and other debris. The sublingua extends below the tip of the tongue and is tipped with keratinized, serrated points that rake between the front teeth.

Slow lorises have relatively large maxillary canine teeth, their inner (mesial) maxillary incisors are larger than the outer (distal) maxillary incisors, and they have a diastema (gap) between the canine and the first premolar. The first mandibular premolar is elongated, and the last molar has three cusps on the crown, the shortest of which is near the back. The bony palate (roof of the mouth) only goes as far back as the second molar.

Slow lorises range in weight from the Bornean slow loris at 265 grams (9.3 oz) to as much as 2,100 grams (74 oz) for the Bengal slow loris. Slow lorises have stout bodies, and their tails are only stubs and hidden beneath the dense fur. Their combined head and body lengths vary by species, but range from 18 to 38 cm (7.1 to 15.0 in) between all species. The trunk is longer than in other living strepsirrhines because they have 15–16 thoracic vertebrae, compared to 12–14 in other living strepsirrhines. This gives them greater mobility when twisting and extending towards nearby branches. Their other vertebrae include seven cervical vertebrae, six or seven lumbar vertebrae, six or seven sacral vertebrae, and seven to eleven caudal vertebrae.

Slow lorises have a powerful grasp with both their hands and feet due to several specializations. They can tightly grasp branches with little effort because of a special muscular arrangement in their hands and feet, where the thumb diverges at nearly 180° from the rest of the fingers, while the hallux(big toe) ranges between being perpendicular and pointing slightly backwards. The toes have a large flexor muscle that originates on the lower end of the thigh bone, which helps to impart a strong grasping ability to the hind limbs. The second digit of the hand is short compared to the other digits, while on the foot, the fourth toe is the longest. The sturdy thumb helps to act like a clamp when digits three, four, and five grasp the opposite side of a tree branch. This gives their hands and feet a pincer-like appearance. The strong grip can be held for hours without losing sensation due to the presence of a rete mirabile (network of capillaries), a trait shared among all lorises. Both slender and slow lorises have relatively short feet. Like nearly all lemuriforms, they have a grooming claw on the second toe of each foot.

Slow lorises have an unusually low basal metabolic rate, about 40% of the typical value for placental mammals of their size, comparable to that of sloths. Since they consume a relatively high-calorie diet that is available year-round, it has been proposed that this slow metabolism is due primarily to the need to eliminate toxic compounds from their food. For example, slow lorises can feed on *Gluta* bark, which may be fatal to humans.

## Distribution and Diversity

Slow lorises are found in South and Southeast Asia. Their collective range stretches from Northeast India through Indochina, east to the Sulu Archipelago (the small, southern islands of the Philippines), and south to the island of Java (including Borneo, Sumatra, and many small nearby islands). They are found in India (Northeastern states), China (Yunnan province), Laos, Vietnam, Cambodia, Bangladesh, Burma, Thailand, Malaysia, the Philippines, Indonesia, Brunei, and Singapore.

There are currently eight recognized species. The pygmy slow loris (*N. pygmaeus*) occurs east of the Mekong River in Yunnan, Laos, Vietnam, and Cambodia. The Bornean slow loris(*N. menagensis*), found on Borneo and nearby islands, including the Sulu Archipelago, and in 2012 was split into four distinct species (adding *N. bancanus*, *N. borneanus*, and *N. kayan*). The Javan slow loris (*N. javanicus*) is only found on the island of Java in Indonesia. The Sunda slow loris (*N. coucang*) occurs on Sumatra and the Malay Peninsula, including Singapore and southern Thailand (the Isthmus of Kra). The Bengal slow loris (*N. bengalensis*) has the largest distribution of all the slow lorises and can be found in Bangladesh, Cambodia, southern China, Northeast India, Laos, Burma, Thailand, and Vietnam.

Slow lorises range across tropical and subtropical regions and are found in primary and secondary rainforests, as well as bamboo groves and mangrove forests. They prefer forests with high, dense canopies, although some species have also been found in disturbed habitats, such as cacao plantations and mixed-crop home gardens. Due largely to their nocturnal behavior and the subsequent difficulties in accurately quantifying abundance, data about the population size or distribution patterns of slow lorises is limited. In general, encounter rates are low; a combined analysis of several field studies involving transect surveys conducted in South and Southeast Asia determined encounter rates ranging from as high as 0.74 lorises per kilometer for *N. coucang* to as low as 0.05 lorises per kilometer for *N. pygmaeus*.

## Behavior and Ecology

Little is known about the social structure of slow lorises, but they generally spend most of the night foraging alone. Individuals sleep during the day, usually alone but occasionally with other slow lorises. Home ranges of adults may significantly overlap, and those of males are generally larger than those of females. In the absence of direct studies of the genus, primatologist Simon Bearder speculated that slow loris social behavior is similar to that of the potto, another slow-moving nocturnal primate. Such a social system is distinguished by a lack of matriarchy and by factors that allow the slow loris to remain inconspicuous and minimize energy expenditure. Vocal exchanges and alarm calls are limited; scent marking with urine is the dominant form of communication. Adult males are highly territorial and are aggressive towards other males. Vocalizations include an affiliative (friendly) call *krik*, and a louder call resembling a crow's caw. When disturbed, slow lorises can also produce a low buzzing hiss or growl. To make contact with other individuals, they emit a single high-pitched rising tone, and females use a high whistle when in estrus.

Slow lorises are slow and deliberate climbers, and often hold on to branches with three of their four limbs. To move between trees, they carefully grip the terminal branches of the neighboring tree and pull themselves across the small gap. They will also grip branches with only their hind feet, lift themselves upright, and quickly launch forward with their hands to catch prey. Due to their slow movement, all lorises, including the slow lorises, have a specially adapted mechanism for defense against predation. Their slow, deliberate movement hardly disturbs the vegetation and is almost completely silent. Once disturbed, they immediately stop moving and remain motionless. In Indonesia, slow lorises are called *malu malu* or "shy one" because they freeze and cover their face when spotted. If cornered, they may adopt a defensive posture by curling up and lunging at the predator. The Acehnese name, *buah angin* ("wind monkey"), refers to their ability to "fleetingly but silently escape". Little is known about the predation of slow lorises. Documented predators include snakes, the changeable hawk-eagle(*Nisaetus cirrhatus*), and Sumatran orangutans (*Pongo abelii*). Other potential predators include cats, sun bears (*Ursus malayanus*), binturongs(*Arctictis binturong*), and civets.

Slow lorises produce a secretion from their brachial gland (a scent gland on the upper arm near the axilla) that is licked and mixed with their saliva. In tests, three predators—binturongs, clouded leopards (*Neofelis nebulosa*), and sun bears—retreated or showed other signs of displeasure when presented with cotton swabs anointed with a mixture of the toxic secretion and the saliva, whereas the toxic secretion alone generated mild interest. Before stashing their offspring in a secure location, female slow lorises will lick their brachial glands, and then groom their young with their toothcomb, depositing the toxin on their fur. When threatened, slow lorises may also lick their brachial glands and bite their aggressors, delivering the toxin into the wounds. Slow lorises can be reluctant to release their bite, which is likely to maximize the transfer of toxins. This toxic bite is a rare trait among mammals and unique to lorisid primates. It may also be used for defense against other slow lorises and parasites. According to Nekaris, this adaptation—along with vocalizations, movement, and coloration patterns similar to those of true cobras—may have evolved through Müllerian mimicry to protect slow lorises when they need to move across the ground due to breaks in the canopy.

According to folklore, brachial gland secretions are generally thought to contain venom because of apparent anaphylactic reactions by humans following their bites. Slow lorises can indeed inflict painful bites. Animal dealers in Southeast Asia keep tanks of water nearby so that in case of a bite, they can submerge both their arm and the slow loris to make the animal let go. The secretion from the brachial gland of captive slow lorises is similar to the allergen in cat dander, hence the secretions may merely elicit an allergic reaction, not toxicosis. Loris bites cause a painful swelling, and the single case of human death reported in the scientific literature was believed to have resulted from anaphylactic shock. However, although the toxin is only produced when the brachial secretion and saliva are mixed, both the secretion and saliva may have unique chemical properties and may act separately. Furthermore, secondary toxins may be introduced from the consumption of wild food, augmenting the toxicity. The combined brachial secretion and saliva of recently captured wild lorises was shown to contain batrachotoxins, which were not found in slow lorises held in captivity for more than a year.

Studies suggest that slow lorises are polygynandrous. Infants are either parked on branches while their parents find food or else are carried by one of the parents. Due to their long gestations (about six months), small litter sizes, low birth weights, long weaning times (three to six months), and long gaps between births, slow loris populations have one of the slowest growth rates among mammals of similar size. Pygmy slow lorises are likely to give birth to twins—from 50% to 100% of births, depending on the study; in contrast, this phenomenon is rare (3% occurrence) in Bengal slow lorises. A seven-year study of captive-bred pygmy slow lorises showed a skewed sex distribution, with 1.68 males born for every 1 female.

Breeding may be continuous throughout the year. Copulation often occurs while suspended with the hands and feet clinging to horizontal branches for support. In captive Sunda slow lorises, mating primarily occurs between June and mid-September, with the estrus cycle lasting 29 to 45 days and estrus lasting one to five days. Likewise, gestation lasts 185 to 197 days, and the young weigh between 30 and 60 grams (1.1 and 2.1 oz) at birth. Females reach sexual maturityat 18 to 24 months, while males are capable of reproducing at 17 months. However, the fathers become hostile towards their male offspring after 12 to 14 months and will chase them away. In captivity, they can live 20 or more years.

### **Diet**

Slow lorises are omnivores, eating insects, other arthropods, small birds and reptiles, eggs, fruits, gums, nectar and miscellaneous vegetation. A 1984 study of the Sunda slow loris indicated that its diet consists of 71% fruit and gums, and 29% insects and other animal prey. A more detailed study of another Sunda slow loris population in 2002 and 2003 showed different dietary proportions, consisting of 43.3% gum, 31.7% nectar, 22.5% fruit, and just 2.5% arthropods and other animal prey. The most common dietary item was nectar from flowers of the Bertram palm (*Eugeissona tristis*). The Sunda slow loris eats insects that other predators avoid due to their repugnant taste or smell.

Preliminary results of studies on the pygmy slow loris indicate that its diet consists primarily of gums and nectar (especially nectar from *Saraca dives* flowers), and that animal prey makes up 30–40% of its diet. However, one 2002 analysis of pygmy slow loris feces indicated that it contained 98% insect remains and just 2% plant remains. The pygmy slow loris often returns to the same gum feeding sites and leaves conspicuous gouges on tree trunks when inducing the flow of exudates. Slow lorises have been reported gouging for exudates at heights ranging from 1 m (3 ft 3 in) to as much as 12 m (39 ft); the gouging process, whereby the loris repetitively bangs its toothcomb into the hard bark, may be loud enough to be heard up to 10 m (33 ft) away. The marks remaining after gouging can be used by field workers to assess loris presence in an area. Captive pygmy slow lorises also make characteristic gouge marks in wooden substrates, such as branches. It is not known how the sympatric pygmy and Bengal slow lorises partition their feeding niches. The plant gums, obtained typically from species in the family Fabaceae (peas), are high in carbohydrates and lipids, and can serve as a year-around source of food, or an emergency reserve when other preferred food items are scarce. Several anatomical adaptations present in slow lorises may enhance their ability to feed on exudates: a long narrow tongue to make it easier to reach gum stashed in cracks and crevices, a large cecum to help the animal digest complex carbohydrates, and a short duodenum to help quickly pass potentially toxic exudates. Slow lorises can use both hands to eat while hanging upside down from a branch. They spend about 20% of their nightly activities feeding.