Molecular Phylogeny of Nycticebus Inferred from Mitochondrial Genes

Researchers are still discussing the classification of Nycticebus. We established a molecular phylogeny covering all recognized taxa in Nycticebus to provide information for further evaluation. We sequenced partial D-loop (ca. 390 bp) and cytochrome b genes (425 bp) from 22 specimens. We separated most of the major groups except for some mixing of Nycticebus. coucang coucang and N. bengalensis. Nycticebus pygmaeus diverged earlier from the ancestral stock than the other taxa. Nycticebus coucang menagensis was well discriminated from N. c. coucang. It may be possible to explain the mixing of Nycticebus coucang coucang and N. bengalensis by the hybridization between the 2 groups in the field. Although our data did not provide direct evidence for or against the new proposal that Nycticebus coucang javanicus be raised to the rank of a distinct species (N. javanicus), we have good evidence for regarding N. c. menagensis as a species.Jing-Hua Chen and Deng Pan made equal contributions to the work.     

Studies on the chromosomes of genusNycticebus

The karyotypes of three species (N. coucang, N. intermedius, andN. pygmaeus) of genusNycticebus, collected from the southern Yunnan of China, have been studied. All individuals from three species possess 2n=50 chromosomes, and all chromosomes in their complement are biarm chromosomes. The karyotype of slow loris (N. coucang) is characterized by having a secondary constriction and Ag-NORs in the short arms of pair No. 1. The G-banding patterns of three species are very similar. Three species are found to have multiple Ag-NORs. InN. coucang, NORs were observed on five pairs (Nos. 1, 6, 9, 15, and 23) and inN. intermedius andN. pygmaeus, NORs were found on four pairs (Nos. 6, 9, 15, and 20). This finding indicates that slow lorises, as primitive primates, also have multiple NOR-bearing chromosomes. Finally, the classification of genusNycticebus by karyotype analysis is discussed, and our results suggest that there are at least two valid species, namely:N. coucang andN. pygmaeus.     

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.     

Phylogeny of the slow lorises (genusNycticebus): An approach using mitochondrial DNA restriction enzyme analysis

Mitochondrial DNA polymorphisms in 15 specimens of three species of slow lorises-Nycticebus coucang, N. intermedius, andN. pygmaeus-were analyzed in order to study the evolutionary relationships among the species. Eight restriction types were observed in the samples. Phylogenetic trees constructed on the basis of genetic distances showed that the slow lorises sort into two clusters: four types ofN. coucang and three types ofN. intermedius plus one type ofN. pygmaeus. Our results suggest that there are two valid species in the genusNycticebus-N. coucang, andN. pygmaeus-and thatN. intermedius should be included withinN. pygmaeus. Divergence between the two species may have begun 2.7 Ma (million years ago). Evolution of gross morphology, chromosomes, and mitochondrial DNA in the slow lorises appears to be concordant.     

A Survey of Husbandry Practices for Lorisid Primates in North American Zoos and Related Facilities

Zoos and related facilities in North America currently manage five species in the primate family Lorisidae: the greater (Nycticebus coucang), Bengal (N. bengalensis) and pygmy (N. pygmaeus) slow lorises, red slender loris (Loris tardigradus), and potto (Perodicticus potto). We used an online survey to describe institutional housing and husbandry practices for these species and assess the extent to which practices are consistent with established guidelines. Our results show that most captive lorisids are housed solitarily or in pairs. Most individuals occupy a single exhibit space in a building dedicated to nocturnal animals. Facilities are commonly meeting recommendations for abiotic exhibit design and are providing animals with an enriched environment. However, pottos and slender lorises currently occupy exhibit spaces smaller than the recommended minimum, and the impact of cleaning protocols on olfactory communication should be critically evaluated. Few facilities are taking advantage of the benefits of positive reinforcement training for promoting animal welfare. Research is greatly needed on the effects of exhibit lighting on behavior, health, and reproduction; and to determine how best to manage the social needs of lorisids with naturally dispersed social structures. Although captive populations of slender lorises, pottos, and slow lorises are declining, we suggest that improved husbandry knowledge has the potential to positively influence population sustainability and to enhance future efforts to manage the growing pygmy loris population. Zoo Biol. 32:88‐100, 2013. © 2012 Wiley Periodicals, Inc.     

Conservation implications of low encounter rates of five nocturnal primate species (<Emphasis Type="Italic">Nycticebus </Emphasis>spp.) in Asia

Five species of slow lorises were once considered to comprise a single strongly polymorphic species, Nycticebus coucang, ranging throughout South and Southeast Asia. The cryptic nature of these nocturnal primates has led to a lack of understanding of their distribution patterns and abundance. In short surveys, often few if any lorises are detected, meaning that the few available density estimates are from long-term studies. Based on new research in Sebangau National Park, Borneo, and compilation of survey data from other areas, we provide the first comparative abundance estimates for all five slow loris species: N. coucang occurred in significantly higher abundances (median encounter rate 0.80/km: n = 15), than N. bengalensis (0.26/km; n = 12), or N. javanicus (0.11/km: n = 2), N. menagensis (0.02/km: n = 3), and N. pygmaeus (0.13/km: n = 4). Abundance estimates in Sebangau (0.19/km) did not increase with increasing survey effort, but for all species and studies combined, study duration was positively correlated with abundance estimates. We did not find a relation between abundance and body mass, nor between abundance and latitude. Long-term studies are more likely to be conducted at sites where the species of interest is particularly plentiful. The data suggest that slow lorises occur at low abundances throughout much of their range, and some in larger social groups than previously assumed. We recommend taking into account the species’ heterogeneous distribution (potentially requiring larger survey effort), their social structure, the use of red lights as opposed to white lights whilst surveying, and to make use of their vocalisations when surveying slow lorises.     

The antecubital organ of the primate slow loris (Nycticebus coucang coucang)

A study of the ‘antecubital organ’ of the slow loris (Nycticebus coucang coucang), was undertaken in light and electron microscopes. As distinct from other prosimian primates there is a complete absence of interstitial cells in the gland suggesting its different functional role. The acinar cells in the ‘antecubital organ’ of slow loris contain large number of smooth ER and electron-dense secretory granules. The granules are seen both in the apical region of the cells as well as in their basal cytoplasmic processes. Some of these processes appear to terminate close to a blood capillary. The structural features of the ‘antecubital organ’ of slow loris suggest that it is a mixed gland of both exocrine and endocrine nature.     

Eastern limit of distribution of the slow loris,Nycticebus coucang

The easternmost known record of the slow loris,Nycticebus coucang, is Tawitawi, Philippines. A report of this species in Mindanao, 500 km northeast of Tawitawi, is based on a mislabeled specimen.     

Protein polymorphism and genetic divergence in slow loris (genusNycticebus)

In this study, protein electrophoresis was assayed to detect genetic variation in GenusNycticebus. A total of 29 samples (2N. coucang and 27N. pygmaeus) were analyzed for 42 genetic loci. In the 27 samples ofN. pygmaeus, 4 loci were observed to be polymerphic. Therefore, the estimatedP value (proportion of polymorphic loci) is 0.095, theA value (average number of alleles each locus) is 1.045, and theH value (mean individual heterozygosity) is 0.040. After comparing theH ofN. pygmaeus with those of other primates reported, we found that the protein variation inN. pygmaeus is slightly lower than the average level. Additionally, we also observed obivious allele difference betweenN. pygmaeus andN. coucang. There are no shared alleles between these two species in eight loci. TheNei's genetic distance between them was calculated as 0.2541, which falls in the spectrum of genetic difference between species in primates.     

Excretion of radiolabeled estradiol metabolites in the slow loris (Nycticebus coucang)

The excretion pattern of estradiol was studied in the slow loris Nycticebus coucang) and the ring-tailed lemur (Lemur catta) in order to compare steroid excretion in two representative prosimian species. Daily urinary estrone conjugate measurements in the female loris provided little information when applied over prolonged periods. As a result of these negative data, a metabolic study was performed to determine if estrogen excretion patterns in the slow loris differed from those in the lemur, where urinary assays proved a useful tool in characterizing reproductive cycles. Radio-labeled estradiol was injected intravenously, and serial urine and fecal collections were analyzed for radiolabeled metabolites. The results of these studies demonstrate that more than 92% of the radiolabel was excreted in the feces of the loris, in contrast to only 16% excreted in the feces of the lemur.     

Mother-infant interactions in slow lorises (Nycticebus bengalensis) and pygmy lorises (Nycticebus pygmaeus)

The study had three purposes: (1) to obtain information about mother-infant interactions in a rarely studied nocturnal prosimian, the pygmy loris (Nycticebus pygmaeus); (2) to compare pygmy lorises with a closely related and better-studied nocturnal prosimian, the Bengal slow loris (Nycticebus bengalensis); and (3) to determine how the presence of a second offspring affected mother-infant interactions in pygmy lorises. Three Bengal slow loris mothers and 3 pygmy loris mothers served as subjects, along with their 10 offspring (4 Bengal slow loris singletons, 2 pygmy loris singletons and 2 sets of pygmy loris twins). Observations were carried out in a zoo research facility for the first 24 weeks of the infants' lives. Although the two species differ in size and reproductive patterns, mother-infant interactions were similar. The primary modes of infant and adult contact were ventral and passive contact, respectively. Mothers parked their infants from the first week, and infants followed from the second week. Mothers displayed little protection or rejection, and there was little aggression. Infants solicited play and social grooming from their mothers. Pygmy loris mothers engaged in social grooming and play with their infants more frequently and for longer periods if the infant was a singleton rather than a twin.     

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.     

Proportions and variability in the Indian lorises: Bone weight observations onLoris tardigradus lydekkerianus andNycticebus coucang

Thirty uniformly prepared, disarticulated complete skeletons of adultLoris tardigradus lydekkerianus andNycticebus coucang have been weighed for preliminary study of the weight relations between different major skeletal parts. In these forms, combined relative weight of the precaudal vertebrae, ribs and sternum surpasses the averages for the rest of the skeletal parts. The weight of the skull equals one-fifth of the total skeletal weight inLoris andNycticebus. The weight of the skeletons of the limbs (including the shoulder girdle and the hip bones) contributes less than half of the total skeletal weight in lorises. The bones of the upper limbs are lighter than those of the lower limbs in the 2 series examined.Loris andNycticebus are distinguished by having the proportionately heaviest axial skeleton and skull and the lowest relative weights of the bones of the 4 limbs. The combined relative skeletal weight of the upper and lower limbs ranges between 45.34 and 50.01 inLoris andNycticebus. The relative weight of the skeletons of the hands and feet are almost similar to the corresponding weights in the 2 series.As far as the weights of the different skeletal parts are concerned, there is no relative asymmetry in the 2 series ofLoris andNycticebus examined.     

The subependyma of the primate, slow loris (Nycticebus coucang coucang)

The subependymal plate of the primate slow loris (Nycticebus coucang coucang) has been studied by electron microscopy. It is composed of a mixed population of several cell types in which the subependymal cells preponderate. Free subependymal cells are found in the ‘border area’ near the corpus callosum or the neuropile of the caudate nucleus. In common with the subependymal cells they show a scanty cytoplasm containing mostly free ribosomes. Typical neuroglial cells namely, microglia, astrocytes and oligodendrocytes are also identified in this region. Among the various cell types mentioned there are present also a few occasional cells which have features bearing a resemblance to the subependymal cell on the one hand and to the microglia on the other. The morphological evidence suggests that in parallel with the macroglia the microglia could be derived by stepwise transformation of the subependymal cells.     

Interactions between a wild Bornean orang-utan and a Philippine slow loris in a peat-swamp forest

All documented orang-utan–loris interactions have been from Sumatra, where lorises were opportunistically preyed upon by orang-utans. In this paper, we describe two accounts of the Bornean orang-utan (Pongo pygmaeus wurmbii) interacting with the Philippine slow loris (Nycticebus menagensis). The interactions were by two adolescent female orang-utans. No attempts to catch the loris were observed on either occasion. Neither interaction was hostile. During the second observation, which was more detailed, we considered the behaviour to be play rather than aggression or attempted predation. Based upon the lack of interest from the adult females during these rare encounters, we propose that the behaviour represents play or non-aggressive exploration rather than predation.     

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.     

Hiding in the dark: Local ecological knowledge about slow loris in Sarawak sheds light on relationships between human populations and wild animals

Local ecological knowledge (LEK) increases understanding of certain species and the threats they face, especially little-studied taxa for which data on distribution and conservation are often lacking. We conducted 111 semi-structured interviews in Sarawak, Malaysia, to collect local knowledge about the behavior and distribution of the Philippine slow loris (Nycticebus menagensis) from two ethnic groups, the Iban and the Penan. Our study revealed that male Penan respondents, generally hunters, who frequently go into the forest were better at identifying animals from pictures. Overall, the Penan have a more detailed knowledge of slow loris behaviors, habitat, and distribution than the Iban. The two ethnic groups have different attitudes towards slow loris as the Penan hunt, eat, or keep them as pets while the Iban consider them sacred and signifiers of good luck. We advocate the use of LEK for providing complementary information to scientific methods in the study of cryptic animals.     

懒猴肩关节的多变量分析

在懒猴与其它灵长类肩关节局部解剖的基础上,对肩关节有关指数的多变量分析结果表明,与骨骼相比,肩关节肌的种间差别明显较大。肩胛盂宽指数、肩胛骨指数和锁肱指数对种的区分有重要意义。懒猴具有类似于叶猴三角肌、大圆肌和喙肱中肌较远的止点及发达的背阔肌和斜方肌颅侧部,增强了肩关节的运动,表现出适应树栖四足运动的特征。而懒猴粗壮的肱骨、较长的锁骨和较长的肱骨,是攀爬型和四足倒挂运动的适应结果。