Mother-infant interactions in captive slow lorises (Nycticebus coucang)

Information is presented about mother-infant interactions and infant development in a rarely studied prosimian primate, the slow loris (Nycticebus coucang). Four dyads were observed, by means of closed circuit TV, in a semi-natural environment for 1 hour per day three times a week. Infants were inactive for the first 6–8 weeks. Although mothers carried infants, they also left them alone for substantial periods of time after the 1st week. Over the 20-week study period, there was a significant decline in ventral contact but not in sitting within 12 inches or engaging in active social interactions. By the end of the study, infants were not yet fully independent. Three of the 4 were primarily responsible for maintaining physical closeness to the mother; they made most of the approaches and mothers made most of the departures. However, only 2 of the 4 infants had assumed responsibility for the initiation and maintenance of social interactions with the mother. By comparison with other nocturnal prosimians of similar size, the rate of development is relatively slow. Unlike many anthropoids, mothers were not strongly protective or rejecting. They did not bring infants back to a fixed location or try to prevent infants from leaving them; and the decline in ventral contact was not accompanied by fights between the pair. The 3 group-living mothers were more protective than the single individually housed mother, and it would seem advisable to isolate mother-infant pairs in laboratory breeding colonies.     

Energy metabolism and thermoregulation in pygmy lorises (Nycticebus pygmaeus) from Yunnan Daweishan Nature Reserve

The pygmy loris (Nycticebus pygmaeus) is a small prosimian living in Vietnam, Laos, eastern Cambodia and the south part of China. In China it is only found in Pingbian, Hekou, Jinping, Luchun of Yunnan. As N. pygmaeus is seriously threatened by hunting, trade and habitat destruction, it is listed in Appendix II of CITES, and in 2006 the IUCN classified it as “vulnerable”. In order to understand the characteristics of energy metabolism and thermoregulation of N. pygmaeus, the resting metabolic rate (RMR) and body temperature (T_b) at different ambient temperature (T_a) of pygmy lorises, as well as body mass, energy intake, digestable energy intake, digestability and the thermal conductance were measured in captivity. The results obtained mainly are as follows: (1) Pygmy loris feed dry food averaged 12.90 ± 1.02 g/d. They could gain 214.87 ± 16.65 kJ/d from food intake, and earned 200.15 ± 16.36 kJ digestable energy intake per day with 90.13 ± 1.34% of the digestability. (2) The T_b at room temperatures was a little low (35.23 ± 0.16 °C) and varied with T_a from 25 °C to 35 °C. There was a positive relationship between T_b and T_a, which was described as: T_b = 27.22 + 0.34T_a (r = 0.880). (3) The resting metabolic rate (RMR) of the pygmy loris was 0.3844 ± 0.0162 mlO₂/g/h, which was 51.91 ± 1.90% of the previous predicted rate by Kleiber (1961) [21]. (4) The average thermal conductance of the pygmy loris (N. pygmaeus) was 0.0449 ± 0.0031 mlO₂/g/h/°C. These characteristics of energy metabolism and thermoregulation of N. pygmaeus in Yunnan Daweishan Nature Reserve might be considered as the adaptive characteristics to their environment in tropical semi-evergreen forests and secondary forests.     

Reproductive patterns in pygmy lorises (Nycticebus pygmaeus): Behavioral and physiological correlates of gonadal activity

The purpose of this study was to evaluate behavioral and physiological parameters of reproduction in a breeding colony of pygmy lorises. To this end, nine male and eight female adult pygmy lorises were kept under natural lighting conditions and monitored through five consecutive breeding seasons. Behavioral data were collected continuously throughout the year on all loris pairs. Behaviors associated with estrogen peaks in females included approaches, leaves, and lunges by females. Whistles were more frequent during estrus, but there was high inter‐individual variability. Males responded to estrous females by persistent following. There was a higher percentage of births in pairs that were together for more than 30 days before onset of estrus, compared with pairs that were put together when females came into estrus. However, these results may have been influenced by factors such as previous familiarity and social compatibility. Fecal testosterone levels were measured using radioimmunoassays and correlated with estrogen peaks and labial swelling of the females. The data showed an annual rhythm in testosterone that was consistent with a July–August mating season. Captive births were significantly higher during January–April than they were during any other months of the year. The earliest testosterone peak in a juvenile male was detected at 58 weeks, while the youngest male to sire offspring was 73 weeks of age at the time of the conception. Zoo Biol 22:15–32, 2003. © 2003 Wiley‐Liss, Inc.     

Learning set formation in slow lorises (Nycticebus coucang)

In primates, learning set formation has been reported in various simian species, but in only few prosimian species. The formation of visual discrimination learning set was tested on a nocturnal prosimian species, slow lorises (Nycticebus coucang). Their performance was higher than that of some New World monkeys. This confirmed the suggestion from the data on black lemurs (Lemur macaco) that there is an overlap between prosimians and simians in learning set ability.     

Cranial allometry and geographic variation in slow lorises (Nycticebus)

A series of 20 craniodental measurements was obtained for two sister taxa: Nycticebus coucang (common slow loris) and N. pygmaeus (pygmy slow loris). Multivariate analysis of variance was performed with adult data to describe patterns of subspecific and specific variation in this genus. The geometric mean of adult cranial dimensions was compared to field data on latitudinal coordinates for available specimens to investigate if size variation in Nycticebus is clinal in nature. Ontogenetic series for larger-bodied N. coucang and smaller-bodied N. pygmaeus were compared to test the hypothesis that species and subspecific variation in skull form results from the differential extension of common patterns of relative growth. A MANOVA provides independent support of Groves's [pp. 44–53 in Proceedings of the Third International Congress on Primatology, Vol. 1 (Basel: S. Karger), 1971] classification of Nycticebus into two species, with four subspecies in the common slow loris and one form of the pygmy slow loris. Within N. coucang, cranial proportions for all four subspecies are ontogenetically scaled, and size differentiation is mainly clinal (Bergmann's Rule). N. c. bengalensis represents the most northerly disposed and the largest form. N. c. javanicus represents the next-largest form and is located in a southerly direction the next-farthest away from the equator. N. c. coucang and N. c. menagensis are both equatorial; however, the latter subspecies is the smallest. A genetic basis for some of the taxonomic variation between N. c. coucang and N. c. menagensis is supported by such nonclinal variation in body size. Variation in the presence/absence of I² is not size-related but rather tracks geographic proximity and isolating factors which predate the most recent inundation of the Sunda Shelf. Although they inhabit a nonequatorial environment, pygmy slow lorises are the smallest of all Nycticebus. As N. pygmaeus is sympatric with N. c. bengalensis, the largest slow loris, it appears that the evolution of its smaller body size represents a case of character displacement. Unlike N. coucang, skull size becomes significantly smaller in more northern N. pygmaeus. This may also reflect character displacement between sympatric sister taxa underlain by a cline-dependent ecological factor which is marked in more northerly latitudes. On the other hand, the negative correlation between body size and latitude in N. pygmaeus could be due to the influence of nonprimate fauna, such as predators, which themselves evince a similar clinal pattern. Analyses of relative growth indicate that skull proportions in the two species of Nycticebus are ontogenetically scaled in two-thirds of the cases. All but one of the seven comparisons (interorbital breadth) which do not indicate ontogenetic scaling represent part of the masticatory complex. This likely reflects a reorganization of N. pygmaeus maxillomandibular proportions linked to smaller size and changes in diet. Am. J. Primatol. 45:225–243, 1998. © 1998 Wiley-Liss, Inc.     

Mitochondrial Control Region and Population Genetic Patterns of Nycticebus bengalensis and N. pygmaeus

Bengal slow lorises (Nycticebus bengalensis) and pygmy slow lorises (Nycticebus pygmaeus) are nocturnal which creates difficulties to study them in the field. There is a scarcity of data on them and their population genetics are poorly understood. We sequenced and analyzed a partial fragment in the first hypervariable region of the mitochondrial control region or D-loop HVRI of 21 Nycticebus bengalensis and 119 N. pygmaeus from the boundary between China and Vietnam where they are sympatric. Though the sample size for Nycticebus pygmaeus is much larger, the polymorphism level is much lower than that of N. bengalensis, possibly because of (1) external gene flow from other habitats of N. bengalensis, (2) gene ingression from Sunda slow lorises (N. coucang coucang) to N. bengalensis, (3) a skewed birth sex ratio in N. pygmaeus, and (4) a possible low survival rate of infant N. pygmaeus. Based on genetic comparisons to Nycticebus bengalensis, we propose that N. pygmaeus in southern China and northern Vietnam might have migrated from middle or southern Vietnam recently. Deng Pan and Jing-Hua Chen made equal contributions to the work.     

Non-invasive detection and monitoring of estrus,pregnancy and the postpartum period in pygmy loris (Nycticebus pygmaeus) using fecal estrogen metabolites

Estrone-conjugates (E₁C) were measured in the feces of six female pygmy lorises (Nycticebus pygmaeus) during estrus (n = 12), pregnancy (n = 4) and the postpartum period (n = 3). Noninvasive feces collection permitted frequent sampling throughout estrus and pregnancy, without disturbance of animals. The estrous period was defined as an increase in fecal E₁C levels above an average of 70 ng/g feces with peaks above 100 ng/g feces obtained in consecutive fecal samples collected over a 6- to 11-day period between the end of July and the first third of October. Comparison of the periovulatory profile of E₁C and the stage of labial opening of the vagina revealed a high agreement (P < 0.001). In all pregnant females, an E₁C rise was found approximately 47 days postestrus, the source of which may be the growing fetal placental unit. Estimated gestation lengths ranged between 187 and 198 days (n = 4). Am. J. Primatol. 41:103–115, 1997. © 1997 Wiley-Liss, Inc.     

Exudativory in the Bengal slow loris (Nycticebus bengalensis) in Trishna Wildlife Sanctuary,Tripura, northeast India

In this study we estimated the extent of exudativory in Nycticebus bengalensis and examined whether exudates can be considered as fallback foods. This study was carried out in Trishna Wildlife Sanctuary, northeastern India, in winter (December–February) and summer (March and April). We estimated time–activity budget using instantaneous sampling and used continuous focal animal sampling to record all instances and durations of feeding, over a total of 177 hr. Feeding accounted for 22.3±2.2% of the activity budget, with no seasonal difference. Bengal slow lorises fed on exudates, nectar, fruit, bark, invertebrates and avian eggs. In addition to scraping they also obtained exudates by gouging holes into the bark of trees. In winter, lorises almost exclusively fed on exudates (94.3% of winter feeding time). In summer, exudates (67.3%) and nectar from one species (22.3%) dominated the diet. This study identifies the Bengal slow loris as the most exudativorous loris. Exudates rather than being a staple fallback food, seem to be a preferred, patchily distributed and common food in the diet of the Bengal slow loris. Exudativory in this species is characterized by high selectivity among species and seasonal variation, which may be related to variations in productivity of exudates and their chemical composition. An understanding of these factors is necessary for predicting the response of this species to human disturbance such as logging. This study also underscores the importance of protecting some of the common species such as Terminalia belerica on which the loris feeds during periods of scarcity. Am. J. Primatol. 72:113–121, 2010. © 2009 Wiley‐Liss, Inc.     

Ecological niche modelling as a technique for assessing threats and setting conservation priorities for Asian slow lorises (Primates: Nycticebus)

Aim Data on geographical ranges are essential when defining the conservation status of a species, and in evaluating levels of human disturbance. Where locality data are deficient, presence‐only ecological niche modelling (ENM) can provide insights into a species’ potential distribution, and can aid in conservation planning. Presence‐only ENM is especially important for rare, cryptic and nocturnal species, where absence is difficult to define. Here we applied ENM to carry out an anthropogenic risk assessment and set conservation priorities for three threatened species of Asian slow loris (Primates: Nycticebus). Location Borneo, Java and Sumatra, Southeast Asia. Methods Distribution models were built using maximum entropy (MaxEnt) ENM. We input 20 environmental variables comprising temperature, precipitation and altitude, along with species locality data. We clipped predicted distributions to forest cover and altitudinal data to generate remnant distributions. These were then applied to protected area (PA) and human land‐use data, using specific criteria to define low‐, medium‐ or high‐risk areas. These data were analysed to pinpoint priority study sites, suitable reintroduction zones and protected area extensions. Results A jackknife validation method indicated highly significant models for all three species with small sample sizes (n = 10 to 23 occurrences). The distribution models represented high habitat suitability within each species’ geographical range. High‐risk areas were most prevalent for the Javan slow loris (Nycticebus javanicus) on Java, with the highest proportion of low‐risk areas for the Bornean slow loris (N. menagensis) on Borneo. Eighteen PA extensions and 23 priority survey sites were identified across the study region. Main conclusions Discriminating areas of high habitat suitability lays the foundations for planning field studies and conservation initiatives. This study highlights potential reintroduction zones that will minimize anthropogenic threats to animals that are released. These data reiterate the conclusion of previous research, showing MaxEnt is a viable technique for modelling species distributions with small sample sizes.     

Reproduction in the slow loris (Nycticebus coucang)

The reproductive biology of the slow loris (Nycticebus coucang) is poorly documented because of infrequent captive breeding success and the absence of field studies of this species. Reproductive data were collected from a breeding colony of slow lorises held at the Duke University Primate Center for the past 10 years. Nineteen infants were born, with a sex ratio of 1:1 and a neonatal mortality rate of 15.8%. In all cases, litter size was one. Females born in the colony copulated for the first time between 18 and 24 months of age. A male that reached sexual maturity in the colony sired his first offspring at the age of 17 months. Estrous cycles ranged in duration from 29–45 days, with copulations usually occurring for 1 day of estrus. Gestation length averaged 192.2 days. Although a postpartum estrus was observed in three cases of infant death, no conceptions resulted. Lactation lasted approximately 6 months. A clear birth peak was observed, with 12 out of 19 births occurring in March, April, and May. The comparatively low basal metabolic rate of this species may account for the unusually low reproductive rate of the slow loris in comparison with other prosimian primates.     

Vertical clingers and gougers: Rapid acquisition of adult limb proportions facilitates feeding behaviours in young Javan slow lorises (Nycticebus javanicus)

Animals of all ages need to access essential food resources, either on their own or with the assistance of conspecifics. Rapid physical and behavioural development is one strategy to help young animals reach adulthood. Specialized gum-feeding mammals exploit a food type that is relatively difficult to access and digest and must possess the appropriate adaptions to access large vertical substrates, i.e. tree trunks. Unlike other gum feeding mammals, the Javan slow loris (Nycticebus javanicus) lacks physical structures, such as keeled nails or claws, which animals commonly use to secure themselves to large vertical substrates. To understand how slow lorises of all ages exploit gum, we examined their vertical gouging posture, locomotor behaviour, habitat use during feeding, and their morphometric measures across three age classes (adult, sub-adult, juvenile). Using data collected in Cipaganti, Java, Indonesia between April 2012 and April 2016, we found that individuals of N. javanicus rely on their hand, foot, and limb morphology to maintain vertical gouging postures, in place of claws or keeled nails. Locomotor behaviour, position in tree, and tree DBH showed no significant difference across age classes while feeding. Juveniles were indistinguishable from adults and sub-adults in regards to limb proportion indices, lower leg length, hand span and foot span. Some morphometric measures scaled isometrically e.g. arm length, but those highlighted during prolonged vertical postures scaled allometrically e.g. leg, hand, and foot measures. These findings suggest that the rapid behavioural and physical development of key features may act as an ontogenetic adaptation to facilitate access to a stable food resource at a young age. The Javan slow loris exemplifies the complex relationship that exists between an animal’s diet and the specializations that facilitate access to these food resources.     

Distribution and Conservation of Nycticebus bengalensis in Northeastern India

We assessed the distribution and conservation status of Bengal slow lorises in Assam and Meghalaya in northeastern India. We surveyed forest reserves, plantations, tea estates, and areas bordering forests in 10 districts of the 2 states and sighted slow lorises in only 4 districts in Assam. Disturbances caused by tree felling, road kills by speeding vehicles, and trapping and hunting are the chief survival threats to the species. We emphasize immediate implementation of conservation measures to ensure the future of the species and recommend additional population surveys to define the distributional extent of Bengal slow lorises.     

Welfare impacts of the illegal wildlife trade in a cohort of confiscated greater slow lorises,Nycticebus coucang

Illegal harvesting and trade are major forces behind population declines of wild slow lorises (genus Nycticebus). The impacts of the wildlife trade on individual slow lorises have not been as well described. In this article, we describe quantitatively the consequences of the wildlife trade for 77 greater slow lorises, N. coucang, who were confiscated en masse and brought to Cikananga Wildlife Center in Indonesia. Medical records indicated that in total, 28.6% of the slow lorises died within the first 6 months, mostly due to traumatic injury, and all the infants died. The greatest sources of morbidity were external wounds (33.1% of 166 total medical events) and dental problems (19.3%). Of the surviving individuals, 25.4% displayed abnormal behavior. Behavioral observations indicated that healthy adults (n = 3) spent 48.2% of their active period performing stereotypies. These data illustrate the physical and behavioral impacts of the illegal wildlife trade on the welfare of slow lorises. We suggest that sharing these individual stories may help generate empathy and educate the public about the impacts of the exotic companion-animal (pet) trade on nonhuman animal welfare.     

昆明动物园笼养倭蜂猴的能量代谢

食物是动物适应性生存的基础,能量平衡对动物生存、繁殖和进化起着至关重要的作用 (McNab,1988).     

Slow loris (Nycticebus borneanus) consumption by a wild Bornean orangutan (Pongo pygmaeus wurmbii)

Primates - Vertebrate predation and consumption by wild Bornean orangutans (Pongo pygmaeus spp.) is rare. In contrast to recorded observations of slow loris consumption by Sumatran orangutans...     

Habitat suitability modeling for the endangered Bengal slow loris (Nycticebus bengalensis) in the Indo-Chinese subregion of India: a case study from southern Assam (India)

Primates - The Bengal slow loris (Nycticebus bengalensis) is an endangered nonhuman primate distributed in Southeast Asia, including India. The species is facing sharp population decline throughout...