Thanatology in the northern muriqui (Brachyteles hypoxanthus).

Primate thanatology, or the study of primate responses to dying and death, has become increasingly relevant in recent years. However, the number of reports remains small and the quality of published records is highly variable. Here, we extend the literature on comparative thanatology with observations on a population of the northern muriqui (Brachyteles hypoxanthus). We compiled all seven cases of muriqui responses to dead, dying, or abandoned infants observed by trained researchers of the Muriqui Project of Caratinga between 1998 and 2020. Four different adult females were observed carrying their dead offspring (n = 4) and one of these females was also observed carrying her dead grand-offspring (n = 1). Five of the seven cases involved dead newborns, one involved a newborn abandoned by its mother on the forest floor, and one involved a 1.6-year-old infant that was visibly ill and died after its mother left it on the ground. Dead newborns were carried for 1-3 days, and all cases occurred during the dry season months. No other age-sex classes were observed to interact with the dead or dying immatures. Our observations are consistent with hypotheses concerning the predominance of dead-infant carrying in other primates, and with the effects of climate on rates of corpse disintegration. They also show the value of long-term studies for obtaining and understanding anecdotal records of rare behavior.

Olfactory sensitivity for mold-associated odorants in CD-1 mice and spider monkeys.

Using operant conditioning procedures, we assessed the olfactory sensitivity of six CD-1 mice and three spider monkeys for mold-associated odorants. We found that with all eight stimuli, the mice detected concentrations as low as 0.1 ppm (parts per million), and with two of them individual animals even detected concentrations as low as 1 ppt (parts per trillion). The spider monkeys detected concentrations as low as 4 ppm with all eight stimuli, and with four of them individual animals even detected concentrations as low as 4 ppb (parts per billion). Between-species comparisons showed that with all eight odorants, the mice displayed significantly lower threshold values, that is, a higher sensitivity than the spider monkeys, but not than human subjects tested in previous studies. Analysis of odor structure-activity relationships showed that in both species, the type of oxygen-containing functional group and the presence versus absence of a double bond as well as the length of the carbon backbone of the odor stimuli had a systematic effect on detectability. We conclude that both mice and spider monkeys are clearly able to detect the presence of molds and thus to assess the palatability of potential food using the volatiles produced by molds during putrefaction.

Social inhibition and behavioural flexibility when the context changes: a comparison across six primate species.

The ability to inhibit previously employed strategies and flexibly adjust behavioural responses to external conditions may be critical for individual survival. However, it is unclear which factors predict their distribution across species. Here, we investigated social inhibition and behavioural flexibility in six primate species (chimpanzees, bonobos, orangutans, gorillas, capuchin monkeys and spider monkeys) differing in terms of phylogenetic relatedness, foraging ecology and social organization. Depending on the social context, individuals could maximize their food intake by inhibiting the selection of a larger food reward in one condition (i.e. inhibition), but not in others, which required them to flexibly switching strategies across conditions (i.e. behavioural flexibility). Overall, our study revealed inter-specific differences in social inhibition and behavioural flexibility, which partially reflected differences in fission-fusion dynamics. In particular, orangutans and chimpanzees showed the highest level of inhibitory skills, while gorillas and capuchin monkeys showed the lowest one. In terms of behavioural flexibility, orangutans and spider monkeys were the best performers, while bonobos and capuchin monkeys were the worst ones. These results contribute to our understanding that inhibition and behavioural flexibility may be linked in more complex ways than usually thought, although both abilities play a crucial role in efficient problem solving.

Behavioural and Glucocorticoid Responses of a Captive Group of Spider Monkeys to Short-Term Variation in Food Presentation.

The presentation of food may affect feeding competition and the well-being of captive social species. We hypothesized that feeding competition in a captive group of 5 black-handed spider monkeys (Ateles geoffroyi) should increase in response to certain food presentations in terms of size, distribution and quality of food, and that higher feeding competition should lead to an increase in agonism and physiological stress (measured by faecal glucocorticoid metabolites, FGCM) as well as to a decrease in affiliation, proximity among individuals and feeding activity. We used 5 experimental treatments representing different combinations of size, distribution and quality of food. We observed social interactions for 100 h, collected 6,500 proximity and feeding activity records, and gathered 226 faecal samples. When food was clumped, individuals spent less time feeding, and there was also significant individual variation in feeding activity within treatments. FGCM levels were higher when food was clumped. These results are probably linked to an increase in feeding competition when food is concentrated. At least in small groups of spider monkeys, dispersing food in two feeding stations may be sufficient to decrease differences among individuals in priority of access to food resources, hence reducing physiological stress and interindividual differences in feeding activity.

Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics.

Elevated risk of disease transmission is considered a major cost of sociality, although empirical evidence supporting this idea remains scant. Variation in spatial cohesion and the occurrence of social interactions may have profound implications for patterns of interindividual parasite transmission. We used a social network approach to shed light on the importance of different aspects of group-living (i.e. within-group associations versus physical contact) on patterns of parasitism in a neotropical primate, the brown spider monkey (Ateles hybridus), which exhibits a high degree of fission-fusion subgrouping. We used daily subgroup composition records to create a 'proximity' network, and built a separate 'contact' network using social interactions involving physical contact. In the proximity network, connectivity between individuals was homogeneous, whereas the contact network highlighted high between-individual variation in the extent to which animals had physical contact with others, which correlated with an individual's age and sex. The gastrointestinal parasite species richness of highly connected individuals was greater than that of less connected individuals in the contact network, but not in the proximity network. Our findings suggest that among brown spider monkeys, physical contact impacts the spread of several common parasites and supports the idea that pathogen transmission is one cost associated with social contact.

Evaluating handedness measures in spider monkeys.

Despite long-standing interest and a vast body of literature, there is still disagreement as to how handedness should be measured in nonhuman primates. The primary goal of this study was to evaluate two common measures of handedness in nonhuman primates using the spider monkey, a unique study species due to its lack of a thumb and limited dexterity. Contrary to our predictions and previous findings in Ateles, there was no evidence for group-level hand biases on either the coordinated bimanual TUBE task or a unimanual reaching task. At the individual level, monkeys exhibited preferences on both tasks. There was a leftward trend on the bimanual task and a rightward trend on the unimanual task. Monkeys that were strongly lateralized on the bimanual task showed a comparable hand preference on the unimanual task, whereas monkeys with a moderate preference on the bimanual task shifted to the opposite hand on the unimanual task. Comparing across measures, the two hand-use patterns reported (consistent and shift) might have obscured group-level findings, given the available sample size. Overall, these data reaffirm that task type influences hand use in primates, and multiple measures are needed to fully characterize the construct of handedness. Consideration should be given to the difficulty required between tasks as well as between species.

Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment.

Numerous animal species currently experience habitat loss and fragmentation. This might result in behavioral and dietary adjustments, especially because fruit availability is frequently reduced in fragments. Food scarcity can result in elevated physiological stress levels, and chronic stress often has detrimental effects on individuals. Some animal species exhibit a high degree of fission-fusion dynamics, and theory predicts that these species reduce intragroup feeding competition by modifying their subgroup size according to resource availability. Until now, however, there have been few studies on how species with such fission-fission dynamics adjust their grouping patterns and social behavior in small fragments or on how food availability influences their stress levels. We collected data on fruit availability, feeding behavior, stress hormone levels (measured through fecal glucocorticoid metabolites (FGCM)), subgroup size, and aggression for two groups of brown spider monkeys (Ateles hybridus) in a small forest fragment in Colombia and examined whether fruit availability influences these variables. Contrary to our predictions, spider monkeys ranged in smaller subgroups, had higher FGCM levels and higher aggression rates when fruit availability was high compared to when it was low. The atypical grouping pattern of the study groups seems to be less effective at mitigating contest competition over food resources than more typical fission-fusion patterns. Overall, our findings illustrate that the relationship between resource availability, grouping patterns, aggression rates, and stress levels can be more complex than assumed thus far. Additional studies are needed to investigate the long-term consequences on the health and persistence of spider monkeys in fragmented habitats.

Ecological factors predictive of wild spider monkey (Ateles belzebuth) foraging decisions in Yasuní, Ecuador.

Because fruiting trees are uncommon in tropical forests, frugivorous primates experience selective pressure to incorporate knowledge of where to find feeding trees, what to expect when they arrive there, and when they can return after depleting a tree. I investigated these abilities in wild spider monkeys (Ateles belzebuth) in Yasuní, Ecuador, by analyzing the characteristics of feeding trees that drive foraging decisions. Foraging data were derived from four 2-week follows of focal adult females, conducted between May and December 1999, during which I measured and mapped all trees in which the focal subject fed, feeding bout duration, and the number of conspecifics feeding simultaneously with the focal. Taking into account the order in which feeding trees were visited across each follow, I analyzed each foraging decision from the second week of a follow, treating all previously visited trees as options for visits. I scored each option tree in terms of nine ecological variables, including the distance from the decision to each location tree, DBH, recent feeding time and mean feeding times for the focal and other monkeys present, and the interval in hours between the foraging decision and the most recent visit to each option tree. I then examined the predictive strength of the model using logistic regression analysis, comparing characteristics of selected trees to those not selected. The overall model successfully predicted trees selected by focal monkeys (r(2) = 0.27). Monkeys preferentially moved to nearby, large canopy trees, in which previous feeding success was high, and which were visited after an interval of 3.5 days. Interval mattered most for medium and large trees, but did not predict selection for trees <10 cm DBH. Despite the large home range and large numbers of trees, Yasuní spider monkeys appeared to integrate spatial, value, and temporal information when deciding where to feed.

A comparison of computer-generated and naturally occurring foraging patterns in route-network-constrained spider monkeys.

The attribution of goal-directed behavior to observations of primate foraging and ranging requires that simpler explanations for observed behavior patterns be eliminated. Computer-generated simulations of non-goal-directed foraging behavior can be used as null models for higher complexity cognitive foraging, and can provide quantifiable data against which to compare the observed behavioral patterns in wild primates. In this paper, we compare the results of two variations of computer simulated null models with observed foraging behavior of wild spider monkeys (Ateles belzebuth). One model simulates monkeys searching using a modified random-walk model in which monkeys alternate 100-m steps with turn angles derived from observed behavior. The second model constrains travel to an observed route system derived from observations of wild spider monkeys. Simulated monkeys in each model searched among increasing densities of feeding trees ranging from 10 to 1,000. We compared travel distance, travel directness, and accuracy of starting direction for each feeding tree discovered for the two models. We then compared these results with those derived from observations of wild spider monkeys. Route-model monkeys traveled shorter distances and more directly to feeding trees than did randomly foraging monkeys, and discovered trees in the direction they started more often. Observed spider monkeys outperformed simulated monkeys from both models in all variables, allowing us to reject the null hypothesis that observed foraging and ranging behavior could be explained by non-goal-directed travel.

Males follow females during fissioning of a group of northern muriquis.

Although well documented in matrilocal primate species, group fission is still a poorly known phenomenon among patrilocal primates. In this paper we describe in detail a group fission event in the population of northern muriquis at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala in Caratinga, Minas Gerais, Brazil, using Social Network Analyses (SNA). Data on association patterns were collected during systematic observations from May 2002 to September 2005, and analyzed for dry (from May to October) and rainy seasons (from November to April). The fission process started with subgroup formation in the rainy season 2002-2003, and was completed by the dry season of 2003. By the dry season 2003, the parent group (Jaó) had fissioned to form a second mixed-sex group (Nadir) while a subgroup of males (MU) moved between the parent group and the newly established group. Before the Jaó group fission started (dry season 2002) and during its initial phases (rainy season 2002-2003), females that ultimately composed the daughter group (Nadir) were the most peripheral in the association network. In the rainy season 2002-2003, the median monthly (N=6) operational sex ratio (OSR) of Jaó group was 2.81. However, once Jaó females initiated the fissioning process to establish the Nadir group, the OSR was more favorable to males in the Nadir group than in the Jaó group. Our results suggest that males followed the females to escape an unfavorable OSR in their natal group.

Site fidelity in space use by spider monkeys (Ateles geoffroyi) in the Yucatan peninsula, Mexico.

Animal home ranges may vary little in their size and location in the short term but nevertheless show more variability in the long term. We evaluated the degree of site fidelity of two groups of spider monkeys (Ateles geoffroyi) over a 10- and 13-year period, respectively, in the northeastern Yucatan peninsula, Mexico. We used the Local Convex Hull method to estimate yearly home ranges and core areas (defined as the 60% probability contour) for the two groups. Home ranges varied from 7.7 to 49.6 ha and core areas varied from 3.1 to 9.2 ha. We evaluated the degree of site fidelity by quantifying the number of years in which different areas were used as either home ranges or core areas. Large tracts were used only as home ranges and only for a few years, whereas small areas were used as either core area or home range for the duration of the study. The sum of the yearly core areas coincided partially with the yearly home ranges, indicating that home ranges contain areas used intermittently. Home ranges, and especially core areas, contained a higher proportion of mature forest than the larger study site as a whole. Across years and only in one group, the size of core areas was positively correlated with the proportion of adult males in the group, while the size of home ranges was positively correlated with both the proportion of males and the number of tree species included in the diet. Our findings suggest that spider monkey home ranges are the result of a combination of long-term site fidelity and year-to-year use variation to enable exploration of new resources.

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.

Influence of climatic variables, forest type, and condition on activity patterns of Geoffroyi's spider monkeys throughout Mesoamerica.

Understanding how species cope with variations in climatic conditions, forest types and habitat amount is a fundamental challenge for ecologists and conservation biologists. We used data from 18 communities of Mesoamerican spider monkeys (Ateles geoffroyi) throughout their range to determine whether their activity patterns are affected by climatic variables (temperature and rainfall), forest types (seasonal and nonseasonal forests), and forest condition (continuous and fragmented). Data were derived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador, Costa Rica, and Panama), cumulatively representing more than 18 years (221 months, >3,645 hr) of behavioral observations. Overall, A. geoffroyi spent most of their time feeding (38.4 ± 14.0%, mean ± SD) and resting (36.6 ± 12.8%) and less time traveling (19.8 ± 11.3%). Resting and feeding were mainly affected by rainfall: resting time increased with decreasing rainfall, whereas feeding time increased with rainfall. Traveling time was negatively related to both rainfall and maximum temperature. In addition, both resting and traveling time were higher in seasonal forests (tropical dry forest and tropical moist forest) than in nonseasonal forests (tropical wet forest), but feeding time followed the opposite pattern. Furthermore, spider monkeys spent more time feeding and less time resting (i.e., higher feeding effort) in forest fragments than in continuous forest. These findings suggest that global climate changes and habitat deforestation and fragmentation in Mesoamerica will threaten the survival of spider monkeys and reduce the distributional range of the species in the coming decades.

To whom the play signal is directed: a study of headshaking in black-handed spider monkeys (Ateles geoffroyi).

Spider monkeys shake their heads so as to facilitate amicable social contact. This occurs frequently during vigorous play fighting, and so is common during the juvenile period. Occasionally, juvenile spider monkeys use headshakes during nonsocial locomotor play. In this study, head shaking in early infancy and in adulthood was studied in a captive troop of spider monkeys, with a total of 8 infants studied from shortly after birth to just before weaning. Three hypotheses to account for these nonsocial headshakes were tested. The play as the experience of the unexpected hypothesis was found wanting because nonsocial headshakes were most common in early infancy, before the onset of the juvenile peak in play. The immature misdirection of signals hypothesis was also found wanting because the headshakes were correctly directed at other monkeys, but not at inanimate objects that were grabbed and mouthed. Both also failed to predict the occurrence of the observed nonsocial headshakes in adults. The hypothesis best supported by the data is that, under some situations, headshakes are self-directed to promote action when confronting contexts of uncertainty.

Inferential reasoning by exclusion in great apes, lesser apes, and spider monkeys.

Using the cups task, in which subjects are presented with limited visual or auditory information that can be used to deduce the location of a hidden reward, Call (2004) found prima facie evidence of inferential reasoning by exclusion in several great ape species. One bonobo (Pan paniscus) and two gorillas (Gorilla gorilla) appeared to make such inferences in both the visual and auditory domains. However, common chimpanzees (Pan troglodytes) were successful only in the visual domain, and Bornean orangutans (Pongo pygmaeus) in neither. The present research built on this paradigm, and Experiment 1 yielded prima facie evidence of inference by exclusion in both domains for two common chimpanzees, and in the visual domain for two Sumatran orangutans (Pongo abelii). Experiments 2 and 3 demonstrated that two specific associative learning explanations could not readily account for these results. Because an important focus of the program of research was to assess the cognitive capacities of lesser apes (family Hylobatidae), we modified Call's original procedures to better suit their attentional and dispositional characteristics. In Experiment 1, testing was also attempted with three gibbon genera (Symphalangus, Nomascus, Hylobates), but none of the subjects completed the standard task. Further testing of three siamangs (Symphalangus syndactylus) and a spider monkey (Ateles geoffroyi) using a faster method yielded prima facie evidence of inferential reasoning by exclusion in the visual domain among the siamangs (Experiment 4).

Spider monkeys (Ateles geoffroyi) and capuchin monkeys (Cebus apella) follow gaze around barriers: evidence for perspective taking?

Gaze following is an adaptive skill that might have been selected in social species, such as many nonhuman primates, to obtain information about food location, predators, and social interactions. The authors investigated the ability of spider monkeys (Ateles geoffroyi) and capuchin monkeys (Cebus apella) to follow the gaze of a human around barriers and the presence of "looking back" behavior. In the 1st experiment, a human looked to a target location inside the testing room, whereas in the 2nd experiment, the human looked behind an opaque barrier placed outside the testing room. The authors compared the frequency of looking at the target location with the corresponding baseline looking frequencies. Both species (a) showed evidence of spontaneous gaze following in the 1st experiment and (b) engaged in gaze following behind the barrier in the 2nd experiment. In contrast, neither species performed "looking back" responses. The authors conclude that both monkey species showed some indication of perspective-taking abilities, although the absence of "looking back" behavior suggests a potential difference from the abilities shown by the great apes.

Intra-community infanticide and forced copulation in spider monkeys: a multi-site comparison between Cocha Cashu, Peru and Punta Laguna, Mexico.

We describe two cases of infanticide, two suspected infanticides, and a forced copulation by familiar resident males in two populations of wild spider monkeys (Ateles belzebuth chamek and A. geoffroyi yucatanensis). These are the first known infanticides and forced copulation in spider monkeys. Data were gathered from four neighboring communities of spider monkeys in Manu National Park at the Cocha Cashu Biological Station, Peru and two communities in the Otoch Ma'ax Yetel Kooh Reserve at Punta Laguna, Mexico, during intensive field studies of over 2,000 hr each. These are rare behaviors, but results suggest that mating history and sexual coercion are important in spider monkey social relationships.

Mother-offspring associations in northern muriquis, Brachyteles hypoxanthus.

Maternal care of offspring is ubiquitous among primates, but its duration varies across species due to factors such as dispersal patterns and social dynamics, which influence opportunities for and potential benefits of maternal investment in older offspring, respectively. We examined mother-offspring associations in wild northern muriquis (Brachyteles hypoxanthus), in which males are philopatric, females typically disperse before puberty, and social relationships among and between males and females are egalitarian. Associations were systematically recorded between ten mothers, each with two-six offspring in the study group, and all group members from August 2003-May 2004 at the RPPN-Feliciano Miguel Abdala in Minas Gerais, Brazil. Infants of both sexes received similarly high percentages of their mothers' association time. Mothers without infants also maintained strong associations with their youngest juvenile sons. Mothers did not spend consistently more time associating with either juvenile or adult sons than daughters. Our finding of non-preferential associations between muriqui mothers and their older male offspring suggests that extended maternal investment in offspring may be of minimal value in their egalitarian society compared with its value for species living in hierarchical societies.

Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications.

Many wild primates occupy large home ranges and travel long distances each day. Navigating these ranges to find sufficient food presents a substantial cognitive challenge, but we are still far from understanding either how primates represent spatial information mentally or how they use this information to navigate under natural conditions. In the course of a long-term socioecological study, we investigated and compared the travel paths of sympatric spider monkeys (Ateles belzebuth) and woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. During several field seasons spanning an 8-year period, we followed focal individuals or groups of both species continuously for periods of multiple days and mapped their travel paths in detail. We found that both primates typically traveled through their home ranges following repeatedly used paths, or "routes". Many of these routes were common to both species and were stable across study years. Several important routes appeared to be associated with distinct topographic features (e.g., ridgetops), which may constitute easily recognized landmarks useful for spatial navigation. The majority of all location records for both species fell along or near identified routes, as did most of the trees used for fruit feeding. Our results provide strong support for the idea that both woolly and spider monkey use route-based mental maps similar to those proposed by Poucet (Psychol Rev 100:163-182, 1993). We suggest that rather than remembering the specific locations of thousands of individual feeding trees and their phenological schedules, spider and woolly monkeys could nonetheless forage efficiently by committing to memory a series of route segments that, when followed, bring them into contact with many potential feeding sources for monitoring or visitation. Furthermore, because swallowed and defecated seeds are deposited in greater frequency along routes, the repeated use of particular travel paths over generations could profoundly influence the structure and composition of tropical forests, raising the intriguing possibility that these and other primate frugivores are active participants in constructing their own ecological niches. Building upon the insights of Byrne (Q J Exp Psychol 31:147-154, 1979, Normality and pathology in cognitive functions. Academic, London, pp 239-264, 1982) and Milton (The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York, 1980, On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 375-417, 2000), our results highlight the likely general importance of route-based travel in the memory and foraging strategies of nonhuman primates.