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.     

Predicting group size in primates: foraging costs and predation risks

We present a direct test of the long-standing hypothesis thatfood competition limits primate group size. Group size is acritical social variable because it constrains most other aspectsof social organization. We develop a simple population-specificindex of indirect feeding competition based on daily foragingcosts. This index explains nearly two-thirds of between-populationvariation in mean group sizes of mostly fruit-eating (but notof mostly leaf-eating) primates. Group size is also significantlyrelated to body size and terrestriality (or use of open country),which are suspected correlates of predation risk, although feedingcompetition remains an important predictor of group size evenwhen these correlates are controlled. Phylogeny also appearsto be important: the differences between observed mean populationgroup sizes and those predicted using ecological factors aremost positive for the Old World monkeys and most negative forthe lemuroids in our sample. The weak relationship between groupsize and feeding competition found for folivorous species maybe explained either by the energetic constraints of a leafydiet or by limits to group size imposed by infanticide as ahabitual male reproductive strategy.     

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.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

The effect of group size on vigilance in Ruddy Turnstones Arenaria interpres varies with foraging habitat

Foraging birds can manage time spent vigilant for predators by forming groups of various sizes. However, group size alone will not always reliably determine the optimal level of vigilance. For example, variation in predation risk or food quality between patches may also be influential. In a field setting, we assessed how simultaneous variation in predation risk and intake rate affects the relationship between vigilance and group size in foraging Ruddy Turnstones Arenaria interpres. We compared vigilance, measured as the number of ‘head‐ups’ per unit time, in habitat types that differed greatly in prey energy content and proximity to cover from which predators could launch surprise attacks. Habitats closer to predator cover provided foragers with much higher potential net energy intake rates than habitats further from cover. Foragers formed larger and denser flocks on habitats closer to cover. Individual vigilance of foragers in all habitats declined with increasing flock size and increased with flock density. However, vigilance by foragers on habitats closer to cover was always higher for a given flock size than vigilance by foragers on habitats further from cover, and habitat remained an important predictor of vigilance in models including a range of potential confounding variables. Our results suggest that foraging Ruddy Turnstones can simultaneously assess information on group size and the general likelihood of predator attack when determining their vigilance contribution.     

Density-dependent investment in costly anti-predator defences: an explanation for the weak survival benefit of group living

A central explanation for group living across animal taxa is the reduced rate of attack by predators. However, many field observations show a weak or non-existent effect of group size on per capita mortality rates. Herein we resolve this apparent paradox. We found that Pieris brassicae larvae defended themselves less readily when in groups than when alone, in that they were more reluctant to regurgitate in response to simulated attacks and produced less regurgitant. Furthermore, a simple model demonstrates that this reluctance was sufficient to cancel out the benefit from being in a group. This conditional strategy can be understood in terms of the costs and benefits of defences. For grouped individuals, defence is less often required because attack rates are lower and the costs of defence may be higher due to competition for resources. These phenomena are likely to be widespread in facultatively gregarious species that utilise anti-predator defences.     

Habitat use of the white‐headed langurs in limestone forest of Southwest Guangxi,China: Seasonality and group size effects

Understanding how animals cope with habitat‐specific environmental factors can assist in species conservation management. We studied the habitat use of four groups (two large and two small groups) of white‐headed langurs (Trachypithecus leucocephalus) living in the forest of southwest Guangxi, China between September 2016 and February 2017 via instantaneous scan sampling. Our results showed that the langurs primarily used hillsides (55.91% ± 6.47%), followed by cliffs (29.70% ± 5.48%), hilltops (7.26% ± 3.55%), flat zones (6.99% ± 6.58%), and farmlands (0.14% ± 0.28%). The langurs moved most frequently on hillsides (49.35% ± 6.97%) and cliffs (35.60% ± 9.17%). The hillsides were more frequently used (66.94% ± 7.86%) during feeding, and the langurs increased the use of hilltops during the rainy season, and the use of cliffs in the dry season. The langurs frequently rested on hillsides (49.75% ± 8.16%) and cliffs (38.93% ± 8.02%). The larger langur group used cliffs more frequently when moving and resting, whereas the small langur group used hillsides more frequently while resting. Langurs in all groups avoided the flat zones for feeding. Their use of habitat reflected the balancing of foraging needs, thermoregulation, and predator avoidance. We conclude that the ecological factors are determinants of habitat use for white‐headed langurs. Our findings suggest that conservation efforts should focus on protecting the vegetation on the hillsides and restoring the vegetation on the flat zones.     

Gorilla society: What we know and don't know

Science is fairly certain that the gorilla lineage separated from the remainder of the hominoid clade about eight million years ago, 2 , 4 and that the chimpanzee lineage and hominin clade did so about a million years after that. 1 , 2 However, just this year, 2007, it was discovered that although the human head louse separated from the congeneric chimpanzee body louse (Pediculus) around the same time as the chimpanzee and hominin lineages split, 3 the human pubic louse apparently split from its sister species, the congeneric gorilla louse, Pthirus, 4.5 million years after their host lineages split. 3 No tested explanations exist for the discrepancy. Much is known about hominin evolution, but much remains to be discovered. The same is true of primate socioecology in general and gorilla socioecology in particular.     

Costs and benefits of flocking in foraging white-fronted geese (Anser albifrons): effects of resource depletion

This study investigated the costs and benefits of flocking in white-fronted geese Anser albifrons foraging on rice grains in Japan. The time budgets of focal geese were recorded, and the effects of flock size on the proportions of time spent in vigilant and agonistic behaviour were tested. The results showed that the decline in vigilance level and consequent increase in foraging time were beneficial results of flocking whereas agonistic interactions, a potential cost of flocking, did not increase with increasing flock size. However, seasonal variation in flock size suggested that exploitative competition could be a cost of flocking; the sizes of flocks in spring, when resource depletion had progressed, were significantly reduced compared with those in autumn. An experimental increase in rice density resulted in a significant increase in flock size. We conclude that the flock size of foraging white-fronted geese is a result of compromise between a constant benefit of flocking (i.e. decline in vigilance level) and a cost of flocking varying with food abundance (i.e. exploitative competition).     

A field demonstration of the costs and benefits of group living to edible and defended prey

Both theoretical and laboratory research suggests that many prey animals should live in a solitary, dispersed distribution unless they lack repellent defences such as toxins, venoms and stings. Chemically defended prey may, by contrast, benefit substantially from aggregation because spatial localization may cause rapid predator satiation on prey toxins, protecting many individuals from attack. If repellent defences promote aggregation of prey, they also provide opportunities for new social interactions; hence the consequences of defence may be far reaching for the behavioural biology of the animal species. There is an absence of field data to support predictions about the relative costs and benefits of aggregation. We show here for the first time using wild predators that edible, undefended artificial prey do indeed suffer heightened death rates if they are aggregated; whereas chemically defended prey may benefit substantially by grouping. We argue that since many chemical defences are costly to prey, aggregation may be favoured because it makes expensive defences much more effective, and perhaps allows grouped individuals to invest less in chemical defences.     

The influence of flock size and geometry on the scanning behaviour of spotted turtle doves,Streptopelia chinensis

Abstract The negative correlation between the time individuals spend scanning the environment for predators and group size is usually explained by the benefit of corporate vigilance. However, this negative correlation may be explained additionally in terms of the ‘dilution effect’ and ‘selfish herd geometry’. Our experimental investigation of the scanning behaviour of free-living spotted turtle doves foraging at different shaped feeders revealed that flock geometry influenced individual scanning rates. The time spent scanning declined with group size less rapidly among birds foraging in linear flocks than among those foraging in more two-dimensional flocks. These results were not confounded by aggressive behaviour, and indicate that the benefits of foraging in groups include the so-called selfish herd geometry.     

Costs and benefits of facultative aggregating behaviour in the orb-spinning spider Gasteracantha minax Thorell (Araneae: Araneidae)

Abstract The potential costs and benefits of foraging in aggregations are examined for the orb-spinning spider Gasteracantha minax. Web-site tenacity is low in this species; individuals frequently move among sites, thereby joining aggregations of different sizes. Female spiders in aggregations suffered lower predation rates and attracted more males than their solitary counterparts. However, aggregated eggsacs, probably produced by females in aggregations, experienced higher rates of parasitism than solitary eggsacs. We found no evidence of higher prey capture success rates among spiders in aggregations. However, we demonstrate a novel way in which spiders can increase their foraging efficiency by decreasing silk investment. A spider spinning a web within an existing aggregation can attach the support threads of its web to those of other webs, thereby exploiting the silk produced by other spiders.     

Growth depensation and group behaviour in juvenile hybrid striped bass Morone chrysops×Morone saxatilis: effects of group membership, feeding method, ration size and size disparity

The effects of group membership (three group sizes), feeding method (single site v. scattered), variation in ration size (low v. high) and starting size disparity (range of starting sizes) on growth, growth depensation and group behaviour of juvenile hybrid striped bass (HSB) Morone chrysops female × Morone saxatilis male were tested. Group membership, starting size disparity and ration size affected the growth, growth depensation and behaviour of juvenile HSB. Growth was higher in fish held within large group memberships and high ration treatments. Growth depensation (size variation among individuals of the same age) in group memberships of three and 12 fish per tank was minimal when compared to intermediate memberships (six fish per tank). In addition, small fish held in tanks with fish of intermediate sizes demonstrated higher growth when compared to small fish housed with large individuals. Some behaviours, specifically activity and scramble feeding, were more elevated in large group memberships when compared to groups with fewer members. Activity was also found to increase over time during size disparity testing. Results suggest that HSB are ideally suited for high-density, intensive aquaculture since they appear to thrive in high group memberships of similar starting sizes and when a sufficient amount of feed in administered.     

Genetic relatedness and group size in an aggregation economy

Summary We use Hamilton's Rule to investigate effects of genetic relatedness on the predicted size of social groups. We assume an aggregation economy; individual fitness initially increases with group size, but in sufficiently large groups each member's individual fitness declines with further increments in the size of the group. We model two processes of group formation, designated free entry and group-controlled entry. The first model assumes that solitary individuals decide to join groups or remain alone; group size equilibrates when solitaries no longer choose to join. The second model allows group members to regulate the size of the group, so that the predicted group size results from members' decisions to repel or accept intruding solitaries. Both the Nash equilibrium group size and any change in the equilibrium caused by varying the level of relatedness depend on the particular entry rule assumed. The largest equilibrium group size occurs when solitaries choose between joining or not joining and individuals are unrelated. Increasing genetic relatedness may reduce and can never increase, equilibrium group size when this entry rule applies. The smallest equilibrium group size occurs when group members choose between repelling or accepting intruders and individuals are unrelated. Under this entry rule, increasing genetic relatedness can increase and can never decrease, equilibrium group size. We extend the models' predictions to suggest when individuals should prefer kin vs non-kin as members of the same group.     

Different effects of mating group size as male and as female on sex allocation in a simultaneous hermaphrodite

Sex allocation theory predicts that the optimal sexual resource allocation of simultaneous hermaphrodites is affected by mating group size (MGS). Although the original concept assumes that the MGS does not differ between male and female functions, the MGS in the male function (MGSm; i.e., the number of sperm recipients the focal individual can deliver its sperm to plus one) and that in the female function (MGSf; the number of sperm donors plus one) do not always coincide and may differently affect the optimal sex allocation. Moreover, reproductive costs can be split into “variable” (e.g., sperm and eggs) and “fixed” (e.g., genitalia) costs, but these have been seldom distinguished in empirical studies. We examined the effects of MGSm and MGSf on the fixed and variable reproductive investments in the sessilian barnacle Balanus rostratus. The results showed that MGSm had a positive effect on sex allocation, whereas MGSf had a nearly significant negative effect. Moreover, the “fixed” cost varied with body size and both aspects of MGS. We argue that the two aspects of MGS should be distinguished for organisms with unilateral mating.     

Costs and benefits of interlarval cannibalism in Harmonia axyridis

Cannibalism, which is rather common in ladybirds, has been usually studied at the individual level: benefits of cannibalism for cannibals were estimated. Our study was conducted at the group level: we evaluated the overall effect of interlarval cannibalism on a group of Harmonia axyridis larvae of the fourth instar deprived of food, including both cannibals and their victims. Experiments showed that the probability of pupation in larvae which were kept individually was significantly higher than in larvae kept in groups of five, other conditions being the same. The proportion of samples in which at least one of five individuals pupated among the larvae kept individually was also higher than among those kept in groups suggesting that the eventual benefit of cannibalism was outweighed by the negative impact of aggressive interlarval interactions. The mean and minimum survival time in samples where none of five larvae pupated were longer when larvae were kept individually than when larvae were kept in groups. However, the maximum survival time (the survival time of the last larva in a sample) increased when larvae were kept in groups, which was the only one benefit of cannibalism found in our study. Under natural conditions, the possible adaptive value of this effect is that in the absence of natural prey, longer larval survival time proportionally increases the possibility of finding a new prey patch thereby ensuring survival of the population.     

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit-productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between-site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between-site differences in sociality seem to reflect differences in average fruit availability.