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.     

Vocal Communication in a Fission-Fusion Society: Do Spider Monkeys Stay in Touch With Close Associates?

In fission-fusion societies, in which animals from the same group may spend long periods of time apart from each other, individuals could use long-distance vocalizations to maintain contact with others. This could be achieved with vocalizations that simply carried information about the caller's identity and location. I explored this possibility using observations and experiments from a 3-year field study of spider monkeys (Ateles geoffroyi) in Punta Laguna, México, analyzing the use of the species' most frequent vocalization, the whinny. By following 2 subgroups simultaneously, I found that subgroups that were within the active space of the whinny approached each other more often than subgroups that were farther apart. Individual adults in these subgroups also emitted more whinnies when they were within hearing range of another subgroup than when farther apart. I used a paired playback design to determine whether whinnies could influence the behavior of close associates as opposed to nonassociated individuals. Although nonassociates were as likely as close associates to respond vocally to playbacks of whinnies, only a close associate ever approached the speaker. Collectively, the results suggest that whinnies are used by spider monkeys to achieve flexibility in spacing while maintaining specific social relationships.     

The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae)

A stable social group of 7 semifree-ranging black-and-white ruffed lemurs (Varecia variegata variegata) was studied for 4 months to catalog the behavioral repertoire of this species. Observations focussed on particular aspects of behavior were conducted before and after this 4-month period to supplement information gathered. Behavior in 11 major categories is detailed: postures, terrestrial locomotion, arboreal locomotion, feeding behavior, vocalizations, scent-marking, affinitive social behavior, agonistic social behavior, play behavior, sexual behavior, and parental behavior. Ruffed lemurs frequently used body positions and locomotor patterns unusual among lemurids, including bipedal hanging and long-descent leaps. These behaviors reinforce dental evidence that Varecia are among the most frugivorous of the Malagasy lemurs. Low intragroup cohesion, infrequent social interaction, and antiphonal use of several long-distance vocalizations suggest that ruffed lemurs naturally exhibit fission-fusion sociality. Social structure based on interindividual familiarity probably extends across foraging parties for several of the diurnally active lemurs; however, thus far only Varecia seems likely to exhibit fission-fusion sociality analogous to that seen in spider monkeys and chimpanzees.     

Tool use in wild spider monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)

Tool use has been observed in a variety of primate species, including both New and Old World monkeys. However, such reports mainly address the most prodigious tool users and frequently limit discussions of tool-using behavior to a foraging framework. Here, we present observations of novel and spontaneous tool use in wild black-handed spider monkeys (Ateles geoffroyi), where female spider monkeys used detached sticks in a self-directed manner. We introduce factors to explain Ateles tool-using abilities and limitations, and encourage the synthesis of relevant research in order to gain insight into the cognitive abilities of spider monkeys and the evolution of tool-using behaviors in primates.     

Network analysis as a tool to understand social development in spider monkeys

The emerging field of network science has demonstrated that an individual's connectedness within their social network has cascading effects to other dimensions of life. Like humans, spider monkeys live in societies with high fission–fusion dynamics, and are remarkably social. Social network analysis (SNA) is a powerful tool for quantifying connections that may vary as a function of initiating or receiving social behaviors, which has been described as shifting social roles. In primatology, the SNA literature is dominated by work in catarrhines, and has yet to be applied to the study of development in a platyrrhine model. Here, SNA was utilized in combination with R-Index social role calculation to characterize social interaction patterns in juvenile and adult Colombian spider monkeys (Ateles fusciceps rufiventris). Connections were examined across five behaviors: embrace, face-embrace, grooming, agonism, and tail-wrapping from 186 hr of observation and four network metrics. Mann–Whitney U tests were utilized to determine differences between adult and juvenile social network patterns for each behavior. Face-embrace emerged as the behavior with different network patterns for adults and juveniles for every network metric. With regard to social role, juveniles were receivers, not initiators, for embrace, face-embrace, and grooming (ps < .05). Network and social role differences are discussed in light of social development and aspects of the different behaviors.     

Towing the party line: territoriality, risky boundaries and male group size in spider monkey fission-fusion societies

Spider monkey communities are classic fission-fusion primate societies. I present data suggesting that spider monkeys (Ateles chamek) at Lago Caiman are territorial; adult males traveled further and faster than adult females and subgroup size was significantly higher in boundary areas of the spider monkey territory where intercommunity disputes were observed than in non-boundary areas. I then go on to examine data from 20 Ateles communities distributed across 14 study sites and five species to investigate how a series of demographic, ecological and geographical parameters influence the number of males in a given spider monkey community. Analyses suggest that the number of males is not significantly related to the number of females in a community, the area of the community home range, or the total perimeter length of the community boundary. However, risky boundary perimeter length, or the length of perimeter that directly borders another spider monkey community, explains 88% of observed variations in the number of males in each community. I discuss the results in relation to spider monkey ecology and territoriality, as well as the potential of this relationship for explaining chimpanzee (Pan) behavior given their extremely similar fruit specialist, male philopatry, territoriality and fission-fusion social system.     

Embraces and Grooming in Captive Spider Monkeys

Relatively little information is available regarding the role of social grooming and embraces in spider monkeys that live in fission-fusion societies in which individuals are usually split into subgroups. We investigated whether embraces and grooming have similar roles in captive spider monkeys by examining their occurrence in two contexts. One context was fusion, i.e. when the monkeys moved into an area of the enclosure where other monkeys were present, in which individuals from different subgroups were expected to exchange greeting behavior. The other context was the access to young infants, in which females were expected increase their friendly behavior toward mothers. We collected data by observing all individuals within a subgroup and via focal animal sampling. We found that overall embraces occurred more frequently than grooming and that their distributions were not correlated. The frequency of embraces was positively associated with the number of fusion events per observation, whereas the frequency of grooming bouts was not. Furthermore, embraces were more frequent following initial approaches after fusion versus subsequent approaches, and the figure was higher than the corresponding one for grooming. Mothers received more embraces after than before the birth of their infants, whereas there was no such effect for grooming. Embraces, but not grooming, play a role in the regulation of social relationships in spider monkeys. Embraces may serve as signals of benign disposition in contexts that are likely to be associated with tension, such as fusion and access to infants.     

Communication of food quality in captiveMacaca nemestrina and free-rangingAteles geoffroyi

While observational learning and social communication of feeding behavior have been demonstrated several times for edible foods, to date there has been no experimental evidence for learning to avoid distasteful or inedible foods by social cues in primates. A series of experiments on captive pigtail macaques (Macaca nemestrina) and free-ranging spider monkeys (Ateles geoffroyi) was performed to determine if members of these two species would avoid a food item that was rejected by a conspecific. The results indicated that, while individuals were capable of learning to avoid a distasteful food after personal experience, social cues were not sufficient to prevent other individuals from tasting the rejected foods or for discriminating between neutral and distasteful items. The results are discussed in terms of spacing patterns and visual access in the natural foraging situation.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.     

Raiding parties of male spider monkeys: Insights into human warfare?

Raids into neighboring territories may occur for different reasons, including the increase of foraging and mating opportunities directly or indirectly through the killing of neighboring rivals. Lethal raids have been mainly observed in humans and chimpanzees, with raiding males being reported to search purposefully for neighbors. Here we report on the first cases ever witnessed of raiding parties of male spider monkeys, a species expected to show such a behavioral tendency, given its similarity with humans and chimpanzees in critical socio-ecological characteristics, such as fission-fusion social dynamics and male-male bonding. Despite the high degree of arboreality of spider monkeys, all seven witnessed raids involved the males progressing single file on the ground in unusual silence. This is remarkably similar to the behavior of chimpanzees. The circumstances around the raids suggest that factors such as reduced mating opportunities, number of males relative to that in the neighboring community, and the strength of bonds among males could play a role in the timing of such actions. The raids did not appear to be aimed at finding food, whereas there is some indication that they may directly or indirectly increase reproductive opportunities. Although no killing was observed, we cannot exclude the possibility that spider monkey raids may be aimed at harming rivals if a vulnerable individual were encountered. The similarity of spider monkey raids with those of chimpanzees and humans supports the notion that lethal raiding is a convergent response to similar socio-ecological conditions.     

Interspecific Infanticide and Infant‐Directed Aggression by Spider Monkeys (Ateles hybridus) in a Fragmented Forest in Colombia

Interspecific aggression amongst nonhuman primates is rarely observed and has been mostly related to scenarios of resource competition. Interspecific infanticide is even rarer, and both the ultimate and proximate socio‐ecological factors explaining this behavior are still unclear. We report two cases of interspecific infanticide and five cases of interspecific infant‐directed aggression occurring in a well‐habituated primate community living in a fragmented landscape in Colombia. All cases were initiated by male brown spider monkeys (Ateles hybridus) and were directed toward infants of either red howler monkeys (Alouatta seniculus: n = 6 cases) or white‐fronted capuchins (Cebus albifrons: n = 1 case). One individual, a subadult spider monkey male, was involved in all but one case of interspecific infanticide or aggression. Other adult spider monkeys participated in interspecific aggression that did not escalate into potentially lethal encounters. We suggest that competition for food resources and space in a primate community living in high population densities and restricted to a forest fragment of ca. 65 ha might partly be driving the observed patterns of interspecific aggression. On the other hand, the fact that all but one case of interspecific infanticide and aggression involved the only subadult male spider monkey suggests this behavior might either be pathological or constitute a particular case of redirected aggression. Even if the underlying principles behind interspecific aggression and infanticide are poorly understood, they represent an important factor influencing the demographic trends of the primate community at this study site. Am. J. Primatol. 74:990‐997, 2012. © 2012 Wiley Periodicals, Inc.     

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

Vocal Repertoire of Golden-backed Uakaris (<Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>): Call Structure and Context

The study of vocal behavior can reveal important aspects of how and why a species communicates in relation to ecological and social challenges. We here focus on vocal communication in golden-backed uakaris (Cacajao melanocephalus), diurnal, pitheciine monkeys that exhibit fission-fusion social organization and typically inhabit dense forests that limit the potential for visual communication. Moreover, the species spends little time engaged in tactile or olfactory communication, e.g., social grooming and scent marking, respectively. Hence, vocalizations may be very important for the coordination of social organization in these monkeys. We 1) categorized golden-backed uakari vocalizations, 2) ascertained their behavioral context, and 3) investigated whether golden-backed uakari calls can encode information about the signaler. We observed the monkeys during 2 wet seasons in the flooded igapó forest of Jaú National Park, Brazil. We showed that golden-backed uakaris have 9 call types in their vocal repertoire, all distinguishable by ear and from analysis of spectrograms. Some calls, e.g., play-specific calls, were used only in particular behavioral contexts, and by individuals of specific age, whereas others were emitted under a range of situations. The structure of the loud tchó call varied among individuals, and according to behavioral context, i.e., whether individuals were foraging/feeding, traveling, or performing agonistic interactions. This knowledge of the species’ vocal repertoire is valuable for surveying the monkeys acoustically in habitats where visual surveys are difficult.     

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.     

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.     

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.     

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Proboscis monkey (Nasalis larvatus) social organization: Intergroup patterns of association

Proboscis monkey (Nasalis larvatus) social organization was studied at the Natai Lengkuas station, Tanjung Puting National Park in Kalimantan Tengah, Indonesia. Data were collected on ten one-male groups and two all-male groups using scan sampling and event sampling during follows, and through evening census surveys. Proboscis monkeys were found to form stable one-male groups. Specific groups associated at their sleeping sites, in a manner similar to the fission-fusion pattern described for hamadryas and gelada baboons. Analyses performed on these associations indicated that the groups formed two separate bands. These separate bands appear to be a secondary level of organization, distinct from the primary level of organization, the one-male and all-male groups. This is the first evidence for such a two-tiered system of organization in an arboreal colobine species. Proboscis monkeys closely resemble gelada baboons in their organizational pattern. In both species, adult females direct the majority of their affiliative behavior towards their offspring and other adult females, males do not engage in active herding, all-male groups are present, and one-male groups do spend time apart from other groups. Home ranges of both groups and of bands of proboscis monkeys overlapped extensively; temporal avoidance between bands may have been mediated by early morning vocalizations and branch shaking displays.