Sexual Differences in Ranging of <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis> at La Macarena,Colombia

I examined sex differences in the ranging patterns of 3 female and 3 male wild spider monkeys. Each of the focal males used the home range widely, whereas each of the focal females used a distinct, restricted area of the home range. The males traveled longer distances than the females did. Although males were consistently in larger parties than females were, travel speed was affected by party composition rather than party size. All-male parties traveled faster than other party types did. Foraging manner also differed between sexes. Males spent more time feeding on fruits and less time on flowers and traveled longer distances between feeding trees. Both males and females used salados, where they ate soil and drank water. Salado location is likely to have affected the ranging pattern. Males used boundary areas more frequently than females did, often traveling along the boundary area in alliance with other males. Males also used areas that had been part of neighboring groups home ranges and were not used at all by females of the group. Greater travel distance of males is likely to be facilitated by consumption of a higher caloric diet. I compare the social structure of spider monkeys with that of chimpanzees, whose society is characterized by male-philopatry and female dispersion.     

Male philopatry in spider monkeys revisited

Dispersal patterns are critical for understanding social systems as they influence social interactions and relationships. Spider monkeys (Ateles spp.) are typically described as being characterized by male philopatry and female dispersal, with these patterns reflected in stronger affiliative and cooperative relationships among males than among females. Recent findings, however, indicate that male–male relationships may not be as uniformly strong as previously thought, which suggests that male philopatry in spider monkeys may not be universal. Here, we report the first confirmed cases of male immigration and group takeover in spider monkeys. Data were collected on one community of Ateles geoffroyi in northwestern Costa Rica. Behavioral and demographic data were recorded during subgroup follows across 6.5 years, and fecal samples of community members were collected for genetic analysis of relatedness. We documented two separate cases of immigration involving multiple males, which resulted in take‐over of the study community by extra‐community males and the concomitant disappearance of the resident males. In the study community, males were no more closely related to one another, on average, than females were, contrary to what would be expected if males were the more philopatric sex. Comparison of corrected assignment indices for males and females also revealed no evidence of sex‐biased dispersal. Our findings suggest that in spider monkeys male immigration may occur under certain demographic circumstances, contributing to a view of greater flexibility in their social system than previously appreciated. This discovery has implications for other species that are typically characterized by male philopatry. Am J Phys Anthropol 152:86–95, 2013. © 2013 Wiley Periodicals, Inc.     

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.     

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.     

Range use of the forest chimpanzees of Kibale: Implications for the understanding of chimpanzee social organization

We contrast the range use patterns of male and female chimpanzees (Pan troglodytes) based on repeated sightings over three years of 19 individuals in the Kanyawara community of Kibale Forest Reserve, Uganda. Depending on how home range size was calculated, male chimpanzees used an area that was 1.5 to 2 times greater than that of females. There was no difference between the sexes in whether their home ranges were used in a clumped or uniform fashion. However, males were more likely to be seen in boundary areas than females. These results are discussed in light of previously proposed models of chimpanzee social organization. It is concluded that the scenario in which females have smaller core areas within the defended home range of the males is most strongly supported by the range use patterns observed in Kibale chimpanzees. © 1993 Wiley-Liss, Inc.     

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.     

Assessing the Occurrence of Sexual Segregation in Spider Monkeys (Ateles geoffroyi yucatanensis), Its Mechanisms and Function

Sexual segregation is a recognized dimension of the socioecology of many vertebrates, but it has not been systematically examined in primates. We investigated temporal patterns of sexual segregation in spider monkeys (Ateles geoffroyi yucatanensis) using a test that distinguishes sexual segregation from aggregation and random association between the sexes. We further investigated how sexual segregation varies over time as a function of food availability, and then tested other possible factors that might be causally linked to sexual segregation in spider monkeys. We predicted that male philopatry and cooperative territorial defence leads to sexual dimorphism in behavior, which in turn creates different optimal energetic requirements for males and females as reflected in differing activity budgets and diet. We investigated sexual segregation in a group of 33–35 spider monkeys at Runaway Creek Nature Reserve in Belize over 23 mo in 2008–2009. We used the sex compositions of subgroups recorded in scan samples to test the occurrence of sexual segregation at monthly and biweekly time scales.We found that males and females were significantly segregated in 15 out of the 23 mo of the study, and that periods of nonsegregation coincided with months of low food availability. The sexes differed significantly in activity and diet; males spent more time traveling, and less time resting and feeding than females, and they had a higher proportion of ripe fruits in their diets than did females. We propose that sexual segregation in spider monkeys is primarily a form of social segregation that results from males and females pursuing optimal dietary and behavioral strategies to satisfy sex-specific energetic demands. We further suggest that sexual segregation represents an important constraint on fission–fusion dynamics that should be considered when assessing the potential for variability in subgroup composition.     

Spider monkey home ranges: A comparison of radio telemetry and direct observation

The ranging patterns of two male and five female spider monkeys (Ateles geoffroyi) were studied with the use of radio telemetry in Santa Rosa National Park, Costa Rica. The average size of a spider monkey home range was 62.4 hectares; however, range size varied with sex, and, for females, with the presence of a dependent infant. The probability of encountering a radio-collared spider monkey in a three-hour search using radio telemetry (0.91) was much greater than using a visual search (0.20), and telemetric data resulted in a larger estimate of mean home range size than did observational data, when all subjects were compared. However, the difference appeared to be owing to the presence of male ranges in the telemetric, but not the observational, data. When the size of home ranges derived from radio-tracking data for adult females was compared to size of ranges for adult females derived from observations, the results were not significantly different. Adult males had larger home ranges than adult females, thus lending support to the hypothesis that males have adapted to the dispersion of females by occupying a large home range that overlaps the ranges of several adult females. The smallest home ranges were occupied by low-weight females with dependent infants, perhaps reflecting social and energetic constraints.     

Fission-fusion social organization inAteles andPan

Recent research on the ecology and behavior of free-ranging spider monkeys (Ateles paniscus chamek) allows a more detailed comparison with the chimpanzee,Pan troglodytes, than has been possible previously. Despite their distant common ancestry, chimpanzees and spider monkeys share an unusual fission-fusion social system. In this paper, I compare subgroup size and composition, social unit structure, ranging behavior, patterns of philopatry and dispersal, and social relationships in the two taxa. It is proposed that spatial and temporal patchiness in food dispersion and abundance, resulting in a high-level of feeding competition between females within a group, has been the most important ecological selection pressure leading to the evolution of fission-fusion social organization in both species.     

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.     

How feeding competition determines female chimpanzee gregariousness and ranging in the Taï National Park, Côte d'Ivoire

Socioecological theory suggests that feeding competition shapes female social relationships. Chimpanzees (Pan troglodytes) live in fission–fusion societies that allow them to react flexibly to increased feeding competition by forming smaller foraging parties when food is scarce. In chimpanzees at Gombe and Kibale, female dominance rank can crucially influence feeding competition and reproductive success as high‐ranking females monopolize core areas of relatively high quality, are more gregarious, and have higher body mass and reproductive success than low‐ranking females. Chimpanzee females in Taï National Park do not monopolize core areas; they use the entire territory as do the males of their community and are highly gregarious. Although female chimpanzees in Taï generally exhibit a linear dominance hierarchy benefits of high rank are currently not well understood. We used a multivariate analysis of long‐term data from two Taï chimpanzee communities to test whether high‐ranking females (1) increase gregariousness and (2) minimize their travel costs. We found that high‐ranking females were more gregarious than low‐rankers only when food was scarce. During periods of food scarcity, high rank allowed females to enjoy benefits of gregariousness, while low‐ranking females strongly decreased their gregariousness. High‐ranking females traveled more than low‐ranking females, suggesting that low‐rankers might follow a strategy to minimize energy expenditure. Our results suggest that, in contrast to other chimpanzee populations and depending on the prevailing ecological conditions, female chimpanzees at Taï respond differently to varying levels of feeding competition. Care needs to be taken before generalizing results found in any one chimpanzee population to the species level. Am. J. Primatol. 73:305–313, 2011. © 2010 Wiley‐Liss, Inc.     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km²). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.     

Geophagy in brown spider monkeys (Ateles hybridus) in a lowland tropical rainforest in Colombia

Spider monkeys and howler monkeys are the only Neotropical primates that eat soil from mineral licks. Not all species within these genera visit mineral licks, and geophagy has been restricted to populations of Ateles belzebuth belzebuth,Ateles belzebuth chamek and Alouatta seniculus in western Amazonian rainforests. With the aid of a camera trap we studied the visitation patterns of a group of brown spider monkeys (Ateles hybridus) to a mineral lick at Serrania de Las Quinchas, in Colombia. Spider monkeys visited the lick frequently throughout the year, with a monthly average of 21.7 ± 7.2 visits per 100 days of camera trapping (n = 14 months). Spider monkeys visited the mineral lick almost always on days with no rain, or very little (<3 mm) rain, suggesting that proximate environmental variables might determine spider monkeys' decisions to come to the ground at the licks. This study expands the geographical occurrence of mineral lick use by spider monkeys providing additional data for future assessments on the biogeographical correlates of mineral lick use by platyrrhines.     

Female competition and male territorial behaviour influence female chimpanzees' ranging patterns

Current models of chimpanzee social structure differ in the extent to which females range with the males and are loyal to a particular social group. We tested these models by analysing 18 years of observational data on the Gombe chimpanzees to investigate the relationship between female space use patterns and both female feeding competition and changes in the male-defended range boundaries. Females at Gombe typically spend most of their time in small overlapping core areas within the community range. Most core areas clustered into two neighbourhoods, north and south. Most females maintained a high degree of site fidelity, but altered their space use patterns to stay within a male-defended boundary. This overall pattern supports the male-bonded model of the chimpanzee social system, over the bisexual or male-only community models, but there are many exceptions. Some females were very peripheral and may have associated simultaneously with two communities. Others switched communities as adults. Thus, different individual females displayed a variety of space use patterns. Different space use patterns of individual females were associated with differences in reproductive success. Members of the northern neighbourhood had higher reproductive success than those of the south, and peripheral individuals either did very well or very poorly. Females that moved from one community to another as adults produced the fewest surviving offspring. These results suggest that female ranging patterns are influenced by both feeding competition and male territorial behaviour.     

Group Release of Sanctuary Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) in the Haut Niger National Park,Guinea, West Africa: Ranging Patterns and Lessons So Far

The release of wild or captive-bred mammals within their historical ranges typically aims to reestablish populations in areas where they have become extinct or extirpated, to reinforce natural populations, or to resolve human–wildlife conflicts. Such programs, which also typically in parallel help foster the protection of the release site, concern a wide range of endangered mammalian species, including our closest living relatives: chimpanzees. In June 2008, the Chimpanzee Conservation Center (CCC), which is located in the High Niger National Park (HNNP) in Guinea, released a group of 12 chimpanzees (Pan troglodytes verus) comprised of 6 females and 6 males (8–20 yr old). The selected release site lies 32 km from the sanctuary in the Mafou, a core area of HNNP where wild chimpanzees are also known to occur. The purpose of this release was therefore to reinforce the natural chimpanzee population within the Mafou core area and to promote the protection of the HNNP. Nearly 2 yr postrelease, 9 chimpanzees still remain free-living. Two thirds of the release chimpanzees were equipped with VHF-GPS store-on-board tracking collars. We used data from retrieved collars to explore the release chimpanzees’ habitat use, individual day range, and core area use (50% and 80%) during the first year of the release. Males traveled significantly further than females. Although minimum day range did not differ between the sexes or vary seasonally, some release males were active for longer during the day than the females. Males also ranged over larger areas and used a wider network of core areas than the females. Habitat use was similar to that recorded in wild chimpanzees in the HNNP. As of September 2010, 2 males and 3 females form a group at the release site. Two of these females gave birth to healthy offspring respectively 16 and 20 mo postrelease. Another female successfully immigrated into a wild chimpanzee community. We suggest that the success of this chimpanzee release can be attributed to the CCC’s lengthy rehabilitation process and the savanna-mosaic habitat of the HNNP. This release demonstrates that under special socioecological circumstances, the release of wild-born adult chimpanzees of both sexes is a viable strategy, which can also function as an effective conservation tool.     

Surviving at the extreme: Chimpanzee ranging is not restricted in a deforested human‐dominated landscape in Uganda

Endangered wildlife increasingly inhabits human‐dominated landscapes outside protected areas. Large‐bodied mammals require large spaces, and their ranging may be especially impacted by landscape modifications including farming, road development and urbanisation. We studied the Wagaisa community of chimpanzees (Pan troglodytes) in Uganda, which inhabit a landscape characterised by high human population density, widespread deforestation, and rapid agricultural and infrastructural development. We aimed to assess whether this dynamic, fragmented environment constrains the chimpanzees’ ranging, and to identify critical habitat patches to aid their conservation. During March–May 2018, we assessed range use from locations of direct observations and indirect signs, corroborated by longer‐term behavioural monitoring of the chimpanzees (June 2018–December 2019). No evidence of limited ranging was found. The Wagaisa chimpanzees used an area measuring ≥ 43 km² (100% MCP) and ranged extensively in the anthropogenic matrix. Most frequently used parts of the range (‘core habitat areas’) centred around small (5–20 acres), widely dispersed remnant forest patches and exotic eucalyptus plantations. Forty per cent of chimpanzee nests were constructed in eucalyptus trees, suggesting a behavioural adjustment to landscape changes. Actions to facilitate conservation of these ‘village chimpanzees’ and others surviving in transformed human‐dominated habitat need not conflict with the sustainable development of the region.     

Seasonal variation in association patterns of wild spider monkeys (<Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>) at La Macarena,Colombia

Spider monkeys exhibit a fission–fusion type of social organization. I studied party size and party composition in wild long-haired spider monkeys (Ateles belzebuth belzebuth) in three study periods at La Macarena, Colombia and found that overall party size was larger in the fruit-abundant season. Mean party size in which males were observed was relatively stable across seasons. In contrast, the mean party size of females varied. Females were observed in larger parties in the fruit-abundant season than in the fruit-scarce season. Moreover, whereas males associated with each other at an almost equal frequency across seasons, females associated with each other more frequently in the fruit-abundant season. Females with infants or small juveniles were more often in association with other individuals than were cycling females. The intensity of individual relationships varied according to season, such that even mothers and sons were not always strongly associated. In a large party, females with infants may gain from predation avoidance but they are at a disadvantage in terms of scramble competition. The balance between these factors may change with fruit availability and may influence party size in different periods. For males, party formation may facilitate the defense of resources from neighboring groups more than provide predation avoidance. Electronic Publication     

Housing with Females Increases Testosterone and Cortisol Levels in Captive Groups of Black-Handed Spider Monkeys (Ateles geoffroyi)

The black‐handed spider monkey (Ateles geoffroyi) is a seasonal reproducer that requires a seclusiveness to copulate and has a fusion–fission social system. These features impose important restrictions to achieve reproduction of captive animals. We investigated if group composition in captive spider monkeys has any endocrine effects. We compared testosterone and cortisol concentrations during the mating season in all‐male and multifemale–multimale groups to study if the former condition impairs reproductive potential and increases stress. Concentrations of testosterone and cortisol of males living with females were higher than those of all‐male groups. In the multifemale–multimale condition, dominant males had the highest levels of testosterone, while the youngest males showed the highest concentrations of cortisol. Results show that males adjust well to isosexual grouping, this being an appropriate condition to keep animals when controlled reproduction is sought. Zoo Biol 31:490;–497, 2012. © 2012 Wiley Periodicals, Inc.     

Intra‐community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides)

We report on the first evidence of intra‐community coalitionary lethal aggression in muriquis (Brachyteles). The event occurred in southern muriquis (Brachyteles arachnoides) during a long‐term study (>15 years) of two social groups inhabiting mostly pristine Atlantic forest habitat in the Parque Estadual Carlos Botelho, southern São Paulo State, Brazil. The attack took place deep in the core area of the Group Caetê home range. Tense agonistic behaviors and vocalizations preceded the lethal coalitionary attack, and the tension increased over a 36–48 hr period. One adult female and two unidentified individuals also took part in a coalition led by six adult males. The members of the coalition collectively approached, embraced, immobilized and repeatedly bit the entire body of an adult male, resulting in severe bleeding injuries and the victim's death in less than 1 hr after the attack commenced. Combined ecological, behavioral and spatial data related to the event indicate that this was an intra‐community attack and suggest social tensions related to mating competition as the proximate trigger of the coalitionary killing. The attack resembled those reported for chimpanzees, with clear numeric superiority and a low risk of injury to aggressors, resulting in the death of a lone conspecific victim. This observation (n=1) is suggestive of a capacity for escalated aggression in muriquis and reinforces arguments for the potential adaptive significance of intra‐community aggression in male philopatric societies, as reported for spider monkeys and chimpanzees. These characteristics challenge the view of the muriquis as a peaceful primate and support the general hypothesis that imbalances of power contribute to intra‐specific killing in primates, such as chimpanzees and humans. Am. J. Primatol. 71:860–867, 2009. © 2009 Wiley‐Liss, Inc.