Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia

In this study, I revise three aspects of the socioecology of woolly monkeys (genus Lagothrix) that might give us a better understanding of the patterns found in this species: (1) the association between temporal variation in fruit abundance and diet, activity, and ranging patterns; (2) the individual trade-offs associated with living in small or large groups, and (3) the relationship between social dominance and foraging success. Using behavioral and ecological data collected during 3 years in Tinigua Park, Colombia, I found that woolly monkeys tend to avoid open-degraded forests, where fruit production is generally lower than it is in mature forests. Diet and activity budgets were highly associated with temporal patterns of fruit production. Daily path length was positively correlated with group size and monthly fruit abundance, and negatively correlated with habitat quality. I found differences in activity budgets and the diet preferences of different age/sex classes. For example, adult males rest more and juveniles play more than other classes. Juveniles and adult females without infants look for arthropods more often than adult males and females with young infants, who showed the highest frequencies of fruit feeding. Dominant adult males were not consistently the most efficient foragers on fruits according to two different indexes. Most of these results are consistent with the expectations from strong intra-group competition for resources. However, females with infants received benefits during feeding similar to those of dominant adult males, which may be mediated by differential aggression from males to other group members (juveniles and females without infants).     

Social Behavior,Reproductive Strategies,and Population Genetic Structure of <Emphasis Type="Italic">Lagothrix poeppigii</Emphasis>

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon. Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.     

Male and female range use in a group of white‐bellied spider monkeys (Ateles belzebuth) in Yasuní National Park,Ecuador

Spider monkeys (Ateles sp.) live in a flexible fission–fusion social system in which members of a social group are not in constant association, but instead form smaller subgroups of varying size and composition. Patterns of range use in spider monkeys have been described as sex‐segregated, with males and females often ranging separately, females utilizing core areas that encompass only a fraction of the entire community range, and males using much larger portions of the community range that overlap considerably with the core areas of females and other males. Males are also reported to use the boundary areas of community home ranges more often than females. Spider monkeys thus seem to parallel the “male‐bonded” patterns of ranging and association found among some groups of chimpanzees. Over several years of research on one group of spider monkeys (Ateles belzebuth) in Yasuní National Park, Ecuador, we characterized the ranging patterns of adult males and females and evaluated the extent to which they conform to previously reported patterns. In contrast to ranging patterns seen at several other spider monkey sites, the ranges of our study females overlapped considerably, with little evidence of exclusive use of particular areas by individual monkeys. Average male and female home range size was comparable, and males and females were similar in their use of boundary areas. These ranging patterns are similar to those of “bisexually bonded” groups of chimpanzees in West Africa. We suggest that the less sex‐segregated ranging patterns seen in this particular group of spider monkeys may be owing to a history of human disturbance in the area and to lower genetic relatedness between males, highlighting the potential for flexibility some aspects of the spider monkeys' fission–fusion social system. Am. J. Primatol. 72:129–141, 2010. © 2009 Wiley‐Liss, Inc.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus)

We examined adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus), a species in which close relatedness among philopatric males and high paternity uncertainty should minimize both aggressive and affiliative behavior by males toward infants. As expected, male-infant interactions were extremely rare during this 10-month field study. None were observed in over 236 hr of observation on a cohort of six infants (0 – 13 months old). The 29 interactions observed ad lib involved 5 of the 6 infants and 9 of the 16 adult males in the group. All of the male-infant interactions were affiliative, but extremely brief. The median duration of interactions was only 0.33 min, and none lasted longer than 1.52 min. Infants always initiated, and nearly always terminated, their interactions with adult males. The indifference that appears to characterize muriqui male-infant interactions differs from the ways in which other male primates interact with infants when protection of genetic interests or investment in mating effort are involved.     

Adoption in Anthropoid primates

Reports of adoption in nonhuman primates are reviewed, including spontaneous adoptions of orphans or infants whose mothers have been removed from the group, temporary adoptions of offspring of sick mothers, adoptions arising out of kidnapping, and adoptions resulting from manipulations involving presenting infants to adults. Adoptive behavioral patterns resemble nonadoptive alloparental patterns. The literature indicates certain trends: adult females, especially if lactating or in the late stages of pregnancy, are most likely to adopt neonates. Older infants are more likely to be adopted by juveniles or by adult males. Weaned or weanable orphans that get adopted have reasonable chances of survival, while orphans still reliant on milk are unlikely to survive. An infant adopted by an adult female will develop socially as a member of the female’s matriline. Adoptions involving closely related individuals are consistent with kin-selection theory. Others appear to reflect “reproductive error” arising out of an attraction to young infants. Yet other cases might reflect reciprocal altruism. Continued documentation of cases of adoption will yield more data on costs and benefits and on whether rates and forms of adoption, such as alloparental behavior, vary systematically with social systems.     

Mother-infant relationships in Vervet Monkeys: Response to new adult males

The reaction of mothers to replacement of breeding adult males was studied in two captive groups of vervet monkeys. Mother-infant behavior for 15 infants born in the season following the introduction of new males was compared to mother-infant behavior for 35 infants born with adult males that had been resident in the group for more than a year. The mothers responded to the presence of new males by being more protective toward their infants in the first 3 months. Increased protectiveness disappeared in the second 3 months, and in the infant’s sixth month of life mothers with new males in the group became more rejecting than mothers with long-term resident males. The combination of increased protectiveness and increased rejection was unusual among the mothers with long-term resident males but was the most common mothering style used in the presence of new males. The rate of rejection was inversely correlated with the interbirth interval, and mothers with new males in the group conceived sooner and had significantly shorter inter-birth intervals compared to mothers with long-term resident males.     

Affiliative relationships between adult males and immature group members in naturally occurring ringtailed lemurs (Lemur catta)

Affiliative relations between adult males and immature group members were studied in three naturally occurring groups of ringtailed lemurs (Lemur catta) over a 12-month period at Beza-Mahafaly Reserve, southwestern Madagascar. No statistically significant difference was found in rates of affiliative interactions between adult males and older immatures (juveniles and adolescents) over reproductive seasons. However, some of the adult males in two focal groups increased their rates of affiliative behaviors with older immatures during the lactation and subsequent 1993 postmigration periods. Female involvement with infants during lactation season, the increasing independence of juveniles and adolescents, and length of male tenure may be factors contributing to such a pattern. Neither adult males nor immatures were significantly responsible for the initiation and maintenance of proximity in male-immature dyadic interactions. Neither dominance rank nor age-class of the adult male affected their rates of affiliative behavior with immatures. The majority of focal males exhibited an interest in infants and occasionally participated in alloparental care. It is suggested that adult males can benefit from affiliative relations with immatures in terms of opportunities for greater spatial centrality in the group, which can lead to enhanced predator protection and greater opportunities to develop affiliative relationships with females. Immatures can benefit from affiliation with males in relation to enhanced predator detection and protection, alloparental care, and opportunities to develop social skills. Am J Phys Anthropol 103:163–171, 1997. © 1997 Wiley-Liss, Inc.     

The Social Behavior of Brown Spider Monkeys (Ateles hybridus) in a Fragmented Forest in Colombia

Forest fragmentation and habitat loss are two of the main drivers of wildlife population declines. Animals exposed to habitat disturbances must develop behavioral strategies to adapt to novel, rapidly fluctuating socioecological challenges. Understanding the behavioral flexibility of endangered primates as a response to ecological challenges, e.g., anthropogenic habitat disturbance, is a key element in the design of successful conservation initiatives for remaining populations. We studied the social behavior of a group of 11 adult and subadult brown spider monkeys (Ateles hybridus) living in a recently isolated and densely populated forest fragment in the Magdalena River Valley, Colombia, and compared their behavior to that of other wild spider monkey populations. From June 2009 to July 2010 we assessed diet, activity budgets, and the rates of affiliative and agonistic interactions initiated and received by adult male and female spider monkeys. The diet of our focal group was quite different from that in most previous studies of Ateles: leaves accounted for ca. 40?% of their diet, and fruits represented barely half of their diet, suggesting that this population has had to adjust its feeding strategies to the local ecological challenges. We found no sex differences in the time males and females spent resting, moving, and socializing, but females tended to invest more time in feeding than males did. Male-to-female aggression was the most common agonistic interaction, and same-sex aggressions were almost absent. We found no significant differences in rates of grooming or embracing between the different types of dyads. The resemblance of our results to those of similar studies in less disturbed habitats suggests that spider monkeys might adapt to certain levels of ecological and social disturbance, at least initially, and are a starting point to understand better the initial effects of fragmentation on the behavioral repertoire of these primates.     

Allomaternal behavior in a group of free-ranging patas monkeys

A free-ranging group of patas monkeys (Erythrocebus patas) containing 18 individually identifiable adult females was observed for approximately 400 hours, equally distributed over two two-month periods corresponding to the breeding and birth seasons, at the La Parguera facility of the Caribbean Primate Research Center. The large number of infants born in the spring and early summer (n = 14) allowed for detailed observations of alloparental behaviors, with a focus on allomothering by the adult females. Seven types of alloparental behaviors were recorded: contact, nuzzling, grooming, agonism, close visual inspection, attempted kidnapping, and kidnapping. Adult females emitted the vast majority of allomaternal behavior, the patterning and frequency of which closely resembled the patterning and frequency of inter-adult female social grooming. Relative dominance status of the participants did not consistently predict the directionality of allomothering. The most commonly observed allomaternal behaviors were contact and nuzzling, which are primarily affiliative behaviors; agonism was rare. Successful kidnapping occurred eight times. Immature monkeys (n = 22) emitted an additional 32 alloparental acts. A propensity towards allomothering by experienced females would be most beneficial to patas infants due to the patas' tendency towards dispersed foraging and rapid flight in the presence of danger. It is possible that direct competition with groups of rhesus macaques for available resources on the island served as a proximal cause for the allomothering observed in this patas group.     

Costs of twins in free-ranging white-bellied spider monkeys (Ateles belzebuth belzebuth) at Tinigua National Park, Colombia

A female spider monkey (Ateles belzebuth belzebuth) that gave birth to twins was studied during 13 months, and her activity budget and diet were compared to those of females with single offspring and females with no offspring to assess selective pressures that could influence litter size. We recorded qualitative information on the development and social interactions of the twins and three other single infants. Emi, the female that had the twins, had the highest proportion of resting time and the lowest proportion of feeding and moving time compared to other adult females and males. Emi also had the lowest average daily travel distance and relied more heavily on flowers and leaves than other group members who included a higher proportion of fruits in their diets. These results suggest that twins are energetically costly to spider monkeys because of the direct energy allocated into raising and carrying the twins and, also, because these costs have direct effects in the ability of a mother to obtain high-quality resources (e.g., fruits). The twins had a slower rate of physical and social development as well as a smaller body size compared to same-aged singletons by the end of the study. Thus, the extended periods of maternal care and the costs associated with rearing and carrying offspring are some of the factors that influence the evolution and maintenance of a litter size of one in most anthropoid primates.     

Patterns of injury in zoo-housed spider monkeys: A problem with males?

Aggression among wild spider monkeys is most frequently reported to occur between the sexes, with adult males directing aggression towards adult females and the aggression is normally non-injurious. After two severe instances of aggression in the group of spider monkeys housed at Chester Zoo, we developed a questionnaire to investigate the frequency, direction and possible reasons for aggression in zoo-housed spider monkeys. We sent our questionnaire to 55 zoos worldwide and obtained records from 26 groups, which yielded detailed accounts of 143 aggressive incidents: 56 events for the actors and 127 events for the targets of aggression. We found that zoo-housed spider monkeys are predominantly maintained in small social groups, with a single adult male, two adult females and their offspring. Of the aggression reported, 23.1% of incidents resulted in severe or lethal injuries. Adult males were the most frequent actors of aggression and accounted for 66.7% of incidents. Six cases of male–male aggression were lethal. The most striking pattern was that adult males directed aggression towards non-adult males more than any other age/sex category. The most frequently reported context of aggression was tension between adult and non-adult males. These findings contradict previous reports from wild spider monkeys where female-directed male aggression is most frequently reported. In light of our findings, we recommend that males form the core of the group and that females be relocated among groups to reflect the wild condition of male philopatry and female dispersal. In addition, enclosure design should allow opportunities for the monkeys to segregate themselves from other group members, simulating fission, which is a conflict management strategy for avoiding aggression in wild spider monkeys.     

Demography,ranging patterns,and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park,Peru

Results of a long-term field study on the ecology and social organization of two groups of black spider monkeys (Ateles paniscus chamek) in Peru are reported. Demography, ranging patterns, and activity budgets provide insight into some of the proximate determinants of fission-fusion social organization in this species and illustrate the different strategies used by males and females to gain access to critical resources. Longitudinal data on known individuals provide evidence for male natal philopatry and female emigration at sexual maturity in this population. Interbirth intervals are long (mean = 34.5 months) in comparison with most other primate species, and 5 of 15 infants seen within a few days of birth died or disappeared before they were a year old. Home ranges are large (150–250 ha) and fairly discrete; overlap with neighboring groups is on the order of 10–15%. Males and females differed substantially in their ranging patterns; females, particularly those with infants, restricted much of their ranging to a “core area” 20–33% the size of the total group range, whereas males ranged more evenly over the entire area occupied by the group. Daily path length varied over almost an order of magnitude from 465 m to 4,070 m, with a mean of 1977 m. Males spent more time traveling and less time feeding than most females. These results are compared with those obtained in previous studies of Ateles and with similar data from other primate species to assess their implications for the evolution of fission-fusion sociality in spider monkeys. The ecological factors responsible for the evolution of very similar social organizations in spider monkeys and chimpanzees are discussed.     

Female-female social relationships in wild white-faced capuchin monkeys,Cebus capucinus

A single social group of wild white-faced capuchin monkeys was studied for a period of 26 months at Lomas Barbudal Biological Reserve, Costa Rica. A total of 604 hr of focal animal data was collected on six adult females in a group of 21 monkeys. Females could be ranked in a stable, linear dominance hierarchy. Adult females spent much more time in proximity to other adult females than to adult males. Females groomed other females twice as often as they groomed males, and about 55 times more often than males groomed males. Females tended to groom up the dominance hierarchy, and dyads with smaller rank distances groomed more often. Higher-ranking females nursed infants other than their own at lower rates than did lower-ranking females; however, females nursed infants of females ranked both above and below them. Although lower-ranking females were more likely than higher-ranking females to be the victims of aggression, higher-ranking females were not necessarily more aggressive than lower-ranking females. In 96% of female-female coalitions vs. a female, the victim was lower-ranking than both coalition partners; in the remaining 4%, the victim was intermediate in rank between the two coalition partners. Higher-ranking female-female dyads formed coalitions more often than did lower-ranking dyads. Those female-female dyads that groomed more frequently also formed coalitions more frequently. The patterning of social interactions indicates that Cebus capucinus at Lomas Barbudal are female bonded. © 1996 Wiley-Liss, Inc.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Habitat,diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806)

Results of a 10-month study of the ecology and behavior of free- ranging woolly spider monkeys (Brachyteles arachnoides)in Brazil show that these animals are strongly folivorous. Leaf-eating accounted for more than 50% of the total feeding time in all samples but one and accounted for more than 80% of the total feeding time in three samples. Mature foliage was routinely eaten. Woolly spider monkeys consistently spend more than 50% of each day quietly resting and sleeping. Animals travel little except when actively feeding and show low levels of social interaction. Such an activity profile suggests that woolly spider monkeys may often be living near the limits of their energetic resources. The social organization of the species is unusual for a folivorous primate in that small groups of females and associated immature animals confine their activities to discrete home-range areas, whereas males are itinerant, traveling over the home ranges of various female groups. Animals sharing a common home-range area show no permanent daily pattern of association other than that of mother-dependent offspring. Foraging alone or with few conspecifics should maximize each individual’s returns from foraging by minimizing the day range that must be traveled each day to locate foods while simultaneously lowering interference competition for higher-quality dietary resources.     

Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi)

Several aspects of the social system of spider monkeys remain poorly understood in spite of previous studies of their behavior. Our work investigates sex differences of adultAteles geoffroyi to develop a better understanding of their social organization. A six-month field study of this species in Guatemala showed that adult males were both more aggressive and more socially cohesive than females, as well as more territorial. Adult females were more vocal, more submissive, more nonsocial, and more dispersed than adult males. Males were more likely to associate affinitively with other males than with females, and to direct their aggressive behaviors at females rather than males. Spider monkey society was found to be sex-segregated; males traveling and interacting in all-male subgroups, while females travel alone or with offspring. These findings are used, in conjunction with other evidence, to draw inferences about the dynamics of theAteles social system, and to derive an explanation for the evolution of spider monkey social organization. The frugivorous diet ofAteles is linked to the dispersion females and to the cohesion of related adult males, who form cooperative territorial groups, in which the low level of male-male competition is related to the absence of sexual dimorphism. Spider monkeys provide an illuminating contrast to the general primate model, derived from Old World monkeys, which links sexual dimorphism in size to sex differences in behavior, and ultimately to sexual selection.     

Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus)

Primate vocalizations that appear to occur independently of specific contexts typically are considered to be contact calls. However, results from several recent studies indicate that these calls function to facilitate social interactions. White-faced capuchin monkeys (Cebus capucinus) emit a high-frequency vocalization, termed a "trill," in social interactions and during travel. In this study, immatures emitted most trills, but adult females also trilled; by contrast, adult males rarely trilled. Infants emitted the majority of trills, and they trilled at significantly higher rates than adult females. Infants trilled most when approaching other individuals. Furthermore, infants emitted proportionately more trills than other age classes when approaching other individuals. I therefore focused on the detailed context and immediate behavioral correlates of trilling by infants. Infants that trilled when approaching others tended to interact affiliatively with them subsequently (i.e., climbing on, touching, receiving grooming, and performing food inspection) more than infants that did not trill when approaching. Therefore, infant trilling may have had an immediate effect on the recipient's behavior.