Reproductive physiology with emphasis on endometrial cycles of woolly and uakari monkeys-A literature review.

The ability of a species to withstand human impact depends on its life history characteristics, including social, ranging, and reproductive activity. The genera Lagothrix and Cacajao are more susceptible to anthropic action than small-sized primates due to their slower life histories, more restricted geographical ranges, and lower population densities. This narrative literature review aimed to gather scientific information available from the last 60 years on the reproductive biology of females of the genera Lagothrix and Cacajao. Most studies on the genus Lagothrix, mainly focused on L. lagothricha and L. l. poeppigii, present important advances on reproductive strategies, reproductive productivity, functional morphology and physiology, including seasonality, sexual cycle, gestation and fetal development in captive and free-living populations. Contrary, there is much less known about the reproductive biology of the genus Cacajao, with studies on free-living C. calvus and C. melanocephalus highlighting reproductive behavior, and basic description of the sexual cycle, gestation, and lactation. Unfortunately, the morphology of the female genital organs is only described in C. calvus, and there is still scarce information about the menstrual activity and the placenta. This literature review encourages primatologists, morphophysiologists, reproductive specialists, and ecologists to conduct comprehensive studies of these species to better understand the gaps in knowledge about reproduction, their relationship with their environment, including climatic and social variables. Understanding the integrative reproductive biology of these species will be a clue for improving the assessment of the resilience capacity of free-living populations and, consequently, establishing more appropriate management programs, and for the development of ex situ management techniques for the conservation of the species.

New bands in the sleep stages of spider monkeys (Ateles geoffroyi): Electroencephalographic correlations and spatial distribution.

The study of electroencephalographic (EEG) signals in nonhuman primates has led to important discoveries in neurophysiology and sleep behavior. Several studies have analyzed digital EEG data from primate species with prehensile tails, like the spider monkey, and principal component analysis has led to the identification of new EEG bands and their spatial distribution during sleep and wakefulness in these monkeys. However, the spatial location of the EEG correlations of these new bands during the sleep-wake cycle in the spider monkey has not yet been explored. Thus, the objective of this study was to determine the spatial distribution of EEG correlations in the new bands during wakefulness, rapid eye movement (REM) sleep, and non-REM sleep in this species. EEG signals were obtained from the scalp of six monkeys housed in experimental conditions in a laboratory setting. Regarding the 1-21 Hz band, a significant correlation between left frontal and central regions was recorded during non-REM 2 sleep. In the REM sleep, a significant correlation between these cortical areas was seen in two bands: 1-3 and 3-13 Hz. This reflects a modification of the degree of coupling between the cortical areas studied, associated with the distinct stages of sleep. The intrahemispheric EEG correlation found between left perceptual and motor regions during sleep in the spider monkey could indicate activation of a neural circuit for the processing of environmental information that plays a critical role in monitoring the danger of nocturnal predation.

Numerical cognition in black-handed spider monkeys (Ateles geoffroyi).

We assessed two aspects of numerical cognition in a group of nine captive spider monkeys (Ateles geoffroyi). Petri dishes with varying amounts of food were used to assess relative quantity discrimination, and boxes fitted with dotted cards were used to assess discrete number discrimination with equally-sized dots and various-sized dots, respectively. We found that all animals succeeded in all three tasks and, as a group, reached the learning criterion of 70% correct responses within 110 trials in the quantity discrimination task, 160 trials in the numerosity task with equally-sized dots, and 30 trials in the numerosity task with various-sized dots. In all three tasks, the animals displayed a significant correlation between performance in terms of success rate and task difficulty in terms of numerical similarity of the stimuli and thus a ratio effect. The spider monkeys performed clearly better compared to strepsirrhine, catarrhine, and other platyrrhine primates tested previously on both types of numerical cognition tasks and at the same level as chimpanzees, bonobos, and orangutans. Our results support the notion that ecological traits such as a high degree of frugivory and/or social traits such as a high degree of fission-fusion dynamics may underlie between-species differences in cognitive abilities.

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.

Wild robust capuchin monkey interactions with sympatric primates.

Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421 h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species' body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.

Monitoring the variation in the gut microbiota of captive woolly monkeys related to changes in diet during a reintroduction process.

Microbiome is known to play an important role in the health of organisms and different factors such as diet have been associated with modifications in microbial communities. Differences in the microbiota composition of wild and captive animals has been evaluated; however, variation during a reintroduction process in primates has never been reported. Our aim was to identify changes in the bacterial composition of three individuals of reintroduced woolly monkeys (Lagothrix lagothricha) and the variables associated with such changes. Fecal samples were collected and the V4 region of the 16S rRNA gene was sequenced to determine gut microbial composition and functionality. Individual samples from released individuals showed a higher microbial diversity after being released compared to before liberation, associated with changes in their diet. Beta diversity and functionality analysis showed separation of samples from released and captive conditions and the major factor of variation was the moment of liberation. This study shows that intestinal microbiota varies depending on site conditions and is mainly associated with diet diversity. The intake of food from wild origin by released primates may promote a positive effect on gut microbiota, improving health, and potentially increasing success in reintroduction processes.

Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador.

With their large body size and "slow" life histories, atelin primates are thought to follow a risk-averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species-white-bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)-in relation to habitat-wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high-levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year-round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk-averse breeding strategy.

Fruit availability has a complex relationship with fission-fusion dynamics in spider monkeys.

Understanding the ecological and social factors that influence group size is a major focus of primate behavioural ecology. Studies of species with fission-fusion social organizations have offered an insightful tool for understanding ecological drivers of group size as associations change over short temporal and spatial scales. Here we investigated how the fission-fusion dynamics of spider monkeys (Ateles geoffroyi) at Runaway Creek, Belize were affected by fruit availability. When males and females were analyzed together, we found no association between fruit availability and subgroup size. However, when females were analyzed separately, we found that when fruit availability increased, so did subgroup size. In all analyses, higher fruit availability did not influence subgroup spatial cohesion. Our results point to the complexity of understanding grouping patterns, in that while ecological factors make groups of specific sizes advantageous, social factors also play an important determining role.

Network analysis as a tool to understand social development in spider monkeys.

The emerging field of network science has demonstrated that an individual's connectedness within their social network has cascading effects to other dimensions of life. Like humans, spider monkeys live in societies with high fission-fusion dynamics, and are remarkably social. Social network analysis (SNA) is a powerful tool for quantifying connections that may vary as a function of initiating or receiving social behaviors, which has been described as shifting social roles. In primatology, the SNA literature is dominated by work in catarrhines, and has yet to be applied to the study of development in a platyrrhine model. Here, SNA was utilized in combination with R-Index social role calculation to characterize social interaction patterns in juvenile and adult Colombian spider monkeys (Ateles fusciceps rufiventris). Connections were examined across five behaviors: embrace, face-embrace, grooming, agonism, and tail-wrapping from 186 hr of observation and four network metrics. Mann-Whitney U tests were utilized to determine differences between adult and juvenile social network patterns for each behavior. Face-embrace emerged as the behavior with different network patterns for adults and juveniles for every network metric. With regard to social role, juveniles were receivers, not initiators, for embrace, face-embrace, and grooming (ps < .05). Network and social role differences are discussed in light of social development and aspects of the different behaviors.

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).

Correlation between musculoskeletal structure of the hand and primate locomotion: Morphometric and mechanical analysis in prehension using the cross- and triple-ratios.

Biometric ratios of the relative length of the rays in the hand have been analyzed between primate species in the light of their hand function or phylogeny. However, how relative lengths among phalanges are mechanically linked to the grasping function of primates with different locomotor behaviors remains unclear. To clarify this, we calculated cross and triple-ratios, which are related to the torque distribution, and the torque generation mode at different joint angles using the lengths of the phalanges and metacarpal bones in 52 primates belonging to 25 species. The torque exerted on the finger joint and traction force of the flexor tendons necessary for a cylindrical grip and a suspensory hand posture were calculated using the moment arm of flexor tendons measured on magnetic resonance images, and were compared among Hylobates spp., Ateles sp., and Papio hamadryas. Finally, the torques calculated from the model were validated by a mechanical study detecting the force exerted on the phalanx by pulling the digital flexor muscles during suspension in these three species. Canonical discriminant analysis of cross and triple-ratios classified primates almost in accordance with their current classification based on locomotor behavior. The traction force was markedly reduced with flexion of the MCP joint parallel to the torque in brachiating primates; this was notably lower in the terrestrial quadrupedal primates than in the arboreal primates at mild flexion. Our mechanical study supported these features in the torque and traction force generation efficiencies. Our results suggest that suspensory or terrestrial quadrupedal primates have hand structures that can exert more torque at a suspensory posture, or palmigrade and digitigrade locomotion, respectively. Furthermore, our study suggests availability of the cross and triple-ratios as one of the indicators to estimate the hand function from the skeletal structure.

Geophagy in the yellow-tailed woolly monkey (Lagothrix flavicauda) at La Esperanza, Peru: site characterization and soil composition.

Geophagy is the intentional consumption of soil and has been observed in various animal taxa including human and nonhuman primates. Among the numerous adaptive hypotheses proposed to explain this behavior, two of them stand out: soil either protects the gastrointestinal tract from secondary plant compounds, parasites and pathogens, and/or supplements micronutrients in the diet. Few studies have characterized the physical and chemical characteristics of soils consumed by nonhuman primates. Here, we describe the composition of soils consumed by yellow-tailed woolly monkeys (Lagothrix flavicauda) in comparison with soils taken from surrounding areas. We also studied the physical aspects of geophagy sites in terms of accessibility, dimensions and vegetation density. This study took place at the La Esperanza field site, in northern Peru, between 2016 and 2018. We conducted focal follows, placed camera traps at geophagy sites and sampled soils. In total, we recorded 77 geophagy events. Our results highlight some aspects of soil and site selection in these arboreal primates, who face an increased predation risk when descending to the ground. Animals preferred smaller sites with denser surrounding vegetation. Composition of consumed soils was similar between geophagy sites. Soils were poor in micronutrients, but contained around 20% clay. High clay content, coupled with the fact that geophagy was performed significantly more in the dry season, when leaf consumption is highest, lends support to geophagy as a mechanism for protection of the gastrointestinal tract in L. flavicauda.

Potential role in seed dispersal revealed by experimental trials with captive southern muriquis (Brachyteles arachnoides).

Primates are great fruit consumers and disperse intact seeds from most of the plants they consume, but effective seed dispersal depends, amongst other factors, on handling behavior. Likewise, the treatment in gut and mouth may alter seed fate. Overall, frugivore and folivore-frugivore primates are recognized to provide beneficial gut treatment for Neotropical plant species, but this effect might be overlooked at species-specific levels. In this study, we assessed the role of the southern muriqui (Brachyteles arachnoides), an endangered and endemic primate living in restricted fragments of the Brazilian Atlantic Forest, on potential quality of seed dispersal of native plants. Our main goals were to understand the effect of seed ingestion by this large-bodied atelid on germination of defecated seeds and in seed recovery by offering wild fruits of native species to captive individuals. We found that seven out of nine plant species were defecated intact and were able to germinate. Of those seven, one species showed enhanced and another showed decreased germination potential after defecation, while three species germinated faster after being defecated. The remaining species showed no differences from control seeds. The two non-germinating species were heavily predated, and average seed recovery was lower than expected, suggesting high levels of seed predation. The largest species offered (Inga vulpina) showed the highest dispersal potential. Our data support an overall neutral or potentially positive role of southern muriquis in seed dispersal quality for seven out of nine Atlantic Forest plant species, highlighting these primates' potential to produce an effective seed rain.

Habitat preference in the critically endangered yellow-tailed woolly monkey (Lagothrix flavicauda) at La Esperanza, Peru.

Habitat loss is one of the main threats to wildlife. Therefore, knowledge of habitat use and preference is essential for the design of conservation strategies and identification of priority sites for the protection of endangered species. The yellow-tailed woolly monkey (Lagothrix flavicauda Humboldt, 1812), categorized as Critically Endangered on the IUCN Red List, is endemic to montane forests in northern Peru where its habitat is greatly threatened. We assessed how habitat use and preference in L. flavicauda are linked to forest structure and composition. The study took place near La Esperanza, in the Amazonas region, Peru. Our objective was to identify characteristics of habitat most utilized by L. flavicauda to provide information that will be useful for the selection of priority sites for conservation measures. Using presence records collected from May 2013 to February 2014 for one group of L. flavicauda, we classified the study site into three different use zones: low-use, medium-use, and high-use. We assessed forest structure and composition for all use zones using 0.1 ha Gentry vegetation transects. Results show high levels of variation in plant species composition across the three use zones. Plants used as food resources had considerably greater density, dominance, and ecological importance in high-use zones. High-use zones presented similar structure to medium- and low-use zones; thus it remains difficult to assess the influence of forest structure on habitat preference. We recommend focusing conservation efforts on areas with a similar floristic composition to the high-use zones recorded in this study and suggest utilizing key alimentation species for reforestation efforts.

Testicular volume and semen characteristics in the endangered southern muriqui (Brachyteles arachnoides).

BACKGROUND: The southern muriqui (Brachyteles arachnoides) is an endangered Neotropical primate. Semen collection and description of its traits, as well as testicular morphometry, have never been reported for this species. METHODS: Testicles from five healthy adult captive southern muriqui were measured, and semen was collected by rectal probe electrostimulation (RPE). RESULTS AND CONCLUSIONS: A solid coagulum was identified in all ejaculates, and none of them liquefied, spontaneously or non-spontaneously. It was possible to collect semen using RPE, and although solids coagula did not liquefy, we managed to describe ejaculates characteristics and also confirmed that southern muriqui have relatively large testes size. Further investigations are needed to improve coagulum handling, to achieve a better spermatozoa recovery aiming its application in assisted reproductive technologies.

Influence of Arthropod and Fruit Abundance on the Dietary Composition of Highland Colombian Woolly Monkeys (Lagothrix lagotricha lugens).

The woolly monkey's (Lagothrix lagotricha) diet consists primarily of fruits, and for some populations fruit availability predicts its frequency in the diet. Woolly monkeys also eat new leaves, flowers, seeds and arthropods, but it is unclear whether arthropods are consumed in proportion to their environmental availability. We tested the hypothesis that arthropod consumption by woolly monkeys depends on availability. We studied a group of woolly monkeys for 10 months in 2013-2014, in Cueva de los Guácharos National Park, Colombia, in order to test the hypothesis that arthropod consumption by woolly monkeys depends on availability. We carried out surveys of plant phenology each month for 10 months to estimate fruit productivity, and every 2 months we also surveyed 3 canopy substrates (leaves, mosses and bromeliads) to quantify variation in arthropod biomass. During this time, we also quantified the diet of a woolly monkey group. The items most consumed were fruits (60%), followed by arthropods (24%), leaves (13%) and miscellaneous other items (3%). Arthropod biomass in the canopy did not vary considerably over the 10 months (0.014-0.037 g/g substrate) but was lower at the end of the second rainy season. A positive correlation was found between availability and entomophagy, but only when arthropods were relatively abundant. We did not find a relationship between arthropod and fruit feeding frequencies. Our results indicate that arthropods are prevalent in the diet of the woolly monkeys due to their abundance in Andean forest canopies.

Initiation of feeding by four sympatric Neotropical primates (Ateles belzebuth, Lagothrix lagotricha poeppigii, Plecturocebus (Callicebus) discolor, and Pithecia aequatorialis) in Amazonian Ecuador: Relationships to photic and ecological factors.

We examined photic and ecological factors related to initiation of feeding by four sympatric primates in the rain forest of Amazonian Ecuador. With rare exceptions, morning activities of all taxa began only after the onset of nautical twilight, which occurred 47-48 min before sunrise. The larger spider and woolly monkeys, Ateles belzebuth and Lagothrix lagotricha poeppigii, left their sleeping trees before sunrise about half the time, while the smaller sakis and titi monkeys, Pithecia aequatorialis and Plecturocebus (formerly Callicebus) discolor, did not emerge until sunrise or later. None of the four taxa routinely began feeding before sunrise. Pithecia began feeding a median 2.17 h after sunrise, at least 0.8 h later than the median feeding times of the other three taxa. The early movement of Ateles and Lagothrix, and late initiation of feeding by Pithecia are consistent with temporal niche partitioning. Among most New World primate species, all males and many females, have dichromatic color vision, with only two cone photopigments, while some females are trichromats with three cone photopigments. Current evidence indicates that the dichromats have a foraging advantage in dim light, which could facilitate utilization of twilight periods and contribute to temporal niche partitioning. However, in our study, dichromatic males did not differentially exploit the dim light of twilight, and times of first feeding bouts of female Ateles and Lagothrix were similar to those of males. First feeding bouts followed a seasonal pattern, occurring latest in May-August, when ripe fruit abundance and ambient temperature were both relatively low. The most frugivorous taxon, Ateles, exhibited the greatest seasonality, initiating feeding 1.4 h later in May-August than in January-April. This pattern may imply a strategy of conserving energy when ripe fruit is scarcer, but starting earlier to compete successfully when fruit is more abundant. Lower temperatures were associated with later feeding of Ateles (by 26 min / °C) and perhaps Pithecia, but not Lagothrix or Plecturocebus. The potential for modification of temporal activity patterns and temporal niche partitioning by relatively small changes in temperature should be considered when predicting the effects of climate change.

From the field to the lab: Muriqui endocrinology from a collaborative perspective.

The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life history of this species. However, nearly everything that is currently known about the northern muriqui's behavioral endocrinology has come from combining our respective expertise in noninvasive field and laboratory research. Here, we reflect on the history of our collaboration, focusing on major challenges, key scientific findings, and factors that contributed to its success. Challenges included insuring the reliable collection of frequent fecal samples from a large enough number of known individuals over extended periods of time, preserving the steroids in the field and transporting them, developing and validating the fecal steroid assays, and interpreting the hormonal profiles within the behavioral and ecological contexts of the study subjects. Major findings included our thorough description of the fecal progesterone and estradiol profiles associated with muriqui ovarian cycling and gestation, the seasonal resumption of cycling, its onset during puberty of dispersing females, and the differences between fertile and infertile cycles. We also documented the relationship between fecal cortisol and testosterone in sexually active males across breeding and nonbreeding seasons, and sex differences in cortisol levels across the mating and conception seasons. We attribute the success of our collaboration to a number of factors including our mutual appreciation for one another's high standards for ethics, data quality, and data interpretation.

Diel and infradian (7-day) activity rhythms in Mexican spider monkeys (Ateles geoffroyi) kept with and without visitor contact.

Diel activity rhythms in mammals are regulated by an endogenous (circadian) timing system which is synchronized by environmental 24-hr periodicities called zeitgebers. Additional direct responses to stochastic environmental factors ensure the fine-tuning to the actual situation and may mask the circadian time course. Following an observational study on behavioral effects of visitor activities in a group of spider monkeys (Ateles geoffroyi) kept free-ranging on a small island of Lake Catemaco, Veracruz, Mexico, we analyzed the effect of weekly varying numbers of visiting tourist boats on the monkeys' diel activity rhythm. With small accelerometer-data logger devices we recorded the monkeys' locomotor activity continuously for several months each. Then we compared the data with those from spider monkeys living without tourist contact. Neither the duration of the monkeys' activity time (α) nor its phase relationship to the 24-hr solar day did change on different weekdays in either site. However, their activity level showed a clear 7-day rhythm. The monkeys of the tourist site showed highest activity on Saturday and Sunday, when the frequency of visiting tourist boats was highest, whereas those of the non-tourist site were least active on Sunday and Monday, when human activities were lowest there. While the monkeys of the non-tourist site usually displayed a distinct bimodal activity pattern peaking in the morning and late afternoon, the pattern in those of the tourist site mostly lacked a morning peak and varied more over time. Based on our results, we suggest that circadian entrainment is not involved in the differences between the diel activity rhythms of the spider monkeys from the two keeping sites and the differing 7-day variation in their activity level. Rather, these differences seemingly reflect direct responses to the differing human activities and thus may correspond to circadian masking effects.

Seasonal and sex differences in the fission-fusion dynamics of spider monkeys (Ateles geoffroyi yucatanensis) in Belize.

Spider monkeys (Ateles sp.) are characterized by high fission-fusion dynamics, meaning their social grouping pattern is fluid and consists of subgroups that vary in size, composition, and spatial cohesion over time. In this study, we quantify the fission-fusion dynamics of a group of spider monkeys at Runaway Creek Nature Reserve in Belize by measuring subgroup size, spatial cohesion, and stability using data spanning 5 years. We then test whether variation in these three subgroup measures differ according to season, subgroup sex composition, and the reproductive status of female subgroup members. Our results show that subgroups were larger in size and less stable in membership during the wet season compared to the dry season. All-female subgroups were less spatially cohesive but more stable in membership than all-male subgroups. Finally, we report that subgroups with one or more non-lactating females (i.e., without nursing young) were smaller on average than subgroups containing lactating females with nursing young. These data contribute to a growing body of research documenting the ecological and social dimensions along which grouping patterns might vary.