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.     

Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator

Predation is an important selective pressure in natural ecosystems. Among non-human primates, relatively little is known about how predators hunt primate prey and how primates acquire adaptive responses to counteract predation. In this study we took advantage of the recent reintroduction of radio-tagged harpy eagles (Harpia harpyja) to Barro Colorado Island (BCI), Panama to explore how mantled howler monkeys (Alouatta palliata), one of their primary prey, acquire anti-predator defences. Based on the observation that harpies follow their prey prior to attack, and often call during this pursuit period, we broadcast harpy eagle calls to howlers on BCI as well as to a nearby control population with no harpy predation. Although harpies have been extinct from this area for 50-100 years, results indicate that BCI howlers rapidly acquired an adaptive anti-predator response to harpy calls, while showing no response to other avian vocalizations; howlers maintained this response several months after the removal of the eagles. These results not only show that non-human primates can rapidly acquire an alarm response to a newly introduced predator, but that they can detect and identify predators on the basis of acoustic cues alone. These findings have significant implications both for the role of learning mechanisms in the evolution of prey defence and for conservation strategies, suggesting that the use of 'probing' approaches, such as auditory playbacks, may highly enhance an a priori assessment of the impact of species reintroduction.     

Risky Business? Lethal Attack by a Jaguar Sheds Light on the Costs of Predator Mobbing for Capuchins (Cebus capucinus)

While some primates attempt to avoid predation by fleeing or hiding, others actually approach, harass, and sometimes attack potential predators, a behavior known as mobbing. Mobbing seems to invite obvious risks, but predators have rarely been observed to injure or kill animals that harass them. The true costs of predator mobbing and the functional significance of this behavior remain poorly understood. Here, we report a fatal attack by a jaguar (Panthera onca) on a mobbing capuchin (Cebus capucinus) that we observed on Barro Colorado Island, Panama. This rare observation illustrates that mobbing predators such as large felids can, indeed, be costly. However, to understand fully the costs of mobbing, the energetic and opportunity costs that primates incur when they harass predators must also be considered.     

Puncture marks on early African anthropoids

Field studies of living primates have shown that primate predation is a rare event. This must also have been true for past primate communities. In the Fayum Oligocene of Egypt, specimens of all four species of Upper Fossil Wood Zone primates show evidence of tooth puncture marks. Of the four potential groups of primate predators--the snakes, the raptors, the crocodiles, and the primitive carnivores or creodonts--only the crocodiles and the creodonts could have made these puncture marks. When one compares the feeding habits of living crocodiles and mammalian carnivores with the evidence from the Fayum, it appears that the Fayum primates were preyed upon and/or scavenged by mammalian carnivore-like animals. The dismemberment of the Fayum primates by Oligocene predators indicates, in part, why the Fayum fossil material is rarely articulated. Bone damage by predators may well set limits on what bone associations can be discovered in the Fayum even before the bones are scattered and buried by depositional processes.     

Predation and primate evolution

This paper presents the results of a general review of predation on nonhuman primates as a selective force in primate evolution. Testable hypotheses derived from the literature on predation on primates, concerning sexual dimorphism, male defense, group size, solitaries, transfer, subgrouping, and sex ratio, were applied to the available data on populations with varying predation rates in search of significant correlations. All seven hypotheses were supported, indicating that predation is and has been an important determinant of primate evolutionary history. Suggestions for accumulating a larger and more accurate body of information on predation rates on primates are offered.     

Masticatory stress, orbital orientation and the evolution of the primate postorbital bar

A postorbital bar is one of a suite of derived features which distinguishes basal primates from their putative sister taxon, plesiadapiforms. Two hypotheses have been put forward to explain postorbital bar development and variation in circumorbital form: the facial torsion model and visual predation hypothesis. To test the facial torsion model, we employ strain data on circumorbital and mandibular loading patterns in representative primates with a postorbital bar and masticatory apparatus similar to basal primates. To examine the visual predation hypothesis, we employ metric data on orbit orientation in Paleocene and Eocene primates, as well as several clades of visual predators and foragers that vary interspecifically in postorbital bar formation.A comparison of galago circumorbital and mandibular peak strains during powerful mastication demonstrates that circumorbital strains are quite low. This indicates that, as in anthropoids, the strepsirhine circumorbital region is excessively overbuilt for countering routine masticatory loads. The fact that circumorbital peak-strain levels are uniformly low in both primate suborders undermines any model which posits that masticatory stresses are determinants of circumorbital form, function and evolution. This is interpreted to mean that sufficient cortical bone must exist to prevent structural failure due to non-masticatory traumatic forces. Preliminary data also indicate that the difference between circumorbital and mandibular strains is greater in larger taxa.Comparative analyses of several extant analogs suggest that the postorbital bar apparently provides rigidity to the lateral orbital margins to ensure a high level of visual acuity during chewing and biting. The origin of the primate postorbital bar is linked to changes in orbital convergence and frontation at smaller sizes due to nocturnal visual predation and increased encephalization. By incorporating in vivo and fossil data, we reformulate the visual predation hypothesis of primate origins and thus offer new insights into major adaptive transformations in the primate skull.     

Leopard predation and primate evolution

Although predation is an important driving force of natural selection its effects on primate evolution are still not well understood, mainly because little is known about the hunting behaviour of the primates' various predators. Here, we present data on the hunting behaviour of the leopard (Panthera pardus), a major primate predator in the Tai; forest of Ivory Coast and elsewhere. Radio-tracking data showed that forest leopards primarily hunt for monkeys on the ground during the day. Faecal analyses confirmed that primates accounted for a large proportion of the leopards' diet and revealed in detail the predation pressure exerted on the eight different monkey and one chimpanzee species. We related the species-specific predation rates to various morphological, behavioural and demographic traits that are usually considered adaptations to predation (body size, group size, group composition, reproductive behaviour, and use of forest strata). Leopard predation was most reliably associated with density, suggesting that leopards hunt primates according to abundance. Contrary to predictions, leopard predation rates were not negatively, but positively, related to body size, group size and the number of males per group, suggesting that predation by leopards did not drive the evolution of these traits in the predicted way. We discuss these findings in light of some recent experimental data and suggest that the principal effect of leopard predation has been on primates' cognitive evolution.     

Primate Seed Dispersal and Forest Restoration: An African Perspective for a Brighter Future

Primate seed dispersal is a vital, but complex, ecological process that involves many interacting agents and plays important roles in the maintenance of old-growth forest, as well as in the development of regenerating forest. Focusing primarily on African examples, in this article we briefly review the ecological process of primate seed dispersal, highlighting understudied and contentious topics, and then we discuss how our knowledge on primate seed dispersal can promote both forest restoration and primate conservation. Though it is frequently claimed that primates are critically important for the maintenance of diverse tropical forest ecosystems, we believe that more empirical evidence is needed to support this claim. Confounding factors can often be difficult to rule out and long-term studies extending beyond the seedling or sapling stage are very rare. In addition, though primates are critical for initial seed dispersal of many tree species, spatial and temporal variation in post-deposition processes, such as secondary seed dispersal and predation by rodents, can dramatically alter the initial patterns generated by primates. However, given the need for immediate conservation action to prevent further primate extinctions, we advocate that the knowledge about primate seed dispersal be used in formulating informed conservation plans. One prominent area where this knowledge will prove extremely valuable is in forest restoration efforts. To aid in the development of such efforts, we pose five questions, the answers to which will help facilitate forest restoration becoming a useful tool in strategies designed to conserve primates.     

Experimental studies of evolution in guppies: a model for understanding the evolutionary consequences of predator removal in natural communities

Guppies (Poecilia reticulata) in Trinidadian streams are found with a diversity of predators in the lower reaches of streams, but few predators in the headwaters. These differences have caused the adaptive evolution of guppy behaviour, morphology, male colouration and life history. Waterfalls often serve as barriers to the upstream distribution of predators and/or guppies. Such discontinuities make it possible to treat streams like giant test tubes by introducing guppies or predators to small segments of streams from which they were previously excluded. Such experiments enable us to document how fast evolution can occur and the fine spatial scales over which adaptation is possible. They also demonstrate that the role predators play in structuring this ecosystem resembles many others studied from a more purely ecological perspective; in these streams, as elsewhere, predators depress the numbers of individuals in prey species which in turn reduces the effects of the prey species on other trophic levels and hence the structure of the ecosystem. A focus on predators is important in conservation biology because predators are often the organisms that are most susceptible to local extinction. Their selective loss occurs because large predators have been deliberately exterminated and/or are more susceptible to environmental disturbances. Furthermore, we will argue that predator re-introductions might be destabilizing if, in the absence of predators, their prey have evolved in a fashion that makes them highly susceptible to predation, even after time intervals as short as 50-100 years. A better understanding of the evolutionary impacts of top predators will be critical goal for the policy and practice of large carnivore restoration in the future.     

Evidence of leopard predation on bonobos (Pan paniscus)

Current models of social organization assume that predation is one of the major forces that promotes group living in diurnal primates. As large body size renders some protection against predators, gregariousness of great apes and other large primate species is usually related to other parameters. The low frequency of observed cases of nonhuman predation on great apes seems to support this assumption. However, recent efforts to study potential predator species have increasingly accumulated direct and indirect evidence of predation by leopards (Panthera pardus) on chimpanzees and gorillas. The following report provides the first evidence of predation by a leopard on bonobos (Pan paniscus).     

Theory and method in studies of vigilance and aggregation

Predation is considered one of the most important selective pressures on free-ranging animals. Our understanding of it derives mainly from studies of individual vigilance (visual scanning of the surroundings beyond the immediate vicinity) and aggregation in prey. Vigilance bears a direct relationship to aggregation, because animals in groups may rely on associates for early warning of danger. This review addresses the relationship between vigilance and aggregation with particular attention to the prediction that individual vigilance declines with increasing group size. Contrary to most other animals studied, primates do not support the prediction. Exploring this, I examined the assumptions underlying vigilance theory in the light of primate behaviour. First I tested whether manual harvesting and upright processing of food as seen among primates might permit them to feed and scan simultaneously. I found no support for this idea. Next I examined the targets of primate vigilance and found that one component (within-group vigilance) might explain the differences between primates and other animals. Finally, I evaluated whether individual primates in large groups face a lower risk of predation than those in small groups. A conclusion was impossible, but by separating group-level from individual-level risk, I was able to identify several common circumstances in which group size would not predict individual risk or vigilance. These circumstances arose for primates and nonprimates alike. I concluded that the relationship of vigilance to aggregation is not straightforward. The absence of a group-size effect on vigilance among primates is probably due to functional differences in vigilance behaviour or safety in groups, not to methodological differences. Furthermore, future work on animal vigilance and aggregation must fully consider both the targets of glances, and the assumption that larger groups are safer from predators. I predict that animals will not relax vigilance in larger groups if conspecific threat increases with group size. Group size will not predict individual risk of predation nor individual vigilance rates when predators do not rely on surprise, or when predators select a small subset of highly vulnerable group members. Copyright 2000 The Association for the Study of Animal Behaviour.     

Party size and early detection of predators in sumatran forest primates

Theoretical considerations suggest that the ability to detect the presence or approach of a predator when there is still enough time to flee (early detection) should improve with group size, if group living is to be advantageous for individual non-human primates. The hypothesis that the distance at which forest primates detect predators increases with the size of their party was confirmed by observation. It was found that in addition to party size height (vegetation density) could also influence detection distance. Because height relates not only to visibility but also to the number of potential predators, one would predict that small parties are found higher in the canopy to compensate for the increased risk of predation. This prediction was confirmed using data on long-tailed macaques (Macaca fascicularis). The correlation found between party size and predation risk demonstrates that forest monkeys can adjust their behaviour in response to changes in predation risk, and hence support the hypothesis that predation risk has been an important, perhaps even the only, selective force responsible for the evolution of group living in non-human primates.     

Frugivory and Seed Fate in Bursera inversa (Burseraceae) at Tinigua Park,Colombia: Implications for Primate Conservation1

The large ateline primates are efficient seed dispersers in Neotropical forests and hunting is driving their populations to extinction, but we do not know whether other frugivores could substitute primates in their ecological role as seed dispersers. In this study we test this possibility using a potential keystone species (Bursera inversa) at Tinigua Park, Colombia. This plant species allows us to compare seed removal rates between emergent, isolated trees, without primate visitors and trees with connected crowns. We used traps to estimate fruit production and seed removal rates in six different trees, and fruiting trees were observed during 2 yr to quantify the number of seeds manipulated by different animal species. We carried out seed predation experiments to test if seed removal by predators was affected by distance or density effects. We found that the most productive trees attracted more visiting species and seed removal rates differed among trees, the lowest corresponding to trees without primate access. Seed removal rates from the ground by predators were not higher below parental trees than away from them, but the distribution of saplings in the forest suggests that seed dispersal is advantageous. Although it is likely that the effect of primate extinctions will vary depending on tree species traits, conserving the populations of primate seed dispersers is critical to maintain the ecological processes in this forest.     

Run,hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (<Emphasis Type="Italic">Chiropotes albinasus</Emphasis>, Pitheciidae) in southeastern Amazonia

Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.     

Primate group size and interpreting socioecological models: Do folivores really play by different rules?

Because primates display such remarkable diversity, they are an ideal taxon within which to examine the evolutionary significance of group living and the ecological factors responsible for variation in social organization. However, as with any social vertebrate, the ecological determinants of primate social variability are not easily identified. Interspecific variation in group size and social organization results from the compromises required to accommodate the associative and dissociative forces of many factors, including predation, 1 - 3 conspecific harassment and infanticide, 4 - 6 foraging competition 1 , 7 and cooperation, 8 dominance interactions, 9 reproductive strategies, and socialization. 10 - 12 Causative explanations have emerged primarily through the construction of theoretical models that organize the observed variation in primate social organization and group size relative to measurable ecological variation.     

Nocturnal nest predation: a potential obstacle to recovery of a Florida Scrub-Jay population

ABSTRACT.   Population declines among birds are often linked to habitat change and associated increases in nest predation rates. In species of conservation concern identifying nest predators is an important first step in developing management strategies to mitigate low nesting success caused by depredation. Because predator composition varies geographically and with landscape factors habitat restoration may need to be tailored to reduce locally important predators. We used miniature video cameras to identify nest predators in a population of Florida Scrub-Jays ( Aphelocoma coerulescens ) significant to conservation. At 22 nests we observed 25 predation events; 22 (88%) of these events were nocturnal. Yellow rat snakes ( Elaphe obsoleta ) had the highest daily predation rate and accounted for 76% of egg and nestling losses. Florida Scrub-Jays are vulnerable to nocturnal nest predation because their vigilance behavior is ineffective against nocturnal predators, breeders cannot defend against nocturnal predators, and brooding females are at risk of being killed by nocturnal predators. If current habitat restoration efforts do not reduce numbers of yellow rat snakes and improve scrub-jay nesting success, management actions to reduce populations of nocturnal snakes may need to be considered.     

Does predation select for or against avian coloniality? A comparative analysis

Some studies have supported predation as a selective pressure contributing to the evolution of coloniality. However, evidence also exists that colonies attract predators, selecting against colonial breeding. Using comparative analyses, we tested the reduced predation hypothesis that individuals aggregate into colonies for protection, and the opposite hypothesis, that breeding aggregations increase predation risk. We used locational and physical characteristics of nests to estimate levels of species' vulnerability to predation. We analysed the Ciconiiformes, a large avian order with the highest prevalence of coloniality, using Pagel's general method of comparative analysis for discrete variables. A common requirement of both hypotheses, that there is correlated evolution between coloniality and vulnerability to predation, was fulfilled in our data set of 363 species. The main predictions of the reduced predation hypothesis were not supported, namely that (1) solitary/vulnerable species are more prone to become colonial than solitary/protected species and (2) colonial/protected species are more likely to evolve towards vulnerability than solitary/protected species. In contrast, the main predictions of the increased predation hypothesis were supported, namely that colonial/vulnerable species are more prone (1) to become protected than solitary/vulnerable species and/or (2) to become solitary than colonial/protected species. This suggests that the colonial/vulnerable state is especially exposed to predation as coloniality may often attract predators rather than provide safety.     

Not in their genes: Phenotypic flexibility, behavioural traditions and cultural evolution in wild bonnet macaques

Phenotypic flexibility, or the within-genotype, context-dependent, variation in behaviour expressed by single reproductively mature individuals during their lifetimes, often impart a selective advantage to organisms and profoundly influence their survival and reproduction. Another phenomenon apparently not under direct genetic control is behavioural inheritance whereby higher animals are able to acquire information from the behaviour of others by social learning, and, through their own modified behaviour, transmit such information between individuals and across generations. Behavioural information transfer of this nature thus represents another form of inheritance that operates in many animals in tandem with the more basic genetic system. This paper examines the impact that phenotypic flexibility, behavioural inheritance and socially transmitted cultural traditions may have in shaping the structure and dynamics of a primate society — that of the bonnet macaque (Macaca radiata), a primate species endemic to peninsular India. Three principal issues are considered: the role of phenotypic flexibility in shaping social behaviour, the occurrence of individual behavioural traits leading to the establishment of social traditions, and the appearance of cultural evolution amidst such social traditions. Although more prolonged observations are required, these initial findings suggest that phenotypic plasticity, behavioural inheritance and cultural traditions may be much more widespread among primates than have previously been assumed but may have escaped attention due to a preoccupation with genetic inheritance in zoological thinking. This paper is dedicated with admiration and gratitude to the late Dr Raja Ramanna, a man who held all primates in great esteem.     

Cognitive adaptations of social bonding in birds

The 'social intelligence hypothesis' was originally conceived to explain how primates may have evolved their superior intellect and large brains when compared with other animals. Although some birds such as corvids may be intellectually comparable to apes, the same relationship between sociality and brain size seen in primates has not been found for birds, possibly suggesting a role for other non-social factors. But bird sociality is different from primate sociality. Most monkeys and apes form stable groups, whereas most birds are monogamous, and only form large flocks outside of the breeding season. Some birds form lifelong pair bonds and these species tend to have the largest brains relative to body size. Some of these species are known for their intellectual abilities (e.g. corvids and parrots), while others are not (e.g. geese and albatrosses). Although socio-ecological factors may explain some of the differences in brain size and intelligence between corvids/parrots and geese/albatrosses, we predict that the type and quality of the bonded relationship is also critical. Indeed, we present empirical evidence that rook and jackdaw partnerships resemble primate and dolphin alliances. Although social interactions within a pair may seem simple on the surface, we argue that cognition may play an important role in the maintenance of long-term relationships, something we name as 'relationship intelligence'.