Panamanian white-faced capuchin

Walking on four limbs

The Panamanian white-faced capuchin is a diurnal and arboreal animal.[9] However, it does come down to the ground more often than many other New World monkeys.[17] It moves primarily by walking on all four limbs.[18] It lives in troops, or groups, of up to 40 monkeys (mean 16, range 4–40)[19] and has a male/female adult sex ratio of 0.71 on average (range 0.54–0.88).[19] With rare exceptions, females spend their entire lives with their female kin.[19][20][21] Males migrate to new social groups multiple times during the course of their lifetimes, migrating for the first time between 20 months and 11 years of age.[22][23] The median age of migration in the Santa Rosa population is 4.5 years.[22] Males sometimes migrate alone, but more often they migrate in the company of other males who are often their kin.[21][22][23] One of the unusual features of the kinship structure of the Panamanian white-faced capuchin, relative to other primate species, is the high degree of relatedness within groups that results from the long tenures of alpha males who sire most of the offspring.[24][25] Alpha males have been known to keep their positions as long as 17 years in this species[24][25] and this puts them in the unusual position of being available to sire the offspring of their daughters and granddaughters, who produce their first offspring at about 6–7 years of age.[19][25] Typically, however, alpha males do not breed with their own daughters, even though they do sire virtually all offspring produced by females unrelated to them.[24] Those subordinate males who are allies of the alpha male in group defense are the males who sire the offspring of the alpha male's daughters. The high degree to which alpha males monopolize matings results in an unusually large number of paternal half-siblings and full siblings in this species relative to other primate species.[25]

Kinship is an important organizing factor in the structuring of female-female social relationships.[25] Particularly in larger groups, females preferentially associate with, groom, and provide coalitionary support to their matrilineally related female kin. They do not exhibit a similar preference for their paternal half sisters, which may mean that they only are capable of recognizing kinship through the maternal line.[25] Dominance rank is also an important organizing factor, with females more often grooming and associating with females who are closer to them in the dominance hierarchy.[25] Female-female dyads groom far more than male-female and male-male dyads.[26] Coalitionary aggression is common both among males and females, and capuchins seem to have an excellent understanding of the alliance structure in their group. For example, when capuchins are fighting, they sensibly recruit aid from someone who is both higher ranking than they are and also better friends with themselves than with their opponent.[27]

Female capuchins have linear dominance hierarchies.[26][28] In contrast to many Old World monkeys such as macaques, in which females socially inherit the rank just below their mothers and just above their next oldest sisters, capuchins do not have a highly predictable ranking within their matrilines.[25] Males are typically dominant to females.[29] The alpha male is always easy to discern, but there are sometimes ambiguous rankings among subordinate males.[21][30] Male-male relationships are tense, and affiliation between males is typically expressed by resting in contact, playing, or non-conceptive sex rather than by grooming.[30][31] Males cooperate in coalitions against potential predators, and also in defense of the group against other males.[21][30][32] Occasionally male coalitionary aggression becomes so violent that males are killed, particularly if they are encountered roaming the forest unaccompanied by allies.[21][33] Because aggression from other male capuchins is the leading cause of death (aside from poaching by humans, where there is contact between humans and capuchins), male allies are critical for self-defense during migration, and to assist in taking over other groups.[21] Male emigration to a new troop typically occurs about every 4 years, so most males are in constant danger of having to defend themselves against other groups of males.[8][34][35][36]

Immigrating males often kill young infants when they take over a group.[21][37][38] Females band together to defend their infants from infanticidal males, but they rarely succeed in saving their infants.[21] Because infants inhibit their mothers from ovulating by nursing frequently, males are able to bring females into estrus earlier by killing the infants and thereby terminating nursing; this has the effect of increasing their breeding opportunities.[21][38][39] Females do often mate with the killers of their infants, and with time, they typically become as supportive of the new alpha male as they had been of the previous one.[21] The alpha male helps defend females from subordinate males within the group as well as from infanticidal males from other groups.[21][40]

Panamanian white-faced capuchins engage in strange behaviors within their own troops, including eye-poking, tail-sucking, hand-sniffing, finger biting, hair-prying, and retrieval of an inedible object from a partner's mouth. Within the Cebus Capucinus, it has been hypothesized that these behaviors are done to test the strength of social bonds between individuals in a troop.[2] These specific traditions were studied in four sites in northwestern Costa Rica over the course of 19000 hours.[2] While traditions differed slightly at the sites, i.e., hand-sniffing variance differed in frequency among ages of capuchins, the commonalities of all four locations demonstrated the capuchins engaging in these unique behavioral traits. Interestingly, the study found that some of these traditions die off after 7-10 years, researchers believe that this extinction occurs when the social bonds within the species are strong, and therefore no longer need to exhibit these behaviors. These interactions are unique to the species, however other social traditions that are similar have been observed in Japanese Macaques to also strengthen social bonds and have been widely studied to figure out the significance across primate species.

Eye poking involves two individuals in which one individual inserts their finger into the eyeball of the other, allowing for the finger to go between the eyelid and bottom of the eyeball. The capuchins stay in this position for several minutes, and while doing so the recipient capuchin may stick their fingers into the ear or mouth of the poker. Even if the finger is removed from the eye by accident, the capuchin places the finger back into the socket. This behavior has astonished researchers, as the risk of infection and loss of an eye is prevalent due to the sharpness and unsanitized fingers of the capuchin. Despite the risk, capuchins continuously engage in this tradition due to the benefits of pair-bonding.[2]

Hand-sniffing is another tradition in which the capuchin cups their hands over the nose of another individual. It was hypothesized that this could be some type of olfactory communication, yet the observational data conveyed that this was incorrect.[5] Hand-sniffing is seen in both male and female dyads. Originally, researchers assumed that the females engaging in hand-sniffing did so to synchronize ovarian cycles. The thought process was due to pheromones being transmitted through the nostrils that would influence the reproductive cycle, however, birth cycle and synchronization are shown to instead be multifactorial.[1] While biologists are unsure as to why hand-sniffing has developed in particular, it is a form of grooming that appears to have a correlation with the strengthening of social bonds.

Tail-sucking is one of the stranger forms of grooming that the capuchins take part in. This form of grooming involves both participants in a comfortable, relaxed state. It is not exclusive to the tail, as instances of sucking on other body parts have been observed. However, tail-sucking allows for simultaneous and mutual interaction for both parties. Hair-prying involves the pulling or biting of a piece of hair off one individual and sticking it in the pryer/biter’s mouth. The individual whose hair was taken proceeds to extract the hair from the prier’s mouth. This tradition is also very similar to the retrieval of an inedible object from a partner’s mouth. None of these traditions are harmful, rather, like the other unique capuchin behaviors, they serve as means to strengthen social bonds.

Finger biting is one of the behaviors that researchers noticed most often. Researchers coined the finger biting as a “game” in which an individual would place their finger inside another individual’s closed mouth and attempt to pry the closed mouth by means of force. This involved using hands and feet for leverage. Once the finger was taken out, the roles would be reversed.[1]

These behaviors exhibit a unique perspective on how different species utilize traditions and behaviors to strengthen their social bonds. Further investigation and experiments in other capuchin groups would allow researchers to compare and contrast how social bonds are strengthened through different behaviors.

Panamanian white-faced capuchin troops occupy home ranges of between 32 and 86 hectares (79 and 213 acres).[12] They travel between 1 and 3 km (1⁄2 and 1+3⁄4 mi) daily, averaging 2 km (1+1⁄4 mi) per day.[41] Although they engage in activity that has been described as "territorial", more recent research indicates that white-faced capuchin troops tend to behave aggressively to other white-faced capuchin troops regardless of where they meet, and the aggression is not necessarily intended to exclude the other troops from a specific home range.[42]

Home ranges overlap extensively,[32][43] so groups are not territorial in the strictest sense of the word. Perhaps because of the intensity of male-male competition and the threat of infanticide, interactions between groups are typically hostile: the males display aggressively toward one another and sometimes engage in physical aggression (even killing an opponent), while females grab their infants and run.[32][33] Typically, males are the primary participants in aggressive intergroup encounters, and it seems likely that males are defending access to the females in their groups.[32] Alpha males, who have the largest reproductive stake in the group, participate at a higher rate than subordinate males.[32] Groups with more males have an advantage over groups with fewer males, but the location of the encounter within the home range matters as well; smaller groups defeat larger groups when the contest occurs in the core or center area of the smaller group's home range.[43]

The Panamanian white-faced capuchin sometimes interacts with other sympatric monkey species. Panamanian white-faced capuchins sometimes travel with and even groom Geoffroy's spider monkeys.[12][41] However, aggressive interactions between the capuchins and spider monkeys also occur.[44] Interactions between the Panamanian white-faced capuchin and mantled howler are infrequent, and sometimes result in the capuchins threatening the larger howlers.[41] However, affiliative associations between the capuchins and howlers do sometimes occur, mostly involving juveniles playing together.[44]

Although South American capuchin species often travel with and feed together with squirrel monkeys, the Panamanian white-faced capuchin only rarely associates with the Central American squirrel monkey. This appears to be related to the patchier, more dispersed distribution of food resources in Central America and the fact that there is less dietary overlap between the Central American squirrel monkey and the white-faced capuchin than between their South American counterparts. Therefore, there is less benefit to the Central American squirrel monkey in associating with the Panamanian white-faced capuchin in order to exploit the capuchin's knowledge of food resource distribution. In addition, compared to their South American counterparts, male Panamanian white-headed capuchins are relatively more alert to rival males than to predators, reducing the predator detection benefits that the Central American squirrel monkey receives from associating with the Panamanian white-faced capuchin compared to its South American counterparts. Since the squirrel monkeys generally initiate interactions with the capuchins in South America, the fact that similar associations would impose higher foraging costs and impart fewer predator detection benefits to the Central American squirrel monkey leads to fewer associations with the Panamanian white-faced capuchin.[14][45][46][47]

Several non-primate animal species tend to follow troops of white-faced monkeys or are otherwise attracted by their presence. white-lipped peccaries and agoutis are attracted by feeding white-faced capuchins, looking for fruit that the capuchins drop.[41] Several species of bird are also known to follow Panmanian white-faced capuchins looking for food. These include the double-toothed kite, the white hawk and the sharp-shinned hawk.[41]

White-faced capuchin eating a wild banana along the Frío River, Costa Rica

Foraging in the trees

The Panamanian white-faced capuchin is an omnivore. Its primary foods are fruit and insects.[8] It forages at all levels of the forest, including the ground.[41] Methods for finding food include stripping bark off of trees, searching through leaf litter, breaking dead tree branches, rolling over rocks, and using stones as anvils to crack hard fruits.[48] Its prehensile tail assists with feeding, helping support the monkey when foraging for food below the branches.[41]

Fruit can make up between 50% and 67% or more of the capuchin's diet.[8] In one study in Panama, white-faced capuchins ate 95 different fruit species.[8] Among its favorite fruits are figs from the family Moraceae, mangos and related fruits from the family Anacardiaceae, the bean-like fruits from the family Leguminosae and fruits from the family Rubiaceae.[49] It will also eat fruits from Euphorbiaceae such as Mexican jumping bean Sebastiania pavoniana.[50] It generally only eats ripe fruit, testing for ripeness by smelling, tasting and prodding the fruit.[8] It typically eats only the pulp and juice, spitting out the seeds and fibers.[8] Other plant matter eaten includes flowers, young leaves, seeds of certain plants, and bromeliads.[8][51] It also uses the bromelids as a water source, drinking the water that gets trapped inside.[8] In Carara National Park the capuchins have a varied diet in addition to the above of banana fruits and flowers, heliconia seeds, huevos de caballo fruits and anacardiaceae stems.[52]

Insect prey eaten includes beetle larvae, butterfly and moth caterpillars, ants, wasps, and ant and wasp larvae.[8] It also eats larger prey, such as birds, bird eggs, frogs, lizards, crabs, mollusks and small mammals.[8][53] The population in Guanacaste, Costa Rica in particular is noted for hunting squirrels, magpies, white-crowned parrots[8] and baby coatis.[54] The amount of vertebrate prey eaten varies by troop.[8] Even neighboring troops can show significant differences in their diets.[48]

The diet can vary between the rainy and dry season. For example, in Guanacaste, Costa Rica the Panamanian white-faced capuchin can eat a wide variety of fruits as well as caterpillars in the early rainy season (June to November).[49] But during the dry season, only figs and a few other types of fruit are available.[49] During the dry season, chitinous insects, ant and wasp larvae and vertebrates become a particularly important part of the Panamanian white-faced capuchin's diet.[49] Access to water can also become an issue during the dry season. The Panamanian white-faced capuchin likes to drink daily, so in forests where water holes dry up during the dry season, there can be competition between troops over access to the remaining water holes.[49]

Capuchins are considered among the most intelligent of the New World monkeys; they have been the subject of many studies on behaviour and intelligence. The capuchins' intelligence is thought to be an adaptation to support their feeding habits; they rely on ephemeral food sources which may be hard to find. In one particular study conducted in 2007, capuchins were found to be among the ten most intelligent primates, second to spider monkeys among New World monkeys.[55]

The use of stone tools is a marked difference between the gracile capuchins of the genus Cebus and the robust capuchins of the genus Sapajus. Although widespread in robust capuchins, only one case of habitual stone tool use has been reported by gracile capuchins. One population of Panamanian white-faced capuchins found in Coiba National Park in Panama has been observed using hammerstones and anvils to process fruits from Terminalia catappa, Bactris major, and Cocos nucifera (coconuts) and invertebrates such as nerite snails, hermit crabs, and Halloween crabs.[56][57]

The Panamanian white-faced capuchin is known to rub parts of certain plants into their hair. Plants used in this manner include citrus fruits, vines of the genera Piper and Clematis, monkey comb (genus Sloanea), dumb cane and custard apple.[8][53] Ants and millipedes are also used in this way.[8] It is not definitively known what this rubbing is for, but this may deter parasites such as ticks and insects, or it may serve as a fungicide or bactericide or anti-inflammatory agent.[8] Alternatively, it may be a form of scent marking.[8] The Panamanian white-faced capuchin also uses tools in other ways. It has been known to beat snakes with sticks in order to protect itself or to get the snake to release an infant,[8] and it sometimes uses sticks as probes to explore openings.[58] In captivity, it has been known to use tools to get to food or to defend itself, and in one case a white-faced capuchin used a squirrel monkey as a projectile, hurling it at a human observer.[8]

The Panamanian white-faced capuchin's intelligence and ability to use tools allows them to be trained to assist paraplegics.[59] Other species of capuchin monkeys are also trained in this manner.[60] Panamanian white-faced capuchins can also be trained for roles on television and movies, such as Marcel on the television series Friends.[61] They were also traditionally used as organ grinder monkeys.[62]

Facial expression

The Panamanian white-faced capuchin is noisy.[9] Loud calls, such as barks and coughs, are used to communicate threat warnings, and softer calls, such as squeals, are used in intimate discourse.[8] Different types of threats, such as a threat from a terrestrial animal versus a threat from a bird, invoke different vocalizations.[41] Facial expressions and scent are also important to communication.[63] It sometimes engages in a practice known as "urine washing", in which the monkey rubs urine on its feet.[64] The exact purpose of this practice is unknown, but it may be a form of olfactory signal.[63]