Social Learning and Primate Reintroduction

Research on social learning may be of use in the conservation of primates, especially great apes, through (a) promoting their public image, (b) identifying specific adaptations, and (c) devising reintroduction training programs. We surveyed all the instigated social learning studies in primates published since 1950 in order to assess their usefulness to devise reintroduction training programs. We identified 99 publications containing 130 data sets from 27 species of primates. Great apes produced significantly more positive social learning effects than either cercopithecines or cebids. There was also an enhanced social learning effect when skilled demonstrators were used. Our survey indicates that the scientific understanding of many aspects of primate social learning relevant to conservation, including its function, learning spatial route plotting, food and sleeping site location, predator avoidance and detection, and the effect of model and tutee status, would benefit from greater research. Future instigated studies on primate social learning would be most informative for reintroduction if they included ecologically valid tasks presented to 2 similarly composed social groups, one of which functioned as a control, i.e., without being exposed to a model.     

Rethinking Primate Origins Again

In 1974, Cartmill introduced the theory that the earliest primate adaptations were related to their being visually oriented predators active on slender branches. Given more recent data on primate‐like marsupials, nocturnal prosimians, and early fossil primates, and the context in which these primates first appeared, this theory has been modified. We hypothesize that our earliest primate relatives were likely exploiting the products of co‐evolving angiosperms, along with insects attracted to fruits and flowers, in the slender supports of the terminal branch milieu. This has been referred to as the primate/angiosperm co‐evolution theory. Cartmill subsequently posited that: “If the first euprimates had grasping feet and blunt teeth adapted for eating fruit, but retained small divergent orbits…” then the angiosperm coevolution theory would have support. The recent discovery of Carpolestes simpsoni provides this support. In addition, new field data on small primate diets, and a new theory concerning the visual adaptations of primates, have provided further evidence supporting the angiosperm coevolution theory.Am. J. Primatol. 75:95‐106, 2013. © 2012 Wiley Periodicals, Inc.     

Primate taxonomy: Species and conservation

Primatology as a discrete branch of science involving the study of primate behavior and ecology took off in the 1960s after discovery of the importance of primates as models for biomedical research and the realization that primates provide insights into the evolutionary history of humans. Osman Hill's unfortunately incomplete monograph series on the comparative anatomy and taxonomy of the primates¹ and the Napiers' 1967 A Handbook of Living Primates² recorded the world's view of primate diversity at this time. This taxonomy remained the baseline for nearly three decades, with the diversity of each genus being represented by some species, but extensively as subspecies.     

灵长类生态学研究方法

目前,国外对灵长类生态学的研究越来越多,研究内容包括种群动力学、社群结构及行为,野生群繁殖行为等。我国的灵长类生态学研究虽然起步较晚,但发展较快。特别是对我     

Primate archaeology 3.0

The new field of primate archaeology investigates the technological behavior and material record of nonhuman primates, providing valuable comparative data on our understanding of human technological evolution. Yet, paralleling hominin archaeology, the field is largely biased toward the analysis of lithic artifacts. While valuable comparative data have been gained through an examination of extant nonhuman primate tool use and its archaeological record, focusing on this one single aspect provides limited insights. It is therefore necessary to explore to what extent other non-technological activities, such as non-tool aided feeding, traveling, social behaviors or ritual displays, leave traces that could be detected in the archaeological record. Here we propose four new areas of investigation which we believe have been largely overlooked by primate archaeology and that are crucial to uncovering the full archaeological potential of the primate behavioral repertoire, including that of our own: (1) Plant technology; (2) Archaeology beyond technology; (3) Landscape archaeology; and (4) Primate cultural heritage. We discuss each theme in the context of the latest developments and challenges, as well as propose future directions. Developing a more “inclusive” primate archaeology will not only benefit the study of primate evolution in its own right but will aid conservation efforts by increasing our understanding of changes in primate-environment interactions over time.     

Primate sociality in evolutionary context

Much work has been done to further our understanding of the mechanisms that underlie the diversity of primate social organizations, but none has addressed the limits to that diversity or the question of what causes species to either form or not form social networks. The fact that all living primates typically live in social networks makes it highly likely that the last common ancestor of living primates already lived in social networks, and that sociality formed an integral part of the adaptive nature of primate origins. A characterization of primate sociality within the wider mammalian context is therefore essential to further our understanding of the adaptive nature of primate origins. Here we determine correlates of sociality and nonsociality in rodents as a model to infer causes of sociality in primates. We found sociality to be most strongly associated with large-bodied arboreal species that include a significant portion of fruit in their diet. Fruits and other plant products, such as flowers, seeds, and young leaves, are patchily distributed in time and space and are therefore difficult to find. These food resources are, however, predictable and dependable when their location is known. Hence, membership in a social unit can maximize food exploitation if information on feeding sites is shared. Whether sociality evolved in the primate stem lineage or whether it was already present earlier in the evolution of Euarchontoglires remains uncertain, although tentative evidence points to the former scenario. In either case, frugivory is likely to have played an important role in maintaining the presence of a social lifestyle throughout primate evolution.     

Agroecosystems and Primate Conservation in The Tropics: A Review

Agroecosystems cover more than one quarter of the global land area (ca. 50 million km²) as highly simplified (e.g. pasturelands) or more complex systems (e.g. polycultures and agroforestry systems) with the capacity to support higher biodiversity. Increasingly more information has been published about primates in agroecosystems but a general synthesis of the diversity of agroecosystems that primates use or which primate taxa are able to persist in these anthropogenic components of the landscapes is still lacking. Because of the continued extensive transformation of primate habitat into human‐modified landscapes, it is important to explore the extent to which agroecosystems are used by primates. In this article, we reviewed published information on the use of agroecosystems by primates in habitat countries and also discuss the potential costs and benefits to human and nonhuman primates of primate use of agroecosystems. The review showed that 57 primate taxa from four regions: Mesoamerica, South America, Sub‐Saharan Africa (including Madagascar), and South East Asia, used 38 types of agroecosystems as temporary or permanent habitats. Fifty‐one percent of the taxa recorded in agroecosystems were classified as least concern in the IUCN Red List, but the rest were classified as endangered (20%), vulnerable (18%), near threatened (9%), or critically endangered (2%). The large proportion of threatened primates in agroecosystems suggests that agroecosystems may play an important role in landscape approaches to primate conservation. We conclude by discussing the value of agroecosystems for primate conservation at a broad scale and highlight priorities for future research. Am. J. Primatol. 74:696‐711, 2012. © 2012 Wiley Periodicals, Inc.     

Primate pelvic anatomy and implications for birth

The pelvis performs two major functions for terrestrial mammals. It provides somewhat rigid support for muscles engaged in locomotion and, for females, it serves as the birth canal. The result for many species, and especially for encephalized primates, is an ‘obstetric dilemma’ whereby the neonate often has to negotiate a tight squeeze in order to be born. On top of what was probably a baseline of challenging birth, locomotor changes in the evolution of bipedalism in the human lineage resulted in an even more complex birth process. Negotiation of the bipedal pelvis requires a series of rotations, the end of which has the infant emerging from the birth canal facing the opposite direction from the mother. This pattern, strikingly different from what is typically seen in monkeys and apes, places a premium on having assistance at delivery. Recently reported observations of births in monkeys and apes are used to compare the process in human and non-human primates, highlighting similarities and differences. These include presentation (face, occiput anterior or posterior), internal and external rotation, use of the hands by mothers and infants, reliance on assistance, and the developmental state of the neonate.     

Primate genes for glycophorins carrying MN blood group antigens

Glycophorin A, B, and E genes were derived from a common ancestral gene and this gene family appeared during primate evolution, probably between orangutan and gorilla divergences. Based on the study of genomic structures of these human glycophorins and the genetic and immunological study of primate glycophorins, we hypothesize that chimpanzee and gorilla glycophorin B could possess a longer extracellular region and carry a stronger N blood group antigenicity compared with that of the human.     

Primate puzzleboard: A simple environmental enrichment device for captive chimpanzees

An environmental enrichment device was designed and evaluated for captive chimpanzees. The puzzleboard consisted of a 61-cm, square piece of clear plastic with holes of various sizes drilled into the center. The puzzleboard was bolted to the roof of a chimpanzee enclosure. Flavored primate treats were arranged on top of the board, and the chimpanzee used a finger to manipulate the food across the board to be retrieved through the larger holes. The behavior and puzzle use of 29 chimpanzees housed in eight groups were evaluated while the device was empty and while filled with food. For each group, four 1-hr scan samples were recorded for each condition. Data showed that an average of 40 min elapsed from the time the puzzleboard was filled to the last recorded contact by a subject. Mean individual use ranged from 4.8 to 23.8 min/hr. Female chimpanzees used the puzzle significantly more often than did males. Aggressive, affiliative, inactive, and self-directed behaviors were significantly reduced when the puzzle was filled. In addition, the puzzleboard was inexpensive, sturdy, and easily constructed, mounted, and operated.     

非人灵长类的杀婴行为及其适应意义

杀婴现象普遍存在于非人灵长类种类中,本文通过综述目前已知的21 种非人灵长类的69 例杀婴行为记
录,探讨了非人灵长类杀婴行为的适应性意义。大多数雄性杀婴行为符合雄性繁殖策略假说,既满足以下3 个
条件:(1)杀婴雄性与受害婴仔没有父子关系;(2)失去婴猴的母亲会提前进入发情状态;(3)受害雌性随后
可能与杀婴雄性交配。不过有些个别的杀婴现象与雄性繁殖利益无关,文中进一步介绍了误伤假说、减少未来
竞争者假说、肉食假说和病态行为假说。杀婴无疑会对受害母亲造成巨大的损失。雌性防范杀婴的策略包括直
接抵抗、回避接触雄性、积极发情、依靠保护雄性和改变繁殖群组成等多种方式。但是雄性杀婴现象不会完全
消失,因为出现该行为的根本原因是雌性防范雄性杀婴的难度较大,而雄性实施杀婴行为的风险较低、利益较
高。     

Primate communities: Their structure and role in tropical ecosystems

The structure of primate communities living in a number of undisturbed areas is described and compared. Species richness is highest in tropical rain forests of Africa and South America, where up to 14 different species can share the same habitat. The number of sympatric primates in woodlands and savannas is always much lower. Some striking differences in community structure may be observed between communities living in apparently similar habitats. Three major factors may be held responsible for such discrepancies: history and paleoecology, present spatial heterogeneity of the vegetation, and competition with other taxonomic groups. The role of primates in the functioning of forest ecosystems is discussed. Though their trophic impact may be important, the role they play in seed dispersal appears to be more significant; they contribute greatly to homeostasis, as well as to regeneration, of the rain forests. A number of ecological traits are particularly developed among primates and may have contributed to the rapid evolutionary success of the order. Their predominantly vegetarian diet allows them to build up higher population densities than sympatric carnivorous mammals;their arborealism permits them to make use of all edible plant material available in a tridimensional environment; the opportunistic tendencies of some cebids, cercopithecids, and pongids enable them to take advantage of a variety of habitats and situations; and finally, an extended socialization period and a long life-span, allowing them to develop social traditions, give to many of them a further possibility to adapt quickly to novel situations. This paper is a revised version of the third Osman Hill Memorial Lecture delivered at the joint meeting of the Primate Society of Great Britain and the Association for the Study of Animal Behaviour, held in London on 2/3 December 1982.     

Primate origins and the evolution of angiosperms

Traditionally, the morphological traits of primates were assumed to be adaptations to an arboreal way of life. However, Cartmill [1972] pointed out that a number of morphological traits characteristic of primates are not found in many other arboreal mammals. He contends that orbital convergence and grasping extremities indicate that the initial divergence of primates involved visual predation on insects in the lower canopy and undergrowth of the tropical forest. However, recent research on nocturnal primates does not support the visually-oriented predation theory. Although insects were most likely important components of the diets of the earliest euprimates, it is argued here that visual predation was not the major impetus for the evolution of the adaptive traits of primates. Recent paleobotanical research has yielded evidence that a major evolutionary event occurred during the Eocene, involving the angiosperms and their dispersal agents. As a result of long-term diffuse coevolutionary interactions with flowering plants, modern primates, bats, and plant-feeding birds all first arose around the Paleocene-Eocene boundary and became the major seed dispersers of modern tropical flora during the Eocene. Thus, it is suggested here that the multitude of resources available on the terminal branches of the newly evolved angiosperm, rain forest trees led to the morphological adaptations of primates of modern aspect.     

Primate assemblage structure in Amazonian flooded and unflooded forests

There is considerable variation in primate species richness across neotropical forest sites, and the richest assemblages are found in western Amazonia. Forest type is an important determinant of the patterns of platyrrhine primate diversity, abundance, and biomass. Here we present data on the assemblage structure of primates in adjacent unflooded (terra firme) and seasonally inundated (várzea and igapó) forests in the lower Purús region of central-western Brazilian Amazonia. A line-transect census of 2,026 km in terra firme, 2,309 km in várzea, and 277 km in igapó was conducted. Twelve primate species were recorded from 2,059 primate group sightings. Although terra firme was found to be consistently more species-rich than várzea, the aggregate primate density in terra firme forest was considerably lower than that in the species-poor várzea. Consequently, the total biomass estimate was much higher in várzea compared to either terra firme or igapó forest. Brown capuchin monkeys (Cebus apella) were the most abundant species in terra firme, but were outnumbered by squirrel monkeys (Saimiri cf. ustus) in the várzea. The results suggest that floodplain forest is a crucial complement to terra firme in terms of primate conservation in Amazonian forests.     

Primate seed dispersal: Coevolution and conservation implications

Early studies of primates have demonstrated that many species rely heavily on fruit, and that primates constitute a large component of the frugivore biomass in tropical forests. Consequently, primates have long been thought to be important seed dispersers. It is only recently that studies have been conducted that have illustrated the complex nature of the interactions between fruit-eating primates and their food trees. Such studies have raised questions as to the causes and conse-quences of the intriguing differences between primate communities, the importance of other animals in the interactions (such as dung beetles and rodents that secon-darily disperse seeds), how primate-plant interactions evolve, and the significance of primates in forest regeneration and conservation. Since subsistence and com-mercial hunting of primates has heavily impacted frugivore communities, but left the physical structure of the forest relatively unaltered, studies of primate seed dispersal have important implications for the future of forests where seed dispersers have declined or disappeared.     

Lunar Philia in a Nocturnal Primate

The influence of moonlight on behavior has been well documented for many nocturnal mammals, including rodents, lagomorphs, badgers and bats. These studies have consistently shown that nocturnal mammals respond to bright moonlight by reducing their foraging activity, restricting their movement, and reducing their vocalizations. Lunar phobia among nocturnal mammals is generally believed to be a form of predator avoidance: numerous studies indicate that predation increases during moonlit nights. A study I conducted at Tangkoko Nature Reserve in Sulawesi, Indonesia, demonstrates that spectral tarsiers, (Tarsius spectrum), are not lunar phobic, but are lunar philic; they become more active during full moons. During full moons, spectral tarsiers increased foraging, decreased resting, increased travel (distance traveled per unit time, nightly path length, and home range size), increased the frequency of group travel and decreased the frequency of olfactory communication. I explore several potential hypotheses to account for the lack of lunar phobia and potential increased risk of predation resulting from this unusual behavior. Two hypotheses that may account for the behavior are that: 1) foraging efficiency increases during full moons and outweighs the increased risk of predation, and 2) predation risk is not greater during full moons. Instead, predation risk increases during new moons.     

Primate origins: Lessons from a neotropical marsupial

The didelphid Caluromys shows evolutionary convergence towards prosimians in having a relatively large brain, large eyes, small litters, slow development, and agile locomotion. The selection pressures that favored the emergence of primate-like traits in Caluromys from a generalized didelphid ancestor may be analogous to the selection pressures favoring the initial divergence of primates from a primitive nonprimate ancestor, and thus Caluromys provides an independent test of the arboreal hypothesis (Smith: Annual Report of the Board of Regents of the Smithsonian Institution 1912:553–572, 1913), the visual predation hypothesis (Cartmill: The Functional and Evolutionary Biology of Primates, pp. 97–122, 1972), and the angiosperm exploitation hypothesis (Sussman: American Journal of Primatology, in press) of primate origins. Quantitative data on free-ranging C. derbianus in Costa Rica demonstrate that it is highly arboreal, uses visually directed predation to capture arthropod prey, and makes extensive use of terminal branch foraging, where it feeds on small angiosperm products. These observations are consistent with predictions from each model of primate origins, thus suggesting that the hypotheses are not mutually exclusive but are interdependent. The initial divergence of primates probably involved exploitation of the rich angiosperm products and associated insects found in fine terminal branches; visually directed predation may have evolved as an efficient method of insect capture in the terminal branch milieu.     

Primate Diet and Biomass in Relation to Vegetation Composition and Fruiting Phenology in a Rain Forest in Gabon

To test the hypothesis that primate populations are limited by food resources, we studied the feeding ecology of three cercopithecines and one colobine in a rain forest in central Gabon. Simultaneously, we monitored the fruiting phenology of trees and estimated the biomass of the monkey community. The Makandé Forest is dominated by Caesalpiniaceae and characterized by a lack of secondary vegetation and of trees species producing fleshy fruits. Fruit production was irregular intra- and interannually. Fruiting peaks of dry fruits (mainly Caesalpiniaceae) and of fleshy fruits occurred at the same period. However, interseasonal and interannual variability was greater in Caesalpiniaceae than in other families. As a result, the Makandé forest is subject to bottlenecks when food is scarce. On an annual basis, seeds (primarily Caesalpiniaceae) dominated the diet of all monkeys. On a seasonal basis, cercopithecines preferentially consumed fleshy fruits as long as they were available, whereas colobines increased consumption of young leaves when seed availability declined. The consumption of mature leaves was low. The monkey community biomass (ca. 204 kg/km²) is one of the lowest in Central Africa. We suggest that both cercopithecine and colobine populations are limited as a result of the combined effect of the dominance of Caesalpiniaceae, which provide dry fruits according to a mast-fruiting pattern and mature leaves of low quality, and the lack of seral successional stages, which provide fleshy fruit on a more regular pattern and leaves of better quality. During the period of food scarcity, cercopithecines should suffer from the low availability of fleshy fruit, which are their favorite food. At the same period, colobines should be limited by the low availability of edible leaves. Similar low primate biomasses are found in forests dominated by Caesalpiniaceae or Lecythidaceae in South America and in Dipterocarpaceae forests in South Asia, which suggests that their biological characteristics, in particular dry fruits and mast fruiting, are unfavorable to monkey populations. Our results confirm that habitat mosaics may support larger populations of primary consumers than homogeneous primary forests can.     

Tree Climbing Strategies for Primate Ecological Studies

Primate ecological studies can benefit from accessing the canopy to estimate intra-tree and inter-tree variation in food availability and nutrient value, patch and subpatch depletion, foraging efficiency, as well as nest structure and nesting behaviors, parasitic transmission and predator detectability. We compare several ways to access the canopy and examine their suitability for studies of primates. Two of them—the Single Rope Technique and the Climbing Spur Method—allow people to safely access almost all kinds of trees, regardless of their size, height or shape. Modern climbing gear and contemporaneous safety protocols, derived from rock climbers, speleologists, and industrial arborists, are reliable and appropriate for primate ecological studies. Climbing gear is specialized and still expensive for students, but tree climbing can be dangerous during specific maneuvres. Consequently, formal training and preliminary experience are essential before attempting to collect data. We discuss the physics of falling, risk assessment associated with a fall, knots, gear and safety precautions. Finally, we propose a Tree Climbing Safety Protocol adapted for 2 climbing methods and primate field ecology. Researchers should be aware that climbing safety depends on their own judgment, which must be based on competent instruction, experience, and a realistic assessment of climbing ability. Therefore, the information we provide should be used only to supplement competent personal instruction and training in situ. Although most primate observations have been and will mostly be done from the ground in the future, canopy information complements the observations. Canopy data will add a significant new dimension to our knowledge of primates by providing strategic information otherwise unavailable.