6.1.2: Sociality, Residency Patterns, and Dispersal

The majority of mammal species are solitary, with individuals living alone, except for mothers and dependent offspring. However, most primate species live in groups. Primate groups vary in size, composition, and cohesiveness. Gibbons and siamangs of Southeast Asia and titi monkeys of South America form long-term pair bonds with groups consisting of an adult male and female with their dependent young. Ukaris of South America and ring-tailed lemurs of Madagascar both live in groups of up to 35 individuals containing multiple adult males and females, juveniles, and infants. Gorilla troops typically number between eight and 10 individuals, consisting of multiple females, juveniles, and infants but only one adult male, the silverback. Some primate groups (like gorillas, ukaris, and ring-tailed lemurs) are stable and cohesive over long periods, except for the dispersal of some individuals who leave the group. Others, like chimpanzees and spider monkeys, have more fluid social systems, called fission-fusion, where groups break up and reunite based on differences in food availability throughout the year. In this section, we’ll examine why primates live in groups and who stays, who goes, and why.

Why Do Primates Live in Groups?

Because group living is relatively unusual among mammals but quite common among primates, a central question for primatologists is: Why do primates live in groups? The answer is that primates live in groups when the benefits of feeding competition and/or predation avoidance exceed the costs.

Feeding Competition

As discussed in the previous section, when species feed on high-quality, scarce food (like fruit), larger groups mean there are more individuals competing for access to the resource. The result of this competition takes the form of dominance hierarchies and increased day-range length. A dominance hierarchy is the result of aggressive and submissive interactions, but once established, a dominance hierarchy functions to reduce levels of aggression because all individuals “know their place.” Female vervets illustrate the costs and benefits of different dominance ranks (Whitten 1983). Dominant (high-ranking) females spend more time feeding and eat more ripe fruit than subordinates (low-ranking), so they consume more nutrients. This affects their health and fitness (an individual’s reproductive success relative to that of other individuals; Whitten 1983). Dominants weigh more, start reproducing earlier, and produce more offspring than subordinates do. So why do subordinate females remain in the group? The answer is that larger groups are more successful in competition with other groups. In a long-term study of vervets in Kenya’s Amboseli National Park, larger vervet groups had larger and better home ranges, which importantly included access to permanent sources of water. The result? Females in larger groups had shorter interbirth intervals (the average length of time between one birth and the next) and higher average infant and female survival rates than the smallest group. In terms of competition for resources, the benefits of being a member of a larger vervet group (even a low-ranking member) outweigh the costs (Cheney and Seyfarth 1987).

Predator Avoidance

While D. L. Cheney and R. M. Seyfarth (1987) found that larger vervet groups had higher average infant and female survival rates, causes of mortality differed based on group size. Unlike the small group, mortality in larger groups was almost entirely due to predation, and this highlights another set of costs and benefits of group living. Larger groups are more conspicuous than smaller groups. This is one of the reasons that primates who rely on crypsis to avoid predation (like the slow loris; Figure 6.16) are often solitary. However, some anti-predator behaviors, like shared vigilance duties, alarm calling, and mobbing, are responses to predators that are only available to group-living species (like Hanuman langurs; Figure 6.17). Whether or not a primate is group-living or solitary, it engages in some form of vigilance, or watchful behavior to detect potential danger. Often, researchers cannot determine whether vigilance is intended to detect predators or potential competing conspecifics (with predator detection as a side benefit). However, because vigilance interferes with other important behaviors like feeding, resting, or being social, primates who live in groups benefit from sharing the cost of vigilance and reaping the rewards of early predator detection. When a predator is detected, an alarm call is given. We will discuss the information communicated through alarm calls in greater detail in the “Communication” section, but in short, they serve one of two functions: (1) to alert members of the group to the presence of a predator or (2) to alert the predator that it has been detected. In some species, mobbing (the act of cooperatively attacking or harassing a predator) accompanies alarm calls. Mobbing involves two or more individuals making repeated advances on a predator, often while vocalizing and/or displaying. The point of mobbing is to drive off or distract the predator long enough for others to escape. Primates have been observed mobbing several species of predators, including chimpanzees, leopards, and eagles, but snakes are the most common targets. Although mobbing often occurs as the predator is approaching, in some cases, it occurs after a predator has attacked and escalates to a counter-attack. A group of Coquerel’s sifaka mobbed a Madagascar ground boa that had grabbed and was constricting an adult female. The attack, which consisted of loud alarm calls, along with multiple individuals biting and scratching the snake’s body and head, resulted in the snake releasing the female sifaka, who survived (Gardner et al. 2015). Similar reports of mobbing resulting in the rescue of a group member from the coils of a boa constrictor have also been reported for white-faced capuchins and moustached tamarins. Such examples clearly illustrate the benefits of group living.

Polyspecific Associations

In regions with a large number of sympatric primate species (Figure 6.13), interactions between species are bound to occur. Often interactions are competitive (more on this in the “Competition for Food” section). However, polyspecific associations are different. These are associations between two or more different species in which at least one species changes its behavior to maintain the association. Polyspecific associations have been documented in many New World and Old World primate communities. While some associations are short in duration, others can be semi-permanent. In these cases, species are found more often in association than not. As discussed above, decades of research indicates that primates obtain benefits from living in groups with conspecifics. So why do some primates form associations with other species instead of increasing the size of their own group? Although the specific costs and benefits of polyspecific associations differ in each case, in general, species that form these associations gain foraging or anti-predator benefits while avoiding within-group competition for food that occurs in a larger group of conspecifics.

There are many possible foraging benefits of polyspecific associations. In some cases, one species gains access to a food resource that is otherwise inaccessible. In Manu National Park, in Peru, brown capuchins chase smaller squirrel monkeys away from scarce resources. Despite this, squirrel monkeys maintain the association because the capuchins can crack open palm nuts that squirrel monkeys cannot. Squirrel monkeys then feed on kernels dropped by the capuchins (Terborgh 1984). In Brazil, saddle-back tamarins obtain a slightly different foraging benefit by associating with moustached tamarins. The larger (in body and group size) moustached tamarins flush insects from the upper canopy as they forage. The fleeing insects are captured at high rates by saddle-back tamarins foraging below them (Peres 1992). In other cases, associated species avoid competition for food. In Makokou, Gabon, associations form between greater spot-nosed guenons, moustached guenons, and crowned guenons, despite the fact that these closely related species have very similar diets. Instead of competing for food, the species benefit from reduced indirect competition. Because they encounter food sites together, they avoid visiting a site that might have been depleted by one of the other species if they were foraging separately (Gautier-Hion et al. 1983).

In other cases, the benefit of polyspecific associations is predator avoidance. Like foraging benefits discussed above, anti-predator benefits are variable. In some cases, one species may be particularly good at detecting a specific type of predator and may alert the other species to its presence. In Makokou, Gabon, the guenon species discussed above play different alarm call roles when associated (Gautier-Hion et al. 1983). Moustached guenons, who spend more time close to the ground, are usually the first to alarm call at terrestrial predators. Crowned guenons, who spend more time high in the forest canopy, are most likely to detect aerial predators. Because both species give an alarm call familiar to the other species in the association, everyone benefits from increased predator detection. Sometimes associations result in proactive defense against predators. In the Una Biological Reserve in Bahia, Brazil, a mixed-species group of golden-headed lion tamarins and black-tufted ear marmosets was observed jointly mobbing an ocelot (Raboy et al. 2008). In Taï National Park in Côte d’Ivoire, putty-nosed guenons join Diana monkeys in coordinated mobbing of crowned eagles (Eckardt and Zuberbühler 2004).

Dispersal: Who Goes, Who Stays, and Why?

Whether primates live in groups or are solitary, some individuals must disperse, or leave the place or group of their birth. In the solitary orangutan, females spend about seven years caring for each highly dependent offspring. But once mature, offspring of both sexes leave their mother’s home range. If this did not happen, orangutans would not be solitary. In group-living species, one or both sexes must disperse at sexual maturity. Which sex disperses depends on the relative costs and benefits to each. In most primate species, males are the dispersing sex because the benefits of dispersal, including increased access to mates and reduced competition from other males, outweigh the costs. For most female primates, the opposite is true: they usually benefit from remaining philopatric, or in the group of their birth. This allows them to maintain strong social alliances so that they can compete successfully against other groups for food. In species where females are typically philopatric, like vervets and macaques, female dispersal only occurs under extreme circumstances, such as when group size falls to precariously low levels. Despite the patterns discussed below, it is important to remember that there is considerable variation in dispersal and numerous exceptions to any rule. Although uncommon, female dispersal has been observed in typically female philopatric species like capuchins and baboons. Likewise, female philopatry has been recorded in species like chimpanzees and muriquis, whose females typically disperse. These exceptions underscore the high degree of behavioral variation and flexibility displayed by primates.

Costs of Dispersal

Transferring into a new group can be fraught with difficulties. Members of both sexes may experience aggression from same-sex members of their chosen group because they are viewed as potential competitors. Aggression toward transferring individuals has been documented in multiple species, and aggression directed toward transferring males is almost universal and can be lethal (Isbell and Van Vuren 1996). During my fieldwork in Kenya, a subadult male patas monkey who had recently dispersed attempted to return to the group into which he was born, which happened to be our study group. The resident male attacked him and severely wounded him. We did not see the subadult male again and assume he died. Transferring females can also experience aggression. Female red howler monkeys are often prevented from joining established groups and can be injured by resident females when they attempt to do so (Crockett and Pope 1988). Even if new group mates are not aggressive, the dispersing individual has lost all alliances with members of their old group and must expend time and energy developing relationships with members of the new group. New group members are often lower in the dominance hierarchy and may produce fewer offspring and suffer from greater mortality. Individuals who disperse into an unfamiliar home range must contend with a lack of ecological knowledge. For species who feed on clumped and seasonal resources like fruit, the lack of knowledge about food sites in a new area can be a significant cost. Lack of knowledge about predators can also put dispersing individuals at greater risk, as appears to be the case for vervets. When their trees deteriorated, vervets in Amboseli National Park, in Tanzania, began to shift home ranges. Use of unfamiliar areas correlated with an increase in vervet disappearances. Most were suspected to have died from leopard predation, probably due to a lack of knowledge about escape routes and refuges in unfamiliar areas (Isbell et al. 1990). Individuals who lose both social allies and knowledge of a specific area when they disperse may suffer even higher costs (Isbell and Van Vuren 1996).

Benefits of Dispersal

If the costs are so high, why do individuals disperse at all? The answer to this question depends on whether we look at the immediate cause of dispersal or the reproductive consequences over the long term. In the short term, the cause of dispersal is often eviction by same sex members of the group, as occurs in gibbons, ring-tailed lemurs, red howler monkeys, and other species. In Hanuman langurs, the resident male may be kicked out by bachelor males who invade heterosexual groups during the breeding season. In other cases, maturing individuals may choose to leave their group because they are attracted to individuals in another group. This explanation is supported by the observation that most transfers by males between groups occur during the breeding season, when females are sexually receptive, or ready to mate. Among hamadryas baboons of Ethiopia, one cause of female dispersal is abduction of juvenile females by adult males. The male incorporates the female into his harem and mates with her when she reaches adulthood (Swedell and Schreier 2006). In chimpanzees, females disperse because males gain significant benefits from remaining in their natal group (the group into which they are born). These benefits include hunting cooperatively and patrolling the community boundary together (Lutz et al. 2016; Stumpf et al. 2009). Other explanations for dispersal are related to enhancing reproductive success, or one’s genetic contribution to future generations, often measured through number of offspring produced. A male may disperse to enter a group with fewer same-sex individuals, so as to avoid competition for mates. Likewise, dispersing into a group with more members of the opposite sex can increase an individual’s mating opportunities. Perhaps the most common explanation for dispersal of at least one sex from the perspective of reproductive success is to avoid inbreeding, or mating with close relatives. When close relatives mate, the likelihood that the offspring will inherit two copies of a recessive gene increases. If the trait that these recessive genes code for is harmful, then such matings can result in inbreeding depression, or reduced fitness of the population. Evidence for inbreeding avoidance as an explanation for dispersal includes the fact that natal dispersal, or dispersal out of the group of one’s birth, takes place at sexual maturity and that at least one sex always disperses.