Free-ranging Spider Monkeys Research Articles

Strength of minority ties: the role of homophily and group composition in a weighted social network

Homophily describes a fundamental tie-formation mechanism in social networks in which connections between similar nodes occur at a higher rate than among dissimilar ones. In this article, we present an extension of the weighted social network (WSN) model that, under an explicit homophily principle, quantifies the emergence of attribute-dependent properties of a social system. To test our model, we make use of empirical association data of a group of free-ranging spider monkeys in Yucatan, Mexico. Our homophilic WSN model reproduces many of the properties of the empirical association network with statistical significance, specifically, the average weight of sex-dependent interactions (female-female, female-male, male-male), the weight distribution function, as well as many weighted macro properties (node strength, weighted clustering, and weighted number of modules), even for different age group combinations (adults, subadults, and juveniles). Furthermore, by performing simulations with fitted parameters, we show that one of the main features of a spider monkey social system, namely, stronger male-male interactions over female-female or female-male ones, can be accounted for by an asymmetry in the node-type composition of a bipartisan network, independently of group size. The reinforcement of connections among members of minority groups could be a general structuring mechanism in homophilic social networks.

The acoustic structure of spider monkey (Ateles geoffroyi) calls is related both to caller goal and arousal.

Analyzing the factors related to the acoustic structure of primate calls is fundamental to identifying the potential information these signals convey, and therefore, their potential function. It is well-accepted that caller arousal is an important driver of acoustic variation in call structure. However, evidence suggests that arousal alone cannot explain the production of calls with different acoustic structures. The "caller goal" framework posits that a call type (e.g., bark and chitter) is a signal which evolved to elicit specific changes on receiver behavior, and a caller's goal, not its arousal state, determines the basic acoustic structure of animal calls. To get a better insight into the effects of caller goal and arousal on the acoustic structure of primate calls, we analyzed the acoustic variation of 382 calls produced by 27 free-ranging spider monkeys (Ateles geoffroyi) in six call contexts representing three caller goals (establishing contact, engage in aggression, and predator presence) across two arousal states (high and low). Discriminant function analyses and linear mixed models showed a strong effect of caller goal on calls' acoustic structure and supported the effect of arousal state on acoustic variation; misclassified calls mainly occurred between the same caller goal categories (e.g., alarm low arousal and alarm high arousal), and acoustic differences between arousal contexts showed the same pattern across the three caller goals (e.g., low center frequency [kHz] values in high arousal contexts). Our results supported the view that caller goal is the primary driver of acoustic difference and showed the effects of caller arousal on other structural differences.

Dietary ethanol ingestion by free-ranging spider monkeys (Ateles geoffroyi).

Ethanol within ripe and over-ripe fruit is produced naturally through the metabolic activity of fermentative yeasts. As a consequence, frugivorous animals may chronically consume ethanol as part of their routine diet, although direct measurements of such exposure are lacking. Here, we present data on ethanol concentrations within fruits of Spondias mombin (Anacardiaceae) that are eaten by black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama. Of collected fruits that were partially consumed and then dropped by foraging monkeys, pulp-ethanol content was typically in the range of 1–2%; the percentage of pulp for consumed fruits was not significantly correlated with the ethanol concentration of the pulp remaining within each fruit. Urine samples from foraging spider monkeys were also evaluated for the ethanol metabolites ethyl glucuronide and ethyl sulfate; five of six samples tested positive for both compounds. In aggregate, these data indicate natural exposure to fruit-associated ethanol in a wild primate species.

Nocturnal mother–juvenile offspring interaction at the beginning of the juvenile period in free-ranging spider monkeys (Ateles geoffroyi): a report on two cases

The objective of this study was to describe the nocturnal behavior patterns of the interaction between mothers and their juvenile offspring at the beginning of the juvenile period in two dyads of free-ranging spider monkeys (Ateles geoffroyi). Based on direct field observation, we recorded six interaction behaviors between mothers and their juvenile offspring at nighttime and during the daylight period. The frequencies and proportions of each behavior recorded were analyzed for both conditions, and qualitative descriptions of each behavior were made. Observations revealed that the percentage of proximity in the dyads tended to increase at nighttime compared to the daylight period. In one of the dyads, we observed that the percentage of grooming also showed an upward tendency at nighttime compared to the daylight period. The dyads remained together to sleep during all 8 days of the study and were seen to seek arm-in-arm contact and to perform grooming behaviors. Our results suggest that mother–juvenile interaction at the onset of the juvenile period in spider monkeys may be characterized by greater proximity and social grooming behaviors, while the nocturnal observations suggest a strong attachment between mothers and their juveniles in this stage.

Age and social affinity effects on contact call interactions in free-ranging spider monkeys

Nonhuman primates’ vocal repertoire has shown little plasticity, with immatures producing adult-like acoustic structures. Yet, the use of different call types shows a degree of socially dependent flexibility during development. In several nonhuman primate species, group members exchange contact calls respecting a set of social and temporal rules that may be learned (e.g., overlap avoidance, turn-taking, social selection of interacting partners, and call type matching). Here, we study the use of contact calls in free-living adult and immature (old and young) spider monkeys (Ateles geoffroyi). We focused our study in two contact call types of the species’ repertoire: whinnies and high-whinnies. Our results suggest that individuals in all age classes produced both call types, with immatures producing less frequently the whinny call type. Immature individuals exchanged calls less often than adults, although their contribution increased with age. Conversely, mature individuals regulated their emissions by (1) exchanging more calls with their preferred affiliative partner and (2) matching the call type, while immatures did not. Our results show that contact call usage changes during development and suggest that adult rules might be learned. We argue that call matching is a “conversational rule” that young individuals acquire with apparent call-type-dependent variations during development. Our findings support the idea that social factors influence vocal development in nonhuman primates. We studied the social rules underlying vocal interaction patterns in free-ranging spider monkeys. We found that, while both immature (old and young) and mature individuals were able to produce the two species contact call types, they differed strongly in the way they used them. Matures called more often and exchanged more, while the vocal response rates of immature individuals increased with age. Also, mature individuals exchanged preferentially with their close associates and matched their call types while immatures did not. As in other species, we predict that these exchange patterns serve as a social rule to maintain and strengthen social bonds between individuals. We discuss our findings in light of the probable role of social learning during acquisition of the appropriate context of calling and of the response to others’ calls. These findings support the idea that social influences guide vocal development in nonhuman primates.

Acoustic variation of spider monkeys' contact calls (whinnies) is related to distance between vocalizing individuals and immediate caller behavior.

Due to several factors such as ecological conditions, group size, and social organization, primates frequently spend time out of visual contact with individuals of their own group. Through the use of long-distance vocalizations, often termed "contact calls," primates are able to maintain contact with out-of-sight individuals. Contact calls have been shown to be individually distinct, and reverberation and attenuation provide information about caller distance. It is less clear, however, whether callers actively change the structure of contact calls depending on the distance to the presumed listeners. We studied this question in spider monkeys (Ateles geoffroyi), a species with complex spatial dynamics (fission-fusion society) that produces highly frequency modulated contact calls, denominated "whinnies." We determined the acoustic characteristics of 566 whinnies recorded from 35 free-ranging spider monkeys that belong to a community located in Mexico, and used cluster analyses, discriminant function analyses, and generalized linear mixed models to assess if they varied in relation to the presumed distance to the listener. Whinnies could be grouped into five subtypes. Since the lowest frequency subtype was mainly produced by spider monkeys that exchanged whinnies at longer distances, and lower frequency calls propagate across longer distances, our results suggest that whinnies vary in order to enhance vocal contact between individuals separated by different distances. Our results also revealed that whinnies convey potential information about caller immediate behaviors and corroborated that these calls are individually distinct. Overall, our results suggest that whinny acoustic variation facilitates the maintenance of vocal contact between individuals living in a society with complex spatial dynamics.

Proximal and Distal Predictors of the Spider Monkey's Stress Levels in Fragmented Landscapes.

The rapid loss, fragmentation and degradation of tropical forests threaten the survival of many animal species. However, the way in which these phenomena affect animal health has been poorly explored, thus limiting the design of appropriate conservation strategies. To address this, here we identified using linear mixed models the effect of proximal (diet, activity pattern, hunting and logging) and distal (sum of the basal areas of fruiting-tree species [SBAFS], landscape forest cover and degree of forest fragmentation) variables over fecal glucocorticoid metabolite (fGCM) levels–hormones associated with animal health and fitness–of six groups of spider monkeys (Ateles geoffroyi) inhabiting six landscapes with different spatial structures in Mexico. Proximal variables showed a stronger predictive power over fGCMs than distal. In this sense, increases in travel time, the occurrence of hunting, and reductions in rest time and fruit consumption resulted in higher fGCM levels. Regarding distal variables, increases in SBAFS were negatively related to fGCM levels, thus suggesting that food scarcity increases stress hormone levels. Nevertheless, contrary to theoretical expectations, spider monkeys living in smaller tracts of forest spent less time travelling, but the same time feeding on fruit as those in more forested areas. The lower net energy return associated with this combination of factors would explain why, contrary to theoretical expectations, increased forest cover was associated with increased levels of fGCMs in these groups. Our study shows that, at least in the short term, spider monkeys in fragmented landscapes do not always present higher levels of stress hormones compared to those inhabiting continuous forest, and the importance of preserving fruit sources and controlling hunting for reducing the levels of stress hormones in free ranging spider monkeys.

Self-anointing behavior in free-ranging spider monkeys (Ateles geoffroyi) in Mexico

During 250 h of observation, a total of 20 episodes of self-anointing, that is, the application of scent-bearing material onto the body, were recorded in a group of free-ranging Mexican spider monkeys (Ateles geoffroyi). The animals used the leaves of three species of plants (Brongniartia alamosana, Fabaceae; Cecropia obtusifolia, Cecropiaceae; and Apium graveolens, Umbelliferae) two of which have not been reported so far in this context in any New World primate species. The findings that only two males displayed self-anointing, that only the sternal and axillary regions of the body were rubbed with the mix of saliva and plant material, and a lack of correlation between the occurrence of self-anointing and time of day, season of the year, ambient temperature or humidity do not fit the hypothesis that this behavior functions in repelling insects and/or mitigating topical skin infections in this species. Rather, the data and the observation that the leaves of all three plant species spread an intensive and aromatic odor when crushed, support the hypothesis that self-anointing in A. geoffroyi may play a role in the context of social communication, possibly for signaling of social status or to increase sexual attractiveness.

L�vy walk patterns in the foraging movements of spider monkeys (Ateles geoffroyi)

Scale invariant patterns have been found in different biological systems, in many cases resembling what physicists have found in other, nonbiological systems. Here we describe the foraging patterns of free-ranging spider monkeys (Ateles geoffroyi) in the forest of the Yucatan Peninsula, Mexico and find that these patterns closely resemble what physicists know as Levy walks. First, the length of a trajectory’s constituent steps, or continuous moves in the same direction, is best described by a power-law distribution in which the frequency of ever larger steps decreases as a negative power function of their length. The rate of this decrease is very close to that predicted by a previous analytical Levy walk model to be an optimal strategy to search for scarce resources distributed at random. Second, the frequency distribution of the duration of stops or waiting times also approximates to a power-law function. Finally, the mean square displacement during the monkeys’ first foraging trip increases more rapidly than would be expected from a random walk with constant step length, but within the range predicted for Levy walks. In view of these results, we analyze the different exponents characterizing the trajectories described by females and males, and by monkeys on their own and when part of a subgroup. We discuss the origin of these patterns and their implications for the foraging ecology of spider monkeys.

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.

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.

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.