Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

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.

Correction to: Review of GPS collar deployments and performance on nonhuman primates.

In the original publication of the article, figure 1 was wrongly published as a duplication.

Review of GPS collar deployments and performance on nonhuman primates.

Over the past 20 years, GPS collars have emerged as powerful tools for the study of nonhuman primate (hereafter, "primate") movement ecology. As the size and cost of GPS collars have decreased and performance has improved, it is timely to review the use and success of GPS collar deployments on primates to date. Here we compile data on deployments and performance of GPS collars by brand and examine how these relate to characteristics of the primate species and field contexts in which they were deployed. The compiled results of 179 GPS collar deployments across 17 species by 16 research teams show these technologies can provide advantages, particularly in adding to the quality, quantity, and temporal span of data collection. However, aspects of this technology still require substantial improvement in order to make deployment on many primate species pragmatic economically. In particular, current limitations regarding battery lifespan relative to collar weight, the efficacy of remote drop-off mechanisms, and the ability to remotely retrieve data need to be addressed before the technology is likely to be widely adopted. Moreover, despite the increasing utility of GPS collars in the field, they remain substantially more expensive than VHF collars and tracking via handheld GPS units, and cost considerations of GPS collars may limit sample sizes and thereby the strength of inferences. Still, the overall high quality and quantity of data obtained, combined with the reduced need for on-the-ground tracking by field personnel, may help defray the high equipment cost. We argue that primatologists armed with the information in this review have much to gain from the recent, substantial improvements in GPS collar technology.

Traditions in spider monkeys are biased towards the social domain.

Cross-site comparison studies of behavioral variation can provide evidence for traditions in wild species once ecological and genetic factors are excluded as causes for cross-site differences. These studies ensure behavior variants are considered within the context of a species' ecology and evolutionary adaptations. We examined wide-scale geographic variation in the behavior of spider monkeys (Ateles geoffroyi) across five long-term field sites in Central America using a well established ethnographic cross-site survey method. Spider monkeys possess a relatively rare social system with a high degree of fission-fusion dynamics, also typical of chimpanzees (Pan troglodytes) and humans (Homo sapiens). From the initial 62 behaviors surveyed 65% failed to meet the necessary criteria for traditions. The remaining 22 behaviors showed cross-site variation in occurrence ranging from absent through to customary, representing to our knowledge, the first documented cases of traditions in this taxon and only the second case of multiple traditions in a New World monkey species. Of the 22 behavioral variants recorded across all sites, on average 57% occurred in the social domain, 19% in food-related domains and 24% in other domains. This social bias contrasts with the food-related bias reported in great ape cross-site comparison studies and has implications for the evolution of human culture. No pattern of geographical radiation was found in relation to distance across sites. Our findings promote A. geoffroyi as a model species to investigate traditions with field and captive based experiments and emphasize the importance of the social domain for the study of animal traditions.

Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi).

I report three cases of coalitionary aggression by adult male black-handed spider monkeys (Ateles geoffroyi) against subadult males within their community on Barro Colorado Island (BCI), Panama. Two of these cases were followed by the disappearance and presumed death of the victim. Similar behavior was recently reported by Valero et al. [in press], who suggested that this behavior may be the result of intense male reproductive competition. Like the single instance they reported, the cases I report all occurred when the operational sex ratio was approximately 1:1, which suggests that intense competition among males for access to reproductively viable females may be a contributing factor. Additionally the very low density of spider monkeys on BCI may play a significant role in the occurrence of this lethal aggression. Large numbers of adult males are not necessary to protect a territorial boundary against neighboring groups, and additional males may act merely as mating competition.

Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi).

I report ad libitum data on 18 copulations involving free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama. All copulations were performed in a dorsoventral position, as is typically reported for this genus. Intromission often appeared difficult to achieve, possibly as a result of the large size of the glans penis in these animals. The average length from intromission to termination of thrusting exceeded 17 min, followed by an average period of almost 2 min before separation occurred, which suggests the possibility of a copulatory lock. Offspring of the female participant were almost always in close proximity to or in contact with the pair, and harassment by the offspring was observed only during the final stages of the copulation. All but one copulatory event occurred in complete seclusion from other adult males, and sexual behavior was not limited to any one adult male in the group.

Patterns of behavior across reproductive states of free-ranging female black-handed spider monkeys (Ateles geoffroyi).

Reports on the behavior of spider monkeys (genus Ateles) describe a suite of 5-6 behaviors that are indicative of an estrous female. This study presents hormonal data as an independent measure of reproductive state to determine if these behaviors are associated with any particular reproductive state or stage of the ovarian cycle. Fecal samples collected from 6 free-ranging female black-handed spider monkeys (Ateles geoffroyi) over the course of 11 months were assayed for estrogen (E1C) and progesterone (PdG) metabolites, using an enzyme immunoassay. Behavioral data collected from the same females were analyzed for patterns associated with different reproductive states. A more detailed analysis of behavioral data associated with reproductively cycling periods determined whether each behavior clustered with copulations or a particular phase in the ovarian cycle. Observations of place-sniffing were more frequent for 4 of 5 females when reproductively cycling. Of all copulations observed, 80% occurred when the female participant was reproductively cycling. In addition, the rates of self-clitoral hold and self-clitoral rub behaviors were significantly higher for 2 of 4 and 4 of 5 of females, respectively, when reproductively cycling. No behavior consistently occurred in association with copulations or with any particular phase in the ovarian cycle. Results from this study suggest that the behaviors tested in this paper can provide some information regarding female spider monkey reproductive state (whether or not she is reproductively cycling), but that they are not indicators of estrus in female spider monkeys.