Not just females: the socio-ecology of social interactions between spider monkey males.

Male-male relationships are mostly characterized by competition. However, males also cooperate with one another if socio-ecological conditions are suitable. Due to their male philopatry, the need for cooperation in home range defence and high degree of fission-fusion dynamics, spider monkeys provide an opportunity to investigate how male-male interactions are associated with socio-ecological factors, such as the presence of potentially receptive females, the degree of food availability and the likelihood of home range defence. We tested predictions about changes in social interactions between wild spider monkey males in relation to these factors. First, males did not change their interaction patterns when potentially receptive females were in the subgroup compared to when they were absent. Second, males tended to be less tolerant of one another when feeding, but spent more time grooming, in contact and proximity with one another when food availability was lower than when it was higher. Third, males exchanged fewer embraces, spent less time grooming, in proximity and in contact with one another, and spent more time vigilant at the home range boundary area than at other locations. Our findings contribute to the understanding of social flexibility and the importance of considering males in socio-ecological models of any group-living species.

Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

Should I stay or should I go? How activity synchronization affects fission decisions.

Group-living animals need to deal with conflicting interests to maintain cohesion. When the costs of doing so outweigh the benefits, the group may (temporarily) split into two or more subgroups. Conflicting interests can concern what activity to pursue or the direction of travel. Temporary group separation is a common feature in species with a high degree of fission-fusion dynamics. We investigated the role activity synchronization played in fission decisions in a spider monkey group living in the Otoch Ma'ax Yetel Kooh Nature Reserve, Yucatan, Mexico. For 21 months, we recorded every fission event occurring in the followed subgroup, as well as the subgroup activity. We classified the activity as 'synchronized' when at least 75% of subgroup members performed the same activity (resting, foraging, socializing or travelling); otherwise, we classified it as 'non-synchronized'. We found that fission events occurred more often when the activity was non-synchronized. In addition, when the activity was synchronized, fission events occurred more often when spider monkeys were travelling than when they were engaged in other subgroup activities. Our findings highlight the role of conflicting interests over the activity to pursue and travel direction in fission decisions.

A catastrophic tropical drought kills hydraulically vulnerable tree species.

Drought-related tree mortality is now a widespread phenomenon predicted to increase in magnitude with climate change. However, the patterns of which species and trees are most vulnerable to drought, and the underlying mechanisms have remained elusive, in part due to the lack of relevant data and difficulty of predicting the location of catastrophic drought years in advance. We used long-term demographic records and extensive databases of functional traits and distribution patterns to understand the responses of 20-53 species to an extreme drought in a seasonally dry tropical forest in Costa Rica, which occurred during the 2015 El Niño Southern Oscillation event. Overall, species-specific mortality rates during the drought ranged from 0% to 34%, and varied little as a function of tree size. By contrast, hydraulic safety margins correlated well with probability of mortality among species, while morphological or leaf economics spectrum traits did not. This firmly suggests hydraulic traits as targets for future research.

Quantifying uncertainty due to fission-fusion dynamics as a component of social complexity.

Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics.

Homosexual Behavior Between Male Spider Monkeys (Ateles geoffroyi).

Homosexual behavior is defined as genital contact or genital manipulation between same-sex individuals. In nonhuman primates, it may regulate social relationships by serving as a means of reconciliation, tension alleviation, or alliance formation. Grappling is a rare and complex behavior, which most frequently occurs between same-sex individuals of the genus Ateles and can include mutual manipulation of the genitalia. Here we report three cases of penile-anal intromission during grappling between wild male spider monkeys living in the natural protected area of Otoch Ma'ax Yetel Kooh, Mexico. In all the observed cases, the same adult male was the actor. To our knowledge, this is the first report of penile-anal intromission between males in any New World primate species.

Predation Attacks on Wild Spider Monkeys (Ateles geoffroyi).

We report 2 cases of predation on an adult and a subadult spider monkey (Ateles geoffroyi) by a puma (Puma concolor) and an unidentified terrestrial predator at the natural protected area of Otoch Ma'ax yetel Kooh, in the Yucatan Peninsula, Mexico. Although spider monkeys are believed to experience overall low predation pressure compared to other primate species, our observations show that predation occurs in the study area and therefore behavioral strategies are likely to be in place to reduce predation risk. Our observations are further evidence that terrestrial predators are a threat for both young and full-grown spider monkeys.

How Survey Design Affects Monkey Counts: A Case Study on Individually Recognized Spider Monkeys (Ateles geoffroyi).

The fast movement and high degree of fission-fusion dynamics of spider monkeys (Ateles spp.) make them notoriously difficult to survey. We examined which aspects of survey design affect spider monkey sightings along transects in a group of individually recognized spider monkeys (Ateles geoffroyi) in Punta Laguna, Yucatan, Mexico. We calculated the number of monkeys and subgroups sighted per transect walk. Using generalized linear models, we found no effect of the number of observers, transect type (new vs. existing), walking speed, or time of day on individual monkey counts or subgroup counts. Recounting of individuals was relatively rare and occurred when transects were walked relatively slowly. We missed more young than adult monkeys. The group composition based on survey data was similar to the known group composition. Based on our findings we recommend that surveys performed on relatively flat terrain be conducted at speeds similar to or faster than the moving speed of spider monkeys to minimize recounting of individuals and that young:adult female ratios based on survey data be interpreted as conservative indicators of population health. The novel methods presented to determine sources of bias in population estimates are applicable to a wide range of primates that are difficult to survey.

Quality and overlap of individual core areas are related to group tenure in female spider monkeys.

In species with a high degree of fission-fusion dynamics group members may differ in the use of the group home range to reduce food competition. Such differential use may result in distinct individual core areas. We studied core area quality and overlap among 21 female spider monkeys belonging to the same group over a period of 4 years. Core areas ranged between 62 and 161 ha with a mean overlap of 56% between any given two females. Only a small portion (mean = 3 ha) of each individual core area was used exclusively. No single part of the home range was used as core area by all females, and only an area of less than 1 ha was used as part of the core area by 20 of the 21 females. The time a female spent in the group (i.e., group tenure) was associated with characteristics of the core areas: the longer the group tenure, the better the quality of her core area. In addition, the longer the time two females spent together in the same group, the larger the overlap between their individual core areas. As this result was obtained while controlling for the time two females spent together in the same subgroup, females may reduce direct competition by using the same resource at different times. In sum, spider monkey females' group tenure plays a central role in the quality and overlapping patterns of their individual core areas.

Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys.

New World monkeys exhibit prominent colour vision variation due to allelic polymorphism of the long-to-middle wavelength (L/M) opsin gene. The known spectral variation of L/M opsins in primates is broadly determined by amino acid composition at three sites: 180, 277 and 285 (the 'three-sites' rule). However, two L/M opsin alleles found in the black-handed spider monkeys (Ateles geoffroyi) are known exceptions, presumably due to novel mutations. The spectral separation of the two L/M photopigments is 1.5 times greater than expected based on the 'three-sites' rule. Yet the consequence of this for the visual ecology of the species is unknown, as is the evolutionary mechanism by which spectral shift was achieved. In this study, we first examine L/M opsins of two other Atelinae species, the long-haired spider monkeys (A. belzebuth) and the common woolly monkeys (Lagothrix lagotricha). By a series of site-directed mutagenesis, we show that a mutation Y213D (tyrosine to aspartic acid at site 213) in the ancestral opsin of the two alleles enabled N294K, which occurred in one allele of the ateline ancestor and increased the spectral separation between the two alleles. Second, by modelling the chromaticity of dietary fruits and background leaves in a natural habitat of spider monkeys, we demonstrate that chromatic discrimination of fruit from leaves is significantly enhanced by these mutations. This evolutionary renovation of L/M opsin polymorphism in atelines illustrates a previously unappreciated dynamism of opsin genes in shaping primate colour vision.

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.

Why so complex? Emotional mediation of revenge, forgiveness, and reconciliation.

Humans have the cognitive abilities to implement the revenge and forgiveness systems hypothesized by McCullough et al., but the evidence suggests that simpler processes may underlie most revenge cases in humans and other animals. The mediating role of emotions can be at the basis of the flexibility needed in the hypothesized systems and the associated assessment of social relationships.

Variation in communicative complexity in relation to social structure and organization in non-human primates.

Communicative complexity relates to social complexity, as individuals in more complex social systems either use more signals or more complex signals than individuals living in less complex ones. Taking the individual group member's perspective, here we examine communicative complexity in relation to social complexity, which arises from two components of social systems: social structure and social organization. We review the concepts of social relationships and social complexity and evaluate their implications for communicative and cognitive complexity using examples from primate species. We focus on spider monkeys (Ateles geoffroyi), as their social organization is characterized by flexibility in grouping dynamics and they use a variety of communicative signals. We conclude that no simple relationship exists among social complexity, communicative complexity and cognitive complexity, with social complexity not necessarily implying cognitive complexity, and communicative and cognitive complexity being independently linked to social complexity. To better understand the commonly implied link between social complexity and cognitive complexity it is crucial to recognize the complementary role of communicative complexity. A more elaborated communicative toolkit provides the needed flexibility to deal with dynamic and multifaceted social relationships and high variation in fission-fusion dynamics. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Mother-infant relationships and infant independence in wild Geoffroy's spider monkeys (Ateles geoffroyi).

We studied mother-infant relationships and infant independence in wild Geoffroy's spider monkeys (Ateles geoffroyi) during the first 3 years of infant life. We used 15-min focal sampling to collect data on mother-infant interactions and infant behavior in 12 mother-infant dyads in the Yucatan peninsula, Mexico. Data were analyzed using generalized linear mixed models. Newborns spent almost all their time in proximity and in contact with their mothers. The time infants spent within one-arm reach from the mother decreased with age, and the infant was primarily responsible for maintaining proximity. The time infants spent farther than 8 m from the mother, in independent locomotion, exploration, and proximity with group members other than the mother increased with age. We identified two developmental periods associated with critical milestones of infant independence: the first at 8 to 10 months when independent locomotion and exploration began, and the proportion of time in proximity with group members other than the mother increased and the second at 19 to 21 months when the mother's rejection started, maternal carrying ended and mother's help, in the form of bridging canopy gaps, peaked. Compared with other primate species of similar size, Ateles geoffroyi have an extended dependence period, which could be related to the cognitive and developmental challenges imposed by their socioecological characteristics. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Behavioral Responses to Body Position in Bees: The Interaction of Apis mellifera and Lithurgus littoralis in Prickly Pear Flowers.

The behavior of bees is modulated by the presence of other bees and potentially by the visual information transmitted by the different body positions of bees while visiting flowers. We tested whether bee body position promoted the attraction and/or antagonistic behavior of con- and hetero-specific bees that interacted on prickly pear flowers of Opuntia huajuapensis. To test this, we placed dummy model bees of Apis mellifera and the native Lithurgus littoralis in flowers in three common body positions: alert, feeding, and horizontal. The results showed that dummy model bees in feeding and horizontal body positions attracted A. mellifera bees, while the alert position attracted native male L. littoralis. Male L. littoralis bees spent more time attacking model bees in horizontal and alert positions. The position of dummy bees also influenced response times. Bees of A. mellifera responded fastest to L. littoralis in the alert and horizontal position, male L. littoralis responded fastest to con-specific bees in the alert and feeding position, and female L. littoralis responded fastest to A. mellifera bees in the feeding position. A. mellifera reacted fastest to their con-specific bees in the alert and horizontal body positions. Our results demonstrate, for the first time in bees, that the position of individuals on a floral resource provides important visual information that modulates bee behavior, and illuminates aspects that likely have implications for bees in access to floral resources.

An explicit signature of balancing selection for color-vision variation in new world monkeys.

Color vision is an important characteristic of primates and, intriguingly, Neotropical monkeys are highly polymorphic for this trait. Recent field studies have challenged the conventional view that trichromatic color vision is more adaptive than dichromatic color vision. No study has investigated the pattern of genetic variation in the long to middle wavelength-sensitive (L-M or red-green) opsin gene as compared with that of other genomic regions (neutral references) in wild populations of New World monkeys to look for the signature of natural selection. Here, we report such a study conducted on spider monkeys and capuchin monkeys inhabiting Santa Rosa National Park, Costa Rica. The nucleotide sequence of the L-M opsin gene was more polymorphic than the sequences of the neutral references, although the opsin-gene sequences were not more divergent between the two species than were the sequences of the neutral references. In a coalescence simulation that took into account the observed nucleotide diversity of the neutral references, the Tajima's D value of the L-M opsin gene deviated significantly in a positive direction from the expected range. These results are the first to statistically demonstrate balancing selection acting on the polymorphic L-M opsin gene of New World monkeys. Taking the results of behavioral and genetic studies together, the balancing selection we detected may indicate that coexistence of different color-vision types in the same population, also characteristic of humans, is adaptive.

There is no other monkey in the mirror for spider monkeys (Ateles geoffroyi).

Mirror self-recognition (MSR), usually considered a marker of self-awareness, occurs in several species and may reflect a capacity that has evolved in small incremental steps. In line with research on human development and building on previous research adopting a gradualist framework, we categorized the initial mirror responses of naïve spider monkeys (Ateles geoffroyi) according to four levels. We compared social, exploratory, contingent and self-exploratory responses to a mirror and faux mirror during three short trials. If spider monkeys respond as most monkey species, we predicted they would perform at level 0, mainly showing social behavior toward their mirror-image. However, because spider monkeys show enhancement of certain cognitive skills comparable to those of great ape species, we predicted that they would perform at level 1a (showing exploratory behavior) or 1b (showing contingent behavior). GLMMs revealed that monkeys looked behind and visually inspected the mirror significantly more in the mirror than the faux mirror condition. Although the monkeys engaged in contingent body movements at the mirror, this trend was not significant. Strikingly, they showed no social behaviors toward their mirror-image. We also measured self-scratching as an indicator of anxiety and found no differences in frequencies of self-scratching between conditions. Therefore, in contrast to most findings on other species, spider monkeys did not treat their image as another monkey during their initial exposure to the mirror. In fact, they reached at least level 1a within minutes of mirror exposure. These responses recommend spider monkeys as good candidates for further explorations into monkey self-recognition. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Differential impact of severe drought on infant mortality in two sympatric neotropical primates.

Extreme climate events can have important consequences for the dynamics of natural populations, and severe droughts are predicted to become more common and intense due to climate change. We analysed infant mortality in relation to drought in two primate species (white-faced capuchins, Cebus capucinus imitator, and Geoffroy's spider monkeys, Ateles geoffroyi) in a tropical dry forest in northwestern Costa Rica. Our survival analyses combine several rare and valuable long-term datasets, including long-term primate life-history, landscape-scale fruit abundance, food-tree mortality, and climate conditions. Infant capuchins showed a threshold mortality response to drought, with exceptionally high mortality during a period of intense drought, but not during periods of moderate water shortage. By contrast, spider monkey females stopped reproducing during severe drought, and the mortality of infant spider monkeys peaked later during a period of low fruit abundance and high food-tree mortality linked to the drought. These divergent patterns implicate differing physiology, behaviour or associated factors in shaping species-specific drought responses. Our findings link predictions about the Earth's changing climate to environmental influences on primate mortality risk and thereby improve our understanding of how the increasing severity and frequency of droughts will affect the dynamics and conservation of wild primates.

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis).

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.

Development of heterosexual relationships in wied's black tufted-ear marmosets (Callithrix kuhli).

In tamarins and marmosets, long-term stable sociosexual relationships are formed between heterosexual adults, but these "monogamous" relationships are often formed in groups that contain multiple adults of both sexes. The patterning of interactions during pair formation may therefore be shaped by this demographic profile. We evaluated the development of sociosexual relationships in six captive pairs of Wied's black tufted-ear marmosets (Callithrix kuhli) during the 80 days from the initial day of pairing. Social behavior, sexual behavior and activity profiles were recorded. Social behaviors, including allogrooming, grooming solicitation, and intragroup monitoring calls, increased across the four 20-day time blocks. Males were more responsible than females for maintaining intrapair proximity during the first 40 days of pairing. Females and males were equally responsible for intrapair proximity maintenance after this time. The highest rates of sexual behavior, including copulation and proceptive open mouth displays, occurred upon pairing and then decreased non-significantly over time. The results indicate that sexual relationships in callitrichid primates are not dependent on the prior existence of a social relationship between males and females. Higher rates of copulation, greater male responsibility for proximity maintenance, and male initiative in sexual interactions early in pairing are consistent with a male reproductive strategy in which male-male competition may be common. © 1995 Wiley-Liss, Inc.