Ruliang Pan

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Extinction of Snub-Nosed Monkeys in China During the Past 400 Years

We describe the historical change in distribution of snub-nosed monkeys (Rhinopithecus), a genus which includes 3 of the 4 endemic primate species in China, from the Qing Dynasty (1616) to 2001. The monkeys were once widely distributed in south, southwest and central China, and in two provinces in northwest China (Gansu and Shaanxi). Unfortunately, most of their populations in the plains and in some mountainous regions have vanished. Today, extant groups occur only in isolated mountainous regions with an altitude ≤4,500 m above sea level. The dramatic diminution is closely related to social and natural events, which occurred in China during the last 400 years. 1) the rapidly increasing density of human beings, especially during the twentieth century; 2) wars, especially in the first half of the 20th century; 3) deteriorating environments and accelerated deforestation and 4) hunting monkeys for food, medicinal and economic purposes.

Changes in Distribution of the Snub-Nosed Monkey in China

Snub-nosed monkeys (Rhinopithecus), or golden monkeys, are members of the subfamily Colobinae, family Cercopithecinae. They are very beautiful creatures, but are now distributed in very limited areas. The Sichuan species (Rhinopithecus roxellana), the Yunnan species (R. bieti), and the Guizhou species (R. brelichi) are endemic to China (Figure 1). Together with the Vietnamese species (R. avunculus), they were originally regarded as one genus (Napier and Napier, 1967). More recently they have been split, the Chinese forms being classified as one subgenus (R. [Rhinopithecus]) and the Vietnamese as another subgenus (R. [Prebytiscus]) (Jablonski and Peng, 1993; Jablonski, 1998a). Though limited to isolated regions, they form a graded array of species from R. avunculus in subtropical evergreen and deciduous broad-leaf forests at less than 1,000 m altitude to R. bieti in temperate, coniferous forests as high as 3,000 to 4,500 m where annual average temperatures hover near freezing (Pan and Yong, 1989; Boonratana and Le, 1998).

Cranial morphology of the golden monkey (Rhinopithecus) and Douc Langur (Pygathrix nemaeus)

Because they have been less studied than most other non-human primates (partly due to the difficulties in accessing their habitat) the origins and phylogenetic relationships ofR. roxellana andR. bieti are controversial. These controversies may be clarified to some degree by adding information on the cranium. To this end, ten cranial dimensions analysed morphometrically here provide data about cranial differences among species of the genusRhinopithecus, and between species ofRhinopithecus andPygathrix nemaeus. Though more similar to each other than to any others in the same genus, the results show a significant separation betweenR. roxellana andR. bieti to the degree that they may be regarded as two different species. This confirms the conclusions of prior studies of external features, qualitative morphological characteristics and biochemical evidence (Yeet al, 1987; Zhang and Ryder, 1995; Jablonski, 1998; Penget al., 1988). The differences between these two species are mainly size-related, being highly correlated with cranial length. Other differences, probably non-size related shape differences, however, are highly correlated with cranial width. Sexual dimorphism plays a part in these findings. In relation to the other species, however, the results show that the Vietnam golden monkey (R. avunculus) has closer craniometric relationships with the douc langur (Pygathrix nemaeus) rather than with the three Chinese golden monkey species. Of these, the Gouzhou species (R. brelichi) shares more similarity withR. avunculus and is more separate fromRhinopithecus roxellana and R. bieti. The smaller differentiation between the two latter species could be due to their more recent separation following the dramatic elevation of Qinghai-Tibetan Plateau after the Middle Pleistocene.

Craniodental variation among Macaques ( Macaca ), nonhuman primates

BackgroundIn terms of structure and function, the skull is one of the most complicated organs in the body. It is also one of the most important parts in terms of developmental and evolutionary origins. This complexity makes it difficult to obtain evolutionary assessments if, as is usually the case with fossils, only part of the skull is available. For this reason this study involves a set of comparisons whereby the smallest functional units are studied first, and these built up, through a triple-nested hierarchical design, into more complex anatomical regions and eventually into the skull-as-a-whole. This design has been applied to macaques (Macaca) in order to reveal patterns of variation at the different levels. The profiles of such variation have been obtained both within and between species. This has lead to a search for the skull parts that have undergone similar selection pressures during evolution and comparable development patterns in both ontogeny and phylogeny.ResultsMorphometric analysis (Principal Components) was used to obtain these profiles of species and sex separations based on 77 cranial variables from 11 species of macaques. The results showed that 7 functional units could be aggregated into three functionally reasonable anatomical regions on the basis of similarities in profiles. These were: the masticatory apparatus containing mandible, lower teeth and upper teeth, the face as a whole combining maxilla (actually lower face) and upper face, and the cranium as a whole involving cranium and calvaria. Twenty-six variables were finally selected for analyzing the morphology of the whole skull. This last showed an overall profile similar to that revealed in the masticatory apparatus but also contained additional information pertaining to individual species and species-groups separations.ConclusionsThe study provides a model for carrying out analysis of species separations and sex variation simultaneously. Through this design it seems possible to see cranio-dental elements that may result from similar developmental processes, have similar functional adaptations, and show an appropriately integrated structure morphologically. This study also implies that the biological information drawn from part of skull alone, e.g. as in studies of incomplete fossils may provide misleading information.

Morphometric analysis of Macaca arctoides and M-thibetana in relation to other macaque species

As a first step in reviewing the classification of the two stump-tailed macaque species,Macaca arctoides andM. thibetana, as compared with other species of the genusMacaca, 72 linear dental and cranial variables of 11 macaque species were examined by morphometric analyses. The results indicate that the two stump-tailed species are the largest of the macaques and although rather similar overall, they exhibit significant differences in the pattern of variation in most of the five skull regions as shown by Principal Components and Canonical Variate Analyses. Euclidean Distances based on Canonical Variate scores indicate that the females ofM. arctoides andM. thibetana are more widely separated than eight other pairs of macaque species, and that the separations of the respective males are greater than those of three other pairs of species. These findings are consistent withFoodens classification of the stump-tailed macaques as two separate species (Fooden, 1976;Fooden et al., 1985). The present results suggest, as other researchers have proposed on the basis of external features, biochemistry and genetics, that the two stump-tailed macaque species andM. assamensis are closely related. The results also tentatively imply associations withM. fuscata andM. sylvanus but these require further study. The findings have implications for the assessment of the various Chinese Pleistocene macaque fossils.

Craniodental Variation in the African Macaque, with Reference to Various Asian Species

Based on twenty-seven craniodental measurements and ratios derived from them, the relationship between the African macaque (M. sylvanus) and the others in Asia were examined with principal components analyses (PCA) and Euclidean distance analysis based upon prior discriminant function analyses (DFA). Results based on analyses of raw measurements indicate that the variation between species lies in the first axis of PCA; the species are dispersed according to their differences in size. The variation between sexes (sexual dimorphism) lies in the second axis. In the analyses of ratio variables, though these two patterns of separation remain orthogonal, they lie at approximately forty-five degrees to each axis. Variables relating to anterior teeth were found to play an important role in variation analysis, and this may be related to the special food preferences of these monkeys: more frequent usage of the incisor teeth for processing frugivorous diets than in other primates that are mainly folivorous. The results from Euclidean distance analyses indicate that the average distance of species within the Asian group is shorter than that between Asian and African groups regardless of sex and variable type. In addition the variation between African and Asian groups is larger than that within Asian group. Thus, it is reasonable to suggest that the African macaque has a range of measurements and ratios quite distinct from the species found in Asia (though the greatest separations result from the analyses of ratio data). These results therefore support the view that M. sylvanus may be regarded as an independent species group in the genus Macaca as proposed by Delson [1980].

Metrical Dental Analysis on Golden Monkey (Rhinopithecus roxellana)

Dental variation in the Chinese golden monkey (Rhinopithecus roxellana) is here evaluated by univariate, bivariate, and multivariate analyses. Allometric analyses indicate that canines and P3s are positively, but other dimensions negatively scaled to mandible and maxilla, and to body size. With the exception of the mesiodistal dimensions of I1 and M3, and the buccolingual dimension of P4, mandibular dental variables show similar scaling relative to body size. Analysis of residuals shows that males have significantly larger canine, P3 and buccolingual dimensions of the postcanine teeth (M2 and M3) than females. A significant difference in shape between the sexes is found in the buccolingual dimension of the upper teeth, but not in the mandible. Unlike the situation in some other species, female golden monkeys do not exhibit relatively larger postcanine teeth than males. In fact, the reverse is true, expecially for M2s and M3s. The fact that most of the dental variables show low negative allometry to body size might be related a cold environment that has led to the development of larger body size with reduced energy loss. When the raw data are examined by Discriminant Function Analysis the sexes are clearly distinguishable.

Mandibular morphometric variation among Chinese cercopithecoids and the unique structure of the snub-nosed monkey (Rhinopithecus) mandible

In order to understand how mandibular structure differs among the Chinese cercopithecoids (Rhinopithecus, Trachypithecus and Macaca), particularly the uniqueness of the snub-nosed monkeys (Rhinopithecus), we analysed ten mandibular measurements by principal components analysis (PCA), and examined scaling patterns. The results provided by the PCA illustrated differences due to size among the cercopithecoids and the relationship between colobines (Trachypithecus and Rhinopithecus) and cercopithecines, in which macaques (Macaca) are included. Allometric analysis indicated that, biomechanically, there is not a marked difference between macaques and leaf-eating monkeys. This may be associated with the fact that both share some similar ecology and niches in south and southwest China. The snub-nosed monkeys exhibit a significantly more robust mandible, evident in the symphysis, corpus, condyle, and masticatory momentum arm. This supports the hypothesis, based on the study of dental structure, that Rhinopithecus is a unique group in Asian Old World monkeys (OWMs) and has developed some unique characteristics in order to adapt to the tough food available in the severe cold climate of the Plateaux of Qinghai–Tibet, Yun-Gui and Qingling in China.

Male Dispersal Pattern in Golden Snub-nosed Monkey ( Rhinopithecus roxellana ) in Qinling Mountains and its Conservation Implication

Golden snub-nosed monkey (Rhinopithecus roxellana) is one of the most endangered primate species found in China, exhibiting multilevel society consisting of several one-male-females together with their offspring units (OMU), and all-male units (AMU). Female dispersal patterns of the species within herd have been well documented, whereas those of the males within or between herds are still poorly understood. Our results based a long-term observation indicate that more than half of sub-adult males, and half of the deposed males that stayed a short period in OMU disperse between herds, three of them established their own OMU in new herd after the dispersal. Smaller number of the sub-adult and adult males, compared with adult females, stayed in natal herd, implying sub-adult males started dispersing and male-biased dispersal occurred between herds. High frequencies of resident males were wounded as their OUMs were taken over, and resident males co-operation defend bachelor males were found. Mating competition among males within the herd may have contributed to the scenarios of male-biased dispersal. The results also suggest that maintaining connection between isolated herds and establishing the corridors among the fragmented habitats for the species will greatly benefit increasing its gene flow and promoting conservation status.