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Filariae are parasitic nematodes of high veterinary and medical importance, responsible for some acute tropical diseases. They are transmitted through the bite of hematophagous vectors such as biting midges and blackflies. Filariae are among the most prevalent vector-borne parasitoses in Neotropical primates in which severe infections can cause inflammatory reactions and tissue damage. Given the location inside the host (peritoneal cavity, bloodstream, and lymphatics), the detection of filariid nematodes is challenging and is mostly postmortem; hence the scarcity of studies on the prevalence of filariae in wild primate populations. Here, we report the prevalence of filariid infections in free-ranging populations of Geoffroy's spider (Ateles geoffroyi) and black howler (Alouatta pigra) monkeys across southern Mexico, using a combination of noninvasive sampling and molecular diagnostic techniques. Fecal samples were screened for filariid DNA by qPCR protocols. A total of 88 samples were examined with an overall prevalence of 26%. Filariae were slightly more common in spider monkeys compared to howler monkeys. This study constitutes the first report of the prevalence of infection of filariid nematodes in populations of wild spider monkey across southern Mexico, and the first reporting of filariae in black howler monkeys, as part of a new era of primate parasitology and the diagnostics of parasite infections in light of the everyday more affordable molecular tools.
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In May and June 2024, a die-off of Mexican mantled howler monkeys (Alouatta palliata mexicana) occurred in southern Mexico. This commentary documents the event, attributing it to extreme heatwaves, drought, wildfires, and habitat impoverishment. Despite their reported resilience to habitat disturbances, mantled howler monkey mortality rate in some areas reached 31%. Key evidence points to heatstroke as the primary cause of death, exacerbated by limited hydration and reduced dietary diversity in disturbed habitats. Immediate responses included community-led rescues (e.g., hydrating the monkeys), coordination of rescue activities by nongovernmental organizations (NGOs) (e.g., managing donations), involvement of scientists (e.g., monitoring of primate populations), and assistance from government officials (e.g., providing legal support for animal management). This event underscores the urgency of developing action plans to prevent and attend future crises. Among other actions, we highlight (i) establishing primate care infrastructure with medical and rehabilitation centers; (ii) developing protocols and training programs to ensure rapid crisis response; (iii) fostering collaboration among government, NGOs, and academic institutions for effective crisis management; and (iv) developing targeted research on climate change impacts, predictive models, and long-term health monitoring. We emphasize the critical need for coordinated conservation efforts to protect wild primates and maintain natural ecosystem resilience in the face of escalating climate challenges.
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Geoffroy's spider monkeys, an endangered, fast-moving arboreal primate species with a large home range and a high degree of fission-fusion dynamics, are challenging to survey in their natural habitats. Our objective was to evaluate how different flight parameters affect the detectability of spider monkeys in videos recorded by a drone equipped with a thermal infrared camera and examine the level of agreement between coders. We used generalized linear mixed models to evaluate the impact of flight speed (2, 4, 6 m/s), flight height (40, 50 m above ground level), and camera angle (-45°, -90°) on spider monkey counts in a closed-canopy forest in the Yucatan Peninsula, Mexico. Our results indicate that none of the three flight parameters affected the number of detected spider monkeys. Agreement between coders was "substantial" (Fleiss' kappa coefficient = 0.61-0.80) in most cases for high thermal-contrast zones. Our study contributes to the development of standardized flight protocols, which are essential to obtain accurate data on the presence and abundance of wild populations. Based on our results, we recommend performing drone surveys for spider monkeys and other medium-sized arboreal mammals with a small commercial drone at a 4 m/s speed, 15 m above canopy height, and with a -90° camera angle. However, these recommendations may vary depending on the size and noise level produced by the drone model.
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Atelinae , Bosques , Rayos Infrarrojos , Animales , Atelinae/fisiología , Aeronaves , México , Ecosistema , Grabación en Video/métodos , Vuelo Animal/fisiologíaRESUMEN
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.
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Ateles geoffroyi , Atelinae , Masculino , Animales , Fenómenos de Retorno al Lugar HabitualRESUMEN
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.
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Ateles geoffroyi , Glucocorticoides , Masculino , Animales , Femenino , Glucocorticoides/metabolismo , Lactancia , Hidrocortisona , HecesRESUMEN
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).
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Ateles geoffroyi , Atelinae , Femenino , Animales , Humanos , Madres , MéxicoRESUMEN
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'.
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Atelinae , Conducta Social , Animales , Comunicación , Relaciones Interpersonales , Primates/psicología , Estructura SocialRESUMEN
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.
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Atelinae , Animales , Femenino , Aseo Animal , Fenómenos de Retorno al Lugar Habitual , Masculino , Conducta Social , Interacción SocialRESUMEN
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.
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Ansiedad , Ateles geoffroyi , Animales , Ansiedad/diagnóstico , Ateles geoffroyi/psicología , Femenino , Masculino , MéxicoRESUMEN
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.
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Atelinae , Animales , México , Conducta SocialRESUMEN
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.
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Sequías , El Niño Oscilación del Sur , Costa Rica , Bosques , Hojas de la Planta , Clima TropicalRESUMEN
Network analysis has increasingly expanded our understanding of social structure in primates and other animal species. However, most studies use networks representing only one interaction type, when social relationships (and the emerging social structure) are the result of many types of interactions and their interplay through time. The recent development of tools facilitating the integrated analysis of multiple interaction types using multiplex networks has opened the possibility of extending the insight provided by social network analysis. We use a multiplex representation of interactions among the members of a group of wild Geoffroy's spider monkeys (Ateles geoffroyi), to study their social structure. We constructed a six-layered multiplex network based on three indices of overt social interactions (aggression, embraces, grooming) and three distance-based indices (contact, proximity, and association). With tools provided by the MuxViz software, we assessed the relevance of including all six indices in our analysis, the role of individuals in the network (through node versatility), and the presence of modules and non-random triadic structures or motifs. The multiplex provided information which was not equivalent to any individual layer or to the simple aggregation of layers. Network patterns based on associations did not correspond with those observed for overt-interactions or for the multiplex structure. Males were the most versatile individuals, while multiplex modularity and motifs highlighted the relevance of different interaction types for the overall connectivity of the network. We conclude that the multiplex approach improves on previous methods by retaining valuable information from each interaction type and how it is patterned among individuals.
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Agresión/psicología , Atelinae , Aseo Animal , Conducta Social , Red Social , Animales , Femenino , Masculino , Programas InformáticosRESUMEN
Patterns of genetic variation among populations can reveal the evolutionary history of species. Pinworm parasites are highly host specific and form strong co-evolutionary associations with their primate hosts. Here, we describe the genetic variation observed in four Trypanoxyuris species infecting different howler and spider monkey subspecies in Central America to determine if historical dispersal processes and speciation in the host could explain the genetic patterns observed in the parasites. Mitochondrial (cox1) and ribosomal (28S) DNA were analysed to assess genetic divergence and phylogenetic history of these parasites. Sequences of the 28S gene were identical within pinworms species regardless of host subspecies. However, phylogenetic analyses, haplotype relationships and genetic divergence with cox1 showed differentiation between pinworm populations according to host subspecies in three of the four Trypanoxyuris species analysed. Haplotype separation between host subspecies was not observed in Trypanoxyuris minutus, nor in Trypanoxyuris atelis from Ateles geoffoyi vellerosus and Ateles geoffoyi yucatanensis. Levels of genetic diversity and divergence in these parasites relate with such estimates reported for their hosts. This study shows how genetic patterns uncovered in parasitic organisms can reflect the host phylogenetic and biogeographic histories.
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Alouatta/parasitología , Ateles geoffroyi/parasitología , Evolución Biológica , Variación Genética , Interacciones Huésped-Parásitos , Oxyuroidea/genética , Animales , Costa Rica , Femenino , Masculino , México , Enfermedades de los Monos/parasitología , Nicaragua , Oxiuriasis/parasitología , Oxiuriasis/veterinaria , FilogeografíaRESUMEN
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.
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Atelinae , Cadena Alimentaria , Conducta Predatoria , Puma/fisiología , Animales , Femenino , MéxicoRESUMEN
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.
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Atelinae/fisiología , Pan troglodytes/fisiología , Conducta Social , Theropithecus/fisiología , Animales , Conducta Animal , IncertidumbreRESUMEN
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.
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Atelinae/fisiología , Movimiento , Proyectos de Investigación , Conducta Social , Animales , Femenino , Masculino , México , Densidad de PoblaciónRESUMEN
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.
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Atelinae/fisiología , Conducta Animal , Fenómenos de Retorno al Lugar Habitual , Conducta Social , Animales , Costa Rica , Ecosistema , Conducta Alimentaria , Femenino , Factores de TiempoRESUMEN
Animal home ranges may vary little in their size and location in the short term but nevertheless show more variability in the long term. We evaluated the degree of site fidelity of two groups of spider monkeys (Ateles geoffroyi) over a 10- and 13-year period, respectively, in the northeastern Yucatan peninsula, Mexico. We used the Local Convex Hull method to estimate yearly home ranges and core areas (defined as the 60% probability contour) for the two groups. Home ranges varied from 7.7 to 49.6 ha and core areas varied from 3.1 to 9.2 ha. We evaluated the degree of site fidelity by quantifying the number of years in which different areas were used as either home ranges or core areas. Large tracts were used only as home ranges and only for a few years, whereas small areas were used as either core area or home range for the duration of the study. The sum of the yearly core areas coincided partially with the yearly home ranges, indicating that home ranges contain areas used intermittently. Home ranges, and especially core areas, contained a higher proportion of mature forest than the larger study site as a whole. Across years and only in one group, the size of core areas was positively correlated with the proportion of adult males in the group, while the size of home ranges was positively correlated with both the proportion of males and the number of tree species included in the diet. Our findings suggest that spider monkey home ranges are the result of a combination of long-term site fidelity and year-to-year use variation to enable exploration of new resources.
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Atelinae/fisiología , Conducta Alimentaria/fisiología , Fenómenos de Retorno al Lugar Habitual/fisiología , Animales , Atelinae/psicología , Dieta , Ecosistema , Femenino , Masculino , México , Densidad de Población , Dinámica Poblacional/tendencias , Árboles , Clima TropicalRESUMEN
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.
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Conducta de Elección , Matrimonio , Principios Morales , Parejas Sexuales , Femenino , Humanos , MasculinoRESUMEN
Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.