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.     

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.     

Substrate alters forelimb to hindlimb peak force ratios in primates

It is often claimed that the walking gaits of primates are unusual because, unlike most other mammals, primates appear to have higher vertical peak ground reaction forces on their hindlimbs than on their forelimbs. Many researchers have argued that this pattern of ground reaction force distribution is part of a general adaptation to arboreal locomotion. This argument is frequently used to support models of primate locomotor evolution. Unfortunately, little is known about the force distribution patterns of primates walking on arboreal supports, nor do we completely understand the mechanisms that regulate weight distribution in primates. We collected vertical peak force data for seven species of primates walking quadrupedally on instrumented terrestrial and arboreal supports. Our results show that, when walking on arboreal vs. terrestrial substrates, primates generally have lower vertical peak forces on both limbs but the difference is most extreme for the forelimb. We found that force reduction occurs primarily by decreasing forelimb and, to a lesser extent, hindlimb stiffness. As a result, on arboreal supports, primates experience significantly greater functional differentiation of the forelimb and hindlimb than on the ground. These data support long-standing theories that arboreal locomotion was a critical factor in the differentiation of the forelimbs and hindlimbs in primates. This change in functional role of the forelimb may have played a critical role in the origin of primates and facilitated the evolution of more specialized locomotor behaviors.     

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.     

Primate frugivory in Kibale National Park, Uganda, and its implications for human use of forest resources

In an attempt to understand the practical and/or economic implications of primate seed dispersal, it was established which seed species are dispersed by frugivorous primates in Kibale National Park, Uganda, and which of this sort of species were used by Ugandan people. A list of fruit species consumed by Kibale primates was compiled using primary data and by reviewing all known published accounts of their fruit diet. Primates consume the fruit of 87 Kibale forest tree species; the seeds of 11% of these species are destroyed by the primates. The remaining 77 species are dispersed by either one, two, three or all four of the frugivorous Kibale primates. Of these 77 species, 42% have some utility to local Ugandan inhabitants, suggesting that maintaining populations of primates is important not only for natural forest regeneration, but also for human habitat use. This report illustrates the complexity of the seed dispersal process and suggests links not only between plants and their dispersers, but also between sets of plants/dispersers and the human populations that rely on forest resources.     

A primate bioassay for the determination of renin inhibitory peptides in serum

The study of renin inhibitory peptides (RIPs) in rodents and primates requires the establishment of a simple, high volume method for determining the concentration of RIPs in serum after intravenous or oral dosing. The human renin inhibition assay useful for rodents is not directly applicable to primates due to inherent production of angiotensin I from the primate serum angiotensinogen and added recombinant human renin. Therefore, a novel approach to analyze the serum concentrations of RIPs in primates is described based on in vitro studies with monkey serum. The procedure involves the inactivation of monkey angiotensinogen and monkey renin by thermal denaturation prior to analysis. Application of this assay was demonstrated by analyzing serum samples from an in vivo study in monkeys using ditekiren (U-71,038), a renin inhibitory peptide, and by validation of the assay and results using a tritium-based radioimmunoassay (RIA) for ditekiren. The minimum detectable limit of ditekiren for both the RIA and the bioassay for primates was 10ng/ml serum. The reported bioassay should be of value for monitoring serum levels of thermostable RIPs from pharmacokinetic, bioavailability, and pharmacodynamic studies in primates as well as in humans.     

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.     

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.     

Micro-anatomy of the volar skin and interordinal relationships of primates

Paleontological and molecular evidence have been employed to suggest that flying lemurs (Dermoptera) and primates form a monophyletic group, in sharp contrast with cranial and postcranial evidence indicating sister group relationships between flying lemurs and bats (Chiroptera). New evidence from the epidermis of the volar pads of primates, tree shrews, flying lemurs, bats, and other mammals was examined and mapped on to various hypotheses of archontan relationships. The micro-anatomy of the skin on the palm and sole of flying lemurs and bats differs fundamentally from that of tree shrews (Scandentia) and primates. The volar skin of flying lemurs and bats lacks the serial arrangement of papillary ridges and grooves ("fingerprints") found in primates, tree shrews, and many other mammals. Moreover, the junction between the epidermis and dermis in flying lemurs and bats is relatively flat and shows little or no development of the internal ridges that occur in primates and tree shrews. When mapped on to a set of cladograms of mammals currently allocated to the superorder Archonta, this new evidence does not support sister group relationships between flying lemurs and primates, regardless of the volar skin morphology that characterized the last common ancestor of Archonta. Micro-anatomical differences that distinguish the volar skin of flying lemurs and bats from that of primates and tree shrews reflect a profound dichotomy in the functional roles fulfilled by the extremities, which could be significant in a phylogenetic context.     

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?     

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.     

Brief communication: Forelimb compliance in arboreal and terrestrial opossums

Primates display high forelimb compliance (increased elbow joint yield) compared to most other mammals. Forelimb compliance, which is especially marked among arboreal primates, moderates vertical oscillations of the body and peak vertical forces and may represent a basal adaptation of primates for locomotion on thin, flexible branches. However, Larney and Larson (Am J Phys Anthropol 125 [2004] 42–50) reported that marsupials have forelimb compliance comparable to or greater than that of most primates, but did not distinguish between arboreal and terrestrial marsupials. If forelimb compliance is functionally linked to locomotion on thin branches, then elbow yield should be highest in marsupials relying on arboreal substrates more often. To test this hypothesis, we compared forelimb compliance between two didelphid marsupials, Caluromys philander (an arboreal opossum relying heavily on thin branches) and Monodelphis domestica (an opossum that spends most of its time on the ground). Animals were videorecorded while walking on a runway or a horizontal 7‐mm pole. Caluromys showed higher elbow yield (greater changes in degrees of elbow flexion) on both substrates, similar to that reported for arboreal primates. Monodelphis was characterized by lower elbow yield that was intermediate between the values reported by Larney and Larson (Am J Phys Anthropol 125 [2004] 42–50) for more terrestrial primates and rodents. This finding adds evidence to a model suggesting a functional link between arboreality—particularly locomotion on thin, flexible branches—and forelimb compliance. These data add another convergent trait between arboreal primates, Caluromys, and other arboreal marsupials and support the argument that all primates evolved from a common ancestor that was a fine‐branch arborealist. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Primates follow the 'island rule': implications for interpreting Homo floresiensis

When the diminutive skeleton of Homo floresiensis was found on the Indonesian island of Flores, it was interpreted as an island dwarf, conforming to the 'island rule' that large animals evolve smaller size on islands, but small animals tend to get larger. However, previous studies of the island rule have not included primates, so the extent to which insular primate populations undergo size change was unknown. We use a comparative database of 39 independently derived island endemic primate species and subspecies to demonstrate that primates do conform to the island rule: small-bodied primates tend to get larger on islands, and large-bodied primates get smaller. Furthermore, larger species undergo a proportionally greater reduction in size on islands.     

Predictors of orbital convergence in primates: a test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.     

The Hand That Feeds the Monkey: Mutual Influence of Humans and Rhesus Macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) in the Context of Provisioning

Historically, humans and other primates (primates henceforth) have coexisted across cultures and contexts, and many primate populations use anthropogenic food sources as their main or supplementary food. While primates may actively forage for such food, they are also directly provisioned by humans in many regions. Ethnoprimatology views humans and primates as cohabitants of integrated socioecological spaces who mutually influence each other’s ecologies and social lives. We contextualized provisioning of primates by humans within an ethnoprimatological framework and examined if the availability of anthropogenic food affected primate diets or the amount of time primates spent in anthropogenic habitats and whether primates influenced the human act of provisioning. To this end, we used scan sampling on a group of rhesus macaques across a year, and conducted interviews with 86 people who paused at a nearby tea shop for refreshments. We found that the macaques’ consumption of natural resources and dietary diversity decreased, and they spent more time in human-modified habitats when provisioned food was available. We also found that particular behaviors of the provisioned macaques stimulated provisioning by humans. Our findings show that provisioning influences macaque feeding ecology and habitat use, and that the behavior of the macaques themselves drives people to provide them with food subsidies, illustrating a complex web of interactions between the sympatric species.     

Fragile sons or harassed daughters? Sex differences in mortality among juvenile primates

In most mammals, juvenile males tend to be more vulnerable to starvation than females and consequently experience a higher mortality. This has been attributed to selection on high male growth rates in response to strong intrasexual competition. Among primates, by contrast, it has been noted that females tend to be less viable as juveniles. This has been attributed to a greater ability of juvenile males to contest for food. An alternative explanation is that there is local resource competition, and adults of the resident sex (usually females) attempt to limit the recruitment of unrelated immatures of the same sex by harassing them. These ideas are not mutually exclusive. A set of predictions from these three hypotheses was derived for two social systems and two levels of food supply. They were tested using estimates of juvenile mortality and juvenile sex ratios of non-human primates based on over 40 data sets drawn from the literature. The results indicate that the local resource competition hypothesis provides the best explanation for the observed patterns in differential juvenile mortality in primates. The contrast between the findings for primates and those for other taxa is attributed to the low growth rate of immatures and the widespread occurrence of conditions conducive to local resource competition in primates.     

Prevalence of Epstein-Barr virus (EBV) antibodies in primate stocks of zoological gardens

Abstract: Examination of 387 serum samples from 41 primate species with two different ELISAs for the presence of IgG-antibodies against Epstein-Barr virus. Antibodies were detected in 15 out of 32 species of Old World primates and none in six species of New World primates by screening ELISA (Enzygnost, Behringwerke AG, Marburg), a testkit for human diagnostics. To avoid species-dependent factors which could influence the sensitivity of the Enzygnost assay, a competition ELISA was established. The modified test assessed antibodies in all species of Old World primates and three species of the New World primates.     

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.     

Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype

Blastocystis isolates from 56 Danish synanthropic and zoo animals, 62 primates primarily from United Kingdom (UK) collections and 16 UK primate handlers were subtyped by PCR, sequencing and phylogenetic analysis. A new subtype (ST) from primates and artiodactyls was identified and designated as Blastocystis sp. ST10. STs isolated from non-human primates (n = 70) included ST3 (33%), ST8 (21%), ST2 (16%), ST5 (13%), ST1 (10%), ST4 (4%) and ST10 (3%). A high prevalence of ST8 was seen among primate handlers (25%). This ST is normally very rare in humans, suggesting that acquisition of Blastocystis ST8 infections from primates by their handlers had occurred in these cases. Data from published studies of non-human primates, other mammals and birds were collected and interpreted to generate a comprehensive overview on the ST distribution in such animals. On the basis of information on 438 samples, it was found that Blastocystis from primates belong mainly to ST1, ST2, ST3, ST5 and ST8, ungulates and dogs mainly ST1, ST2, ST3, ST5 and ST10, rodents ST4 and birds mainly ST6 and ST7. The data indicate moderate host specificity, most clearly exemplified by the fact that STs isolated from avian and non-avian hosts rarely overlap.     

Physiological reactions of primates to 9-D immersion and head-down tilt

Purpose of the investigation was to compare physiological reactions of primates (Macaca mulatta) to microgravity simulated by immersion and head-down tilt (HDT). In immersion experiments, primates in waterproof suits were put into motion-restraining chairs and immersed into water (t=35.4 degrees C) breast-deep for 9 days. In 9-d HDT experiments, prone primates were motor restrained in dedicated tilt beds at -5 degrees. It was found that the CNS functioning was significantly affected, the plasma volume reduced and the marrow erythropoietic function declined. Atrophy developed in leg muscles on a backdrop of iliopectineal spongy osteopenia. Loss in hydration, inhibition of erythropoietic hemopoiesis and iliopectineal spongy osteopenia were more pronounced following immersion than HDT.