Predation on primates: Ecological patterns and evolutionary consequences

It has long been thought that predation has had important ecological and evolutionary effects on primates as prey. Predation has been theorized to have been a major selective force in the evolution of hominids.¹ In modern primates, behaviors such as active defense, concealment, vigilance, flight, and alarm calls have been attributed to the selective pressures of predation, as has group living itself. It is clear that primates, like other animals, have evolved ways to minimize their risk of predation. However, the extent to which they have been able to do so, given other constraints of living such as their own need to acquire food, has not yet been resolved. Perhaps most hotly debated is whether predation has been the primary selective force favoring the evolution of group living in primates. Part of the difficulty in resolving the debate lies in a paucity of direct evidence of predation. This is regrettable yet understandable since primatologists, by definition, focus on the study of primates, not predators of primates (unless these are also primates). Systematic direct evidence of the effects of predation can best be obtained by studying predators that are as habituated to observers as are their primate prey. Until this is done, we must continue to rely on opportunistic accounts of predation and predation attempts, and on systematically obtained indirect evidence. Such data reveal several interesting patterns: (1) although smaller primates may have greater predation rates than larger primates, even the largest primates are not invulnerable to predation; (2) the use by primates of unfamiliar areas can result in higher predation rates, which might be one pressure favoring philopatry, or site fidelity; (3) arboreal primates are at greater risk of predation when they are more exposed (at forest edges and tops of canopies) than in more concealed locations; (4) predation by mammalian carnivores may often be episodic; and (5) terrestrial primates may not experience greater predation than arboreal primates.     

Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics

Hypotheses for the adaptive origin of primates have reconstructed nocturnality as the primitive activity pattern for the entire order based on functional/adaptive interpretations of the relative size and orientation of the orbits, body size and dietary reconstruction. Based on comparative data from extant taxa this reconstruction implies that basal primates were also solitary, faunivorous, and arboreal. Recently, primates have been hypothesized to be primitively diurnal, based in part on the distribution of color-sensitive photoreceptor opsin genes and active trichromatic color vision in several extant strepsirrhines, as well as anthropoid primates (Tan & Li, 1999 Nature402, 36; Li, 2000 Am. J. phys. Anthrop. Supple.30, 318). If diurnality is primitive for all primates then the functional and adaptive significance of aspects of strepsirrhine retinal morphology and other adaptations of the primate visual system such as high acuity stereopsis, have been misinterpreted for decades. This hypothesis also implies that nocturnality evolved numerous times in primates. However, the hypothesis that primates are primitively diurnal has not been analyzed in a phylogenetic context, nor have the activity patterns of several fossil primates been considered.This study investigated the evolution of activity patterns and trichromacy in primates using a new method for reconstructing activity patterns in fragmentary fossils and by reconstructing visual system character evolution at key ancestral nodes of primate higher taxa. Results support previous studies that reconstruct omomyiform primates as nocturnal. The larger body sizes of adapiform primates confound inferences regarding activity pattern evolution in this group. The hypothesis of diurnality and trichromacy as primitive for primates is not supported by the phylogenetic data. On the contrary, nocturnality and dichromatic vision are not only primitive for all primates, but also for extant strepsirrhines. Diurnality, and possibly X-linked polymorphic trichromacy, evolved at least in the stem lineage of Anthropoidea, or the stem lineage of all haplorhines.     

Being human and doing primatology: national, socioeconomic, and ethnic influences on primatological practice

The emerging manifesto, center of the essay collection this commentary is part of, points out that primatology is a primate's science and field of endeavor. It is about primates, and constructed and carried out by primates. But the relationships between different primates involved in primatology cannot be described merely as scientific, zoological, or conservatory. A main point emerging from this perspective is that the relationships amongst primates (as scientists and as subjects) are affected by primatologists' experiences outside of academic science and within the cultural schema that we acquire as members of human societies. My contribution focuses on the primatologists and their sometimes discussed, but too often ignored, cultural and ethnic contexts as influences on how they study, think about, and interact with other primates. In our views and bonds with other primates, do national, class, and ethnic factors count?     

Encounters between domestic dogs and free-ranging non-human primates

Records of responses of free-ranging primates to domestic dogs are summarized and evaluated. Although dogs are often considered as potential predators of primates, members of only 7 species of monkey are reported as actually having been killed by dogs. Most injurious or fatal attacks by dogs on primates occur near human settlements in Asia. It is suggested that neither domestic dogs nor wild canids are important predators of primates. Since dogs are often used by hunters, primates probably have a conditioned aversion to them, which is expressed through alarm responses, fleeing, and sometimes aggression.     

Quadrupedalism in primates

Although many primates can be classified as quadrupeds, quadrupedalism in primates has not in the past received as much detailed attention as some other locomotor modes. In the present study quadrupedalism in primates is analysed in terms of positional behavior (locomotor and postural activities in an environmental context) and a number of categories are defined. For arboreal primates different adaptations are evident in animals of different body sizes. However, all adaptations are related to the exploitation of the small branch setting.     

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.     

非人灵长类动物雌性携抱婴儿与婴儿吸乳偏好的研究进展

灵长类雌性动物在携抱婴儿时会表现出一种方向偏好,同时,婴儿在吸乳时也会表现出方向偏好.相关研究表明,这两类偏好与灵长类大脑不对称性及其功能的进化有着极其紧密的联系.此方面的研究作为灵长类偏好行为研究的重要关注点之一,在国外已得到了较好的发展,在国内尚处于萌芽阶段.由于多种影响因素的存在,非人灵长类已有的研究结果间存在一定差异.     

Disproportional Representation of Primates in the Ecological Literature

We address the question why papers dealing with the ecology of primates are so sparsely represented in the general ecological literature. A literature analyses based on entries in Web of Science and PrimateLit reveals that despite a large number of papers published on primates in general and on the ecology of primates, only a very small fraction of these papers is published in high-ranking international ecological journals. We discuss a number of potential reasons for the disproportion and highlight the problems associated with experimental research on wild primates and constraints on sample size as major issues.     

Nonconvergence in the evolution of primate life history and socio-ecology

The goal of this study was to investigate the extent of convergence in four basic life history and socio-ecological traits among the primates of Africa, Asia, South America and Madagascar. The convergence hypothesis predicts that similar abiotic conditions should result in similar adaptations in independent taxa. Because primates offer a unique opportunity among mammals to examine adaptations of independent groups to tropical environments, we collected information on body mass, activity pattern, diet and group size from all genera for quantitative tests of this hypothesis. We revealed a number of qualitative and quantitative differences among the four primate groups, indicating a lack of convergence in these basic aspects of life history and socio-ecology. Our analyses demonstrated that New World primates are on average significantly smaller than primates in other regions and characterized by a lack of species larger than about 10 kg. Madagascar harbours significantly more nocturnal species than the other regions and is home to all but one of the primates with irregular bursts of activity. Asia is the only region with strictly faunivorous primates, but lacks primarily gummivorous ones. The Neotropics are characterized by the absence of primarily folivorous primates. Solitary species are not represented in the New World, whereas solitary and pair-living species make up the majority of Malagasy primates. Lemurs live in significantly smaller groups than other primates, even after controlling for differences in body size. The lack of convergence among the major primate groups is neither primarily due to phylogenetic constraints as a result of founder effects, nor can it be sufficiently explained as a passive consequence of body size differences. However, because the role of adaptive forces, such as interspecific competition, predation or phenology in shaping the observed differences is largely unexplored, we conclude that it is premature to discard the convergence hypothesis without further tests.     

Are Primates Ecosystem Engineers?

Animals can play important roles in structuring the plant communities in which they live. Some species are particularly influential in that they modify the physical environment by changing, maintaining, and/or creating new habitats; the term ecosystem engineer has been used to describe such species. We here assess the two major foraging strategies of primates, frugivory and folivory, in terms of the potential for primates to function as ecosystem engineers. We argue that whereas the role of primates as seed dispersers has received a great deal of attention, the potential role that folivorous primates play in structuring their environment through herbivory has received much less attention. Further, while quantifying if frugivorous primates are ecosystem engineers through their seed dispersal has proved very difficult, it is not as difficult to ascertain whether folivorous primates are ecosystem engineers. We document situations in which folivorous primates act as ecosystem engineers by 1) eating the leaves and/or bark of trees to the extent that they kill trees, 2) feeding on trees to the degree that they slow their growth relative to nonpreferred tree species, 3) eating the flowers of species to the extent that it does not set fruit, or 4) feeding on plants in such a way as to increase their productivity and abundance. Because evidence from the literature is very limited, where possible we present new evidence of these processes from the colobus monkeys at our long-term field site in Kibale National Park, Uganda. We conclude by discussing promising research programs that could be established to refine our understanding of the role primates play in shaping the structure of plant communities, especially tropical forests.     

Human is a unique species among primates in terms of telomere length.

TRF (terminal restriction fragments) length in various tissues of non-human primates such as Macaca mulatta (rhesus monkey), Macaca fuscata (Japanese monkey), Macaca fascicularis (crab-eating monkey), Pan troglodytes (common chimpanzee), and Pongo pygmaeus (orangutan) was at least 23 kb without exception, which was quite different from that of human somatic tissues (smaller than 10 kb). The distribution pattern of telomerase activity among tissues was similar between human and non-human primates, while the activity level showed some differences such as that strong telomerase activity was observed in gastrointestinal and lymphocytic tissues from non-human primates. The human appears to be a unique species among primates in terms of telomere length.     

The human–primate interface in the New Normal: Challenges and opportunities for primatologists in the COVID-19 era and beyond

The emergence of SARS-CoV-2 in late 2019 and human responses to the resulting COVID-19 pandemic in early 2020 have rapidly changed many aspects of human behavior, including our interactions with wildlife. In this commentary, we identify challenges and opportunities at human–primate interfaces in light of COVID-19, focusing on examples from Asia, and make recommendations for researchers working with wild primates to reduce zoonosis risk and leverage research opportunities. First, we briefly review the evidence for zoonotic origins of SARS-CoV-2 and discuss risks of zoonosis at the human–primate interface. We then identify challenges that the pandemic has caused for primates, including reduced nutrition, increased intraspecific competition, and increased poaching risk, as well as challenges facing primatologists, including lost research opportunities. Subsequently, we highlight opportunities arising from pandemic-related lockdowns and public health messaging, including opportunities to reduce the intensity of problematic human–primate interfaces, opportunities to reduce the risk of zoonosis between humans and primates, opportunities to reduce legal and illegal trade in primates, new opportunities for research on human–primate interfaces, and opportunities for community education. Finally, we recommend specific actions that primatologists should take to reduce contact and aggression between humans and primates, to reduce demand for primates as pets, to reduce risks of zoonosis in the context of field research, and to improve understanding of human–primate interfaces. Reducing the risk of zoonosis and promoting the well-being of humans and primates at our interfaces will require substantial changes from “business as usual.” We encourage primatologists to help lead the way.     

Extending Ethnoprimatology: Human–Alloprimate Relationships in Managed Settings

The majority of studies in ethnoprimatology focus on areas of sympatry where humans and nonhuman primates (hereafter, primates) naturally coexist. We argue that much can be gained by extending the field’s scope to incorporate settings where humans manage most aspects of primates’ lives, such as zoos, laboratories, sanctuaries, and rehabilitation centers (hereafter, managed settings). We suggest that the mixed-methods approach of ethnoprimatology, which facilitates examination of both humans’ and primates’ responses to one another, can reveal not only how humans’ ideas about primates shape management strategies, but also how those management strategies affect primates’ lives. Furthermore, we note that a greater focus on managed settings will strengthen links between ethnoprimatology and primate rights/welfare approaches, and will introduce new questions into discussions of ethics in primatology. For example, managed settings raise questions about when it might be justifiable to restrict primates’ freedom for a “greater good,” and the desirability of making primates’ lives more “natural” even if this would decrease their well-being. Finally, we propose that because ethnoprimatology is premised on challenging false dichotomies between categories of field site—specifically, between “natural” and “unnatural” free-ranging populations—it makes sense for ethnoprimatologists to examine settings in which humans exert considerable control over primates’ lives, given that the distinction between “wild” and “captive” is similarly unclear.     

Self-injurious Behavior in Zoo Primates

Researchers have long known that social isolation of some primates, particularly in infancy, can lead to the development of abnormal behaviors including self-injurious behavior (SIB). However, SIB can also occur in non-isolate-reared primates and can be triggered by frustration or environmental events. The subjects of reports of SIB have mostly been laboratory primates, usually macaques. Researchers had not systematically studied whether SIB occurs in zoo primates, and if so to what extent. Here we report the results of a questionnaire-based survey of British and Irish zoos on the extent of SIB in zoo primates, and whether it was associated with any environmental or developmental events. Responses indicated that though SIB occurred across a range of primate species, its incidence was very low. Respondents identified a variety of environmental events as implicated in initiating SIB, and though the data set is too small to confirm them statistically, several trends were discernible. We conclude that SIB is not a major problem in zoo primates.     

Reconstructing the Diet of an Extinct Hominin Taxon: The Role of Extant Primate Models

Modern humans represent the only surviving species of an otherwise extinct clade of primates, the hominins. As the closest living relatives to extinct hominins, extant primates are an important source of comparative information for the reconstruction of the diets of extinct hominins. Methods such as comparative and functional morphology, finite element analysis, dental wear, dental topographic analysis, and stable isotope biogeochemistry must be validated and tested within extant populations before they can be applied to extinct taxa. Here we review how these methods have and might be used to reconstruct the diet of a particular extinct hominin, Paranthropus boisei, which has no extant analogue for its highly derived masticatory morphology. Our review emphasizes the potential and limitations of using extant primates as models for the reconstruction of extinct hominin diets. We encourage paleoanthropologists and those who study the feeding behaviors of extant primates to work together to investigate and validate methods for interpreting the diets of all extinct primates, including hominins.     

Bushmeat and the Fate of Trees with Seeds Dispersed by Large Primates in a Lowland Rain Forest in Western Amazonia

In Neotropical forests, large fruit-eating primates play important ecological roles as dispersal agents of large seeds. Bushmeat hunting threatens to disrupt populations of primates and large-seeded trees. We test the hypothesis that otherwise intact Neotropical forests with depressed populations of large primates experience decline in recruitment of large-seeded trees. We quantify the proportion of small juveniles (> 0.5 m tall–1 cm diameter at breast height, DBH) of large primate-dispersed tree species found underneath heterospecifc trees that are also dispersed by large primates at two protected sites in Manu National Park and one hunted site outside Manu N.P. in southeastern Peru. The forests are comparable in edaphic and climatic qualities, successional stage, and adult tree species composition. We found that hunting locally exterminates populations of large primates, and reduced primates of intermediate body size (hereafter "medium primates") by 80 percent. Moreover, tree species richness was 55 percent lower and density of species dispersed by large and medium-bodied primates 60 percent lower in hunted than in protected sites. In addition, richness and density of abiotically dispersed species and plants dispersed by non-game animals are greater in hunted sites. Overhunting threatens to disrupt the ecological interactions between primates and the plants that rely on them for seed dispersal and recruitment. Sustainable wildlife management plans are urgently needed, because protected areas are at risk of becoming "island" parks if buffer zones become empty of animals and have impoverished flora.     

The natural place to begin: The ethnoprimatology of the Waorani

Ethnoprimatology is an important and growing discipline, studying the diverse relationships between humans and primates. However there is a danger that too great a focus on primates as important to humans may obscure the importance of other animal groups to local people. The Waorani of Amazonian Ecuador were described by Sponsel [Sponsel (1997) New World Primates: Ecology, evolution and behavior. New York: Aldine de Gruyter. p 143–165] as the “natural place” for ethnoprimatology, because of their close relationship to primates, including primates forming a substantial part of their diet. Therefore they are an ideal group in which to examine contemporary perceptions of primates in comparison to other types of animal. We examine how Waorani living in Yasuní National Park name and categorize primates and other common mammals. Although there is some evidence that the Waorani consider primates a unique group, the non‐primate kinkajou and olingo are also included as part of the group “monkeys,” and no evidence was found that primates were more important than other mammals to Waorani culture. Instead, a small number of key species, in particular the woolly monkey (Lagothrix poeppigii) and white‐lipped peccary (Tayassu pecari), were found to be both important in the diet and highly culturally salient. These results have implications for both ethnoprimatologists and those working with local communities towards broader conservation goals. Firstly, researchers should ensure that they and local communities are referring to the same animals when they use broad terms such as “monkey,” and secondly the results caution ethnoprimatologists against imposing western taxonomic groups on indigenous peoples, rather than allowing them to define themselves which species are important. Am. J. Primatol. 75:1117–1128, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Primate origins: implications of a cretaceous ancestry

It has long been accepted that the adaptive radiation of modern placental mammals, like that of modern birds, did not begin until after the Cretaceous/Tertiary (K/T) boundary 65 million years (Ma) ago, following the extinction of the dinosaurs. The first undoubted fossil relatives of modern primates appear in the record 55 Ma ago. However, in agreement with evidence from molecular phylogenies calibrated with dates from denser parts of the fossil record, a statistical analysis of the primate record allowing for major gaps now indicates a Cretaceous origin of euprimates 80-90 Ma ago. If this interpretation is correct, primates overlapped with dinosaurs by some 20 Ma prior to the K/T boundary, and the initial radiation of primates was probably truncated as part of the major extinction event that occurred at the end of the Cretaceous. Following a review of evidence for an early origin of primates, implications of this are discussed with respect to the likely ancestral condition for primates, including a southern continental area of origin and moderately large body size. The known early Tertiary primates are re-interpreted as northern continental offshoots of a 'second wave' of primate evolution.     

Molecular and evolutionary analyses of formyl peptide receptors suggest the absence of VNO-specific FPRs in primates

Formyl peptide receptors (FPRs) were observed to expand in rodents and were recently suggested as candidate vomeronasal chemo-sensory receptors. Since vomeronasal chemosensory receptors usually underwent positive selection and evolved concordantiy with the vomeronasal organ (VNO) morphology, we surveyed FPRs in primates in which VNO morphology is greatly diverse and thus it would provide us a clearer view of VNO-FPRs evolution. By screening available primate genome sequences, we obtained the FPR repertoires in representative primate species. As a result, we did not find FPR family size expansion in primates. Further analyses showed no evolutionary force variance between primates with or without VNO structure, which indicated that there was no functional divergence among primates FPRs. Our results suggest that primates lack the VNO-specific FPRs and the FPR expansion is not a common phenomenon in mammals outside rodent lineage, regardless of VNO complexity.