TILETAMINE-ZOLAZEPAM-XYLAZINE ANESTHESIA IN EX SITU BLACK-HANDED SPIDER MONKEYS (ATELES GEOFFROYI SSP.).

Black-handed spider monkeys (Ateles geoffroyi ssp.) are endangered in Mexico. Safe anesthetic protocols are important for in situ and ex situ conservation problems. Such protocols are scarce in the literature; nor have safety and physiologic responses been reported. High doses and volume are a counter side for field immobilizations. We tested an anesthetic protocol with a combination of tiletamine-zolazepam (5 mg/kg) plus xylazine (1 mg/kg) in 14 black-handed spider monkeys under human care from two facilities in Mexico. Physiological parameters such as HR, RR, T, SPO2, systolic arterial pressure (), diastolic arterial pressure (DAP), and median arterial pressure (MAP) were obtained. HR and RR decreased over time, but T increased significantly during the anesthetic time for the whole group; RR and T decreased for juveniles only. Variation between individuals was observed for HR, RR, and DAP. Volume reduction of drugs was achieved compared to previously reported anesthesia protocols. Induction time was fast (6.2 ± 10.4 min) and no tail prehension was seen. Recovery was prolonged (mean and SD). Physiologic parameters remained stable throughout. The protocol proved to be safe for the chemical immobilization of black-handed spider monkeys.

Let's not use it! A dynamic no-use zone between the home ranges of two spider monkey groups.

It is common that neighboring groups of the same species use some of the same areas, resulting in home-range overlap. Areas between the home ranges of neighboring groups not used by either group (no-use zone or NUZ) are rarely reported. Here, we report the existence of a NUZ between the home ranges of two Geoffroy's spider monkey groups, and examine its spatial changes over time and the ecological and behavioral underpinnings of such phenomenon. Although its size and location changed between 2017 and 2022, the NUZ was always present. We did not find any differences in the vegetation structure and composition between the NUZ and the ranging areas and in the monkeys' activity patterns between areas adjacent to the NUZ and the other parts of the ranging areas. The number of monkey vocalizations was lower and subgroup size was smaller (although the number of males did not differ) in areas adjacent to the NUZ than in the other parts of the ranging areas. Both changes possibly reflect the tendency to conceal their presence to the neighboring group. Our findings contribute to the understanding of primate space use and highlight the need to focus on the areas delimiting home ranges.

Gestural communication in wild spider monkeys (Ateles geoffroyi).

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy's spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals' gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients' attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

Analytical and biological validation of a noninvasive measurement of glucocorticoid metabolites in feces of Geoffroy's spider monkeys (Ateles geoffroyi).

We report on an analytical and biological validation of a commercial cortisol enzyme immunoassay (EIA) to measure glucocorticoids (GC) in feces of Geoffroy's spider monkeys (Ateles geoffroyi). Validation of endocrinological methods for each sample matrix and study species is crucial to establish that the methods produce reliable results. For the analytical validation of the EIA, we assessed parallelism, accuracy, and precision. We carried out a biological validation based on three well-studied GC patterns with the following predictions: (1) increased fecal GC metabolite (fGCM) concentrations after veterinary intervention; (2) increased fGCM concentrations during early morning hours; and (3) higher fGCM concentrations during gestation than in other female reproductive states. For the first prediction, we sampled feces of two zoo-housed females 2 days before, the day of, and 2 days after a veterinary intervention. For the second prediction, we analyzed 284 fecal samples collected from 12 wild males using a linear mixed model (LMM). For the third prediction, we analyzed 269 fecal samples of eight wild females using an LMM. Analytical validation revealed that the EIA showed parallelism, was accurate, and precise within each assay. However, there was elevated variation in between-assay precision. The biological validation supported all predictions: (1) the two zoo-housed females showed a substantial increase in fGCM concentrations 2.5 and 11 h after veterinary intervention; (2) there was a negative effect of sample collection time on fGCM concentrations (i.e., higher concentrations during early morning); (3) gestating females had significantly higher fGCM concentrations than lactating females. Thus, we analytically validated the commercial EIA and, despite between-assay variation, we were able to find three biologically relevant GC signals in captive and wild settings, and in males and females. We are therefore confident that the method can be used to noninvasively address behavioral endocrinology questions in Geoffroy's spider monkeys.

Vigilance has mainly a social function in a wild group of spider monkeys (Ateles geoffroyi).

Vigilance is a widespread behavior that allows individuals to socially acquire information and/or effectively detect potential risks posed by predators and conspecifics. In this study, we aimed to investigate how social factors (i.e., subgroup size, number of males and immatures in the subgroup, presence of fission and fusion events, subgroup activity), individual characteristics (i.e., sex, presence of dependent offspring) and possible vulnerability to predation (i.e., being in smaller subgroups or lower in the canopy) explain variation in vigilance behavior in a wild group of spider monkeys (Ateles geoffroyi). We collected vigilance data during focal samples of all adults, subadults and juveniles of the group (N = 38), and ran generalized linear mixed models with a Bayesian approach. We found that the proportion of time both sexes spent in vigilance increased with subgroup size and during fusion events. Individuals also spent more time in vigilance when the subgroup was resting or socializing compared to other activities. Moreover, the proportion of time spent in vigilance increased in subgroups with more immatures. An alternative model with similar fit suggested that the proportion of time spent in vigilance increased in females when subgroups included more adult and subadult males. Overall, these results suggest that our study group mainly directed vigilance toward conspecifics (i.e., social vigilance), probably as a result of the relatively low predation pressure experienced, and contribute to the understanding of the multiple social factors affecting vigilance in group-living primates.

Primate richness and abundance is driven by both forest structure and conservation scenario in Costa Rica.

Variation in tropical forest management directly affects biodiversity and provisioning of ecosystem services on a global scale, thus it is necessary to compare forests under different conservation approaches such as protected areas, payments for ecosystem services programs (PES), and ecotourism, as well as forests lacking any formal conservation plan. To examine the effectiveness of specific conservation approaches, we examined differences in forest structure and tree recruitment, including canopy cover; canopy height; seedling, sapling, and adult tree density; and average and total diameter at breast height (DBH) across 78 plots in 18 forests across Costa Rica representing protected areas, private forests utilizing PES and/or ecotourism, and private forests not utilizing these economic incentives. The effectiveness of conservation approaches in providing suitable primate habitat was assessed by conducting broad primate census surveys across a subset of eight forests to determine species richness and group encounter rate of three primate species: mantled howler monkey (Alouatta palliata), Central American spider monkey (Ateles geoffroyi), and the white-faced capuchin monkey (Cebus imitator). Only canopy height was significantly different across the three approaches, with protected areas conserving the tallest and likely oldest forests. Canopy height was also significantly associated with the group encounter rate for both mantled howler and spider monkeys, but not for capuchins. Total group encounter rate for all three monkey species combined was higher in incentivized forests than in protected areas, with capuchin and howler monkey group encounter rates driving the trend. Group encounter rate for spider monkeys was higher in protected areas than in incentivized forests. Incentivized conservation (PES and ecotourism) and protected areas are paragons of land management practices that can lead to variation in forest structure across a landscape, which not only protect primate communities, but support the dietary ecologies of sympatric primate 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.

Yawning and scratching contagion in wild spider monkeys (Ateles geoffroyi).

Behavioural contagion is a widespread phenomenon in animal species, which is thought to promote coordination and group cohesion. Among non-human primates, however, there is no evidence of behavioural contagion in Platyrrhines (i.e. primates from South and Central America) yet. Here, we investigated whether behavioural contagion is also present in this taxon, by assessing yawning and scratching contagion in a wild group (N = 49) of Geoffroy's spider monkeys (Ateles geoffroyi). We conducted focal samples to examine whether individuals observing the triggering event (i.e. a naturally occurring yawning or scratching event in the group) would be more likely to yawn or scratch in the following 3 min, as compared to individuals who did not observe the triggering event. We ran generalized linear mixed models using a Bayesian approach, and found that the probability of yawning and scratching was higher for individuals observing others yawning and scratching, respectively, as compared to individuals who did not observe such an event. Behavioural contagion did not vary depending on the observer's sex, kinship or relationship quality with the individual performing the triggering event. These findings provide the first evidence for yawning and scratching contagion in a wild group of spider monkeys, and importantly contribute to the debate about the evolutionary origins of behavioural contagion in primates.

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

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

Automated acoustic detection of Geoffroy's spider monkey highlights tipping points of human disturbance.

As more land is altered by human activity and more species become at risk of extinction, it is essential that we understand the requirements for conserving threatened species across human-modified landscapes. Owing to their rarity and often sparse distributions, threatened species can be difficult to study and efficient methods to sample them across wide temporal and spatial scales have been lacking. Passive acoustic monitoring (PAM) is increasingly recognized as an efficient method for collecting data on vocal species; however, the development of automated species detectors required to analyse large amounts of acoustic data is not keeping pace. Here, we collected 35 805 h of acoustic data across 341 sites in a region over 1000 km2 to show that PAM, together with a newly developed automated detector, is able to successfully detect the endangered Geoffroy's spider monkey (Ateles geoffroyi), allowing us to show that Geoffroy's spider monkey was absent below a threshold of 80% forest cover and within 1 km of primary paved roads and occurred equally in old growth and secondary forests. We discuss how this methodology circumvents many of the existing issues in traditional sampling methods and can be highly successful in the study of vocally rare or threatened species. Our results provide tools and knowledge for setting targets and developing conservation strategies for the protection of Geoffroy's spider monkey.

Convergence between G and g in three monkey species (Sapajus spp, Ateles geoffroyi, and Macaca fascicularis).

An open question in comparative psychology is whether the source of correlations among different measures of ability (the g factor) is shared between species, or is distinct. This is examined using data on the performance of three monkey species (tufted capuchins, black-handed spider monkeys, and long-tailed macaques) on 16 cognitive ability measures. The differences between species pairs across measures are not generally strongly related to the degree to which the g factor loads on each subtest. Iteratively removing the subtests with the lowest coefficients of variance (CV), and recorrelating the species differences with subtest g-loadings was found to increase the association between the two. Across iterations, subtest pooled CV strongly and positively predicts the increase in the degree to which g-loadings are predictive of species difference in two comparisons, but is a weaker predictor in the comparison between tufted capuchins and black-handed spider monkeys. These associations were not related to phylogenetic distance but were very strongly related to species differences in the means of certain ecological factors. g-scores computed for each species on the basis of the three subtests with the highest CV values exhibited very-high magnitude (>.9) associations with species-level G-scores. G is simply the species-level equivalent of g, resulting from covariation among cognitive ability measures at the level of species differences. Finally, as with previous studies, subtests that show the greatest species differences seem to draw on executive functioning, and attention, suggesting that these may be a phylogenetically conserved source of g across many animal taxa. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Estimating the impact of the illegal trade of primates in Mexico: a potential threat to wildlife.

The primates of Mexico, Ateles geoffroyi, Alouatta palliata, and Alouatta pigra, are seriously threatened by habitat loss, fragmentation, and illegal hunting and trade. Very little is known about the extent of illegal trade and its impacts on declining primate populations. Our study proposes a potential method based on estimating the number of individuals that die in the trade before being detected and those that probably cannot be detected. This facilitates estimating the number of animals extracted and allows an assessment of how trafficking impacts their populations. We derive estimates from seizure data of primates in Mexico between 2010 and 2019. To do this, we created wildlife detection rates and mortality rates from the existing literature (scientific articles, journalistic articles, and notes) to estimate the number of primates that die during capture, transport, and sale and the number of trafficked primates that were not detected by Mexican authorities. We estimate that 946 primates were removed from the wild for the pet trade each year (spider monkey Ateles geoffroyi = 854; black howler monkeys Alouatta pigra = 38, mantled howler monkey Alouatta palliata = 54). The annual reduction in population size caused by trafficking was greatest for Ateles geoffroyi (2.2%), followed by Alouatta pigra (1.3%), and Alouatta palliata (0.4%). Our estimates show the percentage of impacts that trafficking has on Mexican primate populations. Nevertheless, trade has the potential to impact declining populations and still must be addressed.

Influence of tannic acid concentration on the physicochemical characteristics of saliva of spider monkeys (Ateles geoffroyi).

Tannins are a chemical defense mechanism of plants consumed by herbivores. Variations in salivary physicochemical characteristics such as pH, total protein concentration (TP), and presence of proline-rich proteins (PRPs) in animals have been reported as a mechanism to protect the oral cavity when consuming food with variations in pH and tannins. Variations in salivary physiochemistry as adaptations for consuming tannin-rich foods have been found in omnivorous and folivorous primates, but have not yet been reported in frugivorous species such as spider monkeys. We therefore assessed changes in pH using test strips, TP concentration by measuring absorbance at 595 nm in a spectrophotometer and salivary PRPs using the SDS-PAGE electrophoresis technique in the saliva of nine captive spider monkeys in response to the consumption of solutions with different concentrations of tannic acid. The results showed variations in pH, TP concentration and the presence and variation of possible salivary PRPs associated with tannic acid concentration. These findings suggest that spider monkeys may tailor their salivary physicochemical characteristics in response to the ingestion of potentially toxic compounds.

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).

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.

HEMATOLOGIC REFERENCE INTEVALS FOR SPIDER MONKEYS (ATELES GEOFFROYI) IN MANAGED CARE WITH RESPECT TO SEX AND AGE.

The determination of health status in spider monkeys (Ateles geoffroyi) that are held in managed care requires periodic evaluation. The present study obtained baseline data on hematologic values, body weight, and length in A. geoffroyi. A total of 118 individuals from three housing centers were included in the study and grouped into two categories by age (92 adults, 26 juveniles) and sex (46 males, 72 females). Body weight, red blood cell (RBC) counts, and hemoglobin counts were significantly higher in adult males than in adult females. No differences in length were found between sex and age groups. The present findings indicate that hematologic values by age and sex in A. geoffroyi are similar to those reported in other spider monkey populations in both managed care and the wild. These results will be useful as a reference for young individuals and adults in future studies of the health of this species.

Anxiety in Geoffroy's spider monkeys (Ateles geoffroyi): Can scratching be used as an indicator?

Self-directed behavior, such as self-scratching (hereafter, scratching), occurs in several taxa across the animal kingdom, including nonhuman primates. There is substantial evidence that scratching is an indicator of anxiety-like emotions in a variety of nonhuman primate species. Despite its importance as a window into emotional states, few studies have investigated scratching in Platyrrhines. We investigated scratching patterns of 24 Geoffroy's spider monkeys (Ateles geoffroyi) belonging to a group living in the Otoch Ma'ax Yetel Kooh protected area in the Yucatàn peninsula (Mexico). We assessed whether scratching could be used as an indicator of anxiety levels in this species by testing predictions based on contexts and behaviors associated with risk and uncertainty. We found no effect of the subject's sex and age, subgroup size, male presence, and the occurrence of fusions between subgroups on scratching rates. Similarly, we found no effect of infant proximity on their mother's scratching rates. Supporting our prediction, we found evidence that isolation from conspecifics affected scratching rates as individuals scratched more frequently the more time they spent isolated. Being in proximity with a partner with a relationship characterized by uncertainty affected scratching rates as individuals scratched more frequently when in proximity with a partner with whom they engaged in embraces (an indicator of uncertainty) than when in proximity with a partner with whom they did not exchange embraces. Our study provides insight into the factors affecting scratching in Geoffroy's spider monkeys, suggesting that scratching may indicate anxiety in this species at least in some contexts and thus opening a window into the emotional experience of another Platyrrhine monkey species.

Presence and potential distribution of malaria-infected New World primates of Costa Rica.

BACKGROUND: In South and Central America, Plasmodium malariae/Plasmodium brasilianum, Plasmodium vivax, Plasmodium simium, and Plasmodium falciparum has been reported in New World primates (NWP). Specifically in Costa Rica, the presence of monkeys positive to P. malariae/P brasilianum has been identified in both captivity and in the wild. The aim of the present study was to determine the presence of P. brasilianum, P. falciparum, and P. vivax, and the potential distribution of these parasites-infecting NWP from Costa Rica. METHODS: The locations with PCR (Polymerase Chain Reaction) positive results and bioclimatic predictors were used to construct ecological niche models based on a modelling environment that uses the Maxent algorithm, named kuenm, capable to manage diverse settings to better estimate the potential distributions and uncertainty indices of the potential distribution. RESULTS: PCR analysis for the Plasmodium presence was conducted in 384 samples of four primates (Howler monkey [n = 130], White-face monkey [n = 132], Squirrel monkey [n = 50], and red spider monkey [n = 72]), from across Costa Rica. Three Plasmodium species were detected in all primate species (P. falciparum, P. malariae/P. brasilianum, and P. vivax). Overall, the infection prevalence was 8.9%, but each Plasmodium species ranged 2.1-3.4%. The niche model approach showed that the Pacific and the Atlantic coastal regions of Costa Rica presented suitable climatic conditions for parasite infections. However, the central pacific coast has a more trustable prediction for malaria in primates. CONCLUSIONS: The results indicate that the regions with higher suitability for Plasmodium transmission in NWP coincide with regions where most human cases have been reported. These regions were also previously identified as areas with high suitability for vector species, suggesting that enzootic and epizootic cycles occur.

Molecular evidence of Leishmania spp. in spider monkeys (Ateles geoffroyi) from The Tuxtlas Biosphere Reserve, Veracruz, Mexico.

The black-handed spider monkey (Ateles geoffroyi) is a platyrrhine primate distributed in southern Mexico, Central America, and part of South America. Two subspecies inhabit Mexico: Ateles geoffroyi vellerosus and Ateles geoffroyi yucatanensis, both threatened with extinction. Serological evidence of exposure of spider monkeys to various groups of parasites such as Trypanosoma cruzi in México and Leishmania spp. in Brazil has been reported. The genus Leishmania encompasses about 23 species of flagellate protozoa that are transmitted by the bite of females of Phlebotominae sand flies. These parasites cause a zoonotic disease called leishmaniasis, which generates skin, mucocutaneous and/or visceral manifestations. The aim of the present study was to demonstrate the presence of Leishmania sp. in spider monkeys from the Tuxtlas Biosphere Reserve, Veracruz, Mexico. Blood samples from 10 free- ranging specimens of A. geoffroyi yucatanensis and 11 specimens in captivity of A. geoffroyi vellerosus were collected and used. The samples were subjected to a conventional Polymerase Chain Reaction test for the identification of a 116 bp fragment of a region from the kinetoplast minicircle of the parasite. Our analyzes showed that 71.4% of the sampled animals had fragment sizes compatible with Leishmania spp. The implications involve the survival of the specimens and the possibility that these primates act as sentinels of the disease. Furthermore, it is the first report suggesting the presence of Leishmania spp. in A. geoffroyi vellerosus and A. geoffroyi yucatanensis in Veracruz, Mexico.

Factors in forgetting in spider monkeys, Ateles geoffroyi.

This essay discusses current problems and factors with memory testing in spider monkeys. (PsycInfo Database Record (c) 2021 APA, all rights reserved).