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Capuchin Monkey Research Priorities and Urgent Issues
Abstract
The "Capuchin research community roundtable: working together towards a comparative biology of Cebus and Sapajus" was held at the International Primatological Society Congress in Cancún, Mexico, August 2012. Goals of the roundtable were to strengthen interactions among the capuchin research community, and to prioritize and coordinate research and training in a more systematic and interactive way in light of increasing conservation urgency. New phylogenetic and biogeographic evidence highlights the distinct evolutionary histories of the two radiations of capuchin monkeys, Cebus (untufted or gracile capuchins) and Sapajus (tufted or robust capuchins), that were formerly lumped under Cebus, and points to a higher number of species, or Evolutionarily Significant Units, in each compared to past capuchin taxonomies. Many of the lesser-known species face increasing fragmentation and destruction of habitat, and most populations of still non-threatened species face encroachment from human settlements. Here, we present capuchin research priorities and urgent issues based on the discussion by capuchin researchers in the roundtable. These include a call for the immediate end to the use of the name Cebus apella and the employment of the term Sapajus spp. instead for captive robust capuchins of unknown origin; for the implementation of rapid assessments for previously unstudied capuchin species or populations in biomes of interest; for the development of standardized methods to allow for comparative analyses across capuchin field sites; and for the creation and maintenance of an open-access website for capuchin monkey data. Finally, we planned the creation of an international Capuchin Action Network, to help disseminate research information; to work as a research community in a more efficient, collaborative manner; to help prioritize research and conservation goals as a community of experts; and to strengthen our political voice. Am. J. Primatol. © 2014 Wiley Periodicals, Inc.
... This region has already been proposed as a priority area for research on Sapajus spp. (Lynch Alfaro et al. 2014). However, socioenvironmental conflicts added to difficulty of access prevent primate research and conservation in this region (Sampaio et al. 2017). ...
... The collection and publication of demographic data on capuchin monkey groups are considered of high importance to enable group and regional comparisons (Lynch Alfaro et al. 2014). What is known thus far is that population sizes and compositions of groups do not seem to differ greatly between Sapajus species (Fragaszy et al. 2004;Izar et al. 2012). ...
... We also emphasize that unpublished theses and dissertations are not included in international bibliometric search platforms, and are therefore usually absent from reviews such as ours. The findings of these works are, however, essential for advancing certain areas of knowledge (Lynch Alfaro et al. 2014), yet because of their regional nature along with a possible language barrier, and the fact that they are not included in indexes, they are not included in the core body of publications. ...
Knowledge of the feeding habits of primate species is important for an understanding of their natural history and ecological interactions between their groups, and their interactions with their environments. Capuchin monkeys (Sapajus spp.) present significant diet flexibility and are a good model for investigating diet diversity between species. We undertook a systematic literature review of publications on the diet of free-living Sapajus spp. groups by using the Web of Science platform. We performed scientometric analyses of the objectives and hypotheses of the reviewed works, identified knowledge gaps, and evaluated the composition of each group’s diet. Our results indicate geographic and taxonomic biases among the 59 published studies that we examined. The studies were focused on Sapajus nigritus, Sapajus libidinosus, and Sapajus apella, and undertaken in long-term study sites. Foraging and behavioral aspects of how food is processed were recurring themes. Capuchin monkeys increase their consumption of anthropogenic food according to its supply. Despite the similar objectives of these studies, standardized data collection protocols were not employed. Although Sapajus spp. are widely distributed and are used for cognitive studies, basic aspects of their natural history, such as their diet, remain unknown. We emphasize the importance of undertaking studies on this genus to fill the identified knowledge gaps, and propose that investigations should be carried out on the effects of dietary changes on individuals and groups. We stress that, as the Neotropical region is one of those most affected by anthropogenic impacts, opportunities to study these primates in their natural environments are diminishing daily.
... Argentina, while S. n. nigritus is restricted to Brazil, in the states of Minas Gerais, Espírito Santo, São Paulo and Rio de Janeiro (Lynch Alfaro et al. 2014). The wide distribution favors the intraspecific diversity reported for S. nigritus, be it phenotypic (Silva Jr. 2001;Vieira and Oliveira 2014), molecular (Ruiz-García et al. 2012;Martins-Junior et al. 2018) or cytogenetic (Freitas and Seuánez 1982;Matayoshi et al. 1987;Nieves et al. 2017). ...
... It has been emphasized that in order to understand the diversity within the species, studies are needed that include populations throughout the distribution, mainly in environments subjected to increasing fragmentation (Lynch Alfaro et al. 2014). Groups of capuchin monkeys inhabit the Ilha da Marambaia (Marambaia Island), Mangaratiba city, south of Rio de Janeiro state, Brazil. ...
... The coat coloration patterns and the shapes of the tufts on the top of the head observed in the individuals from Ilha da Marambaia correspond to that described for Sapajus nigritus nigritus (Groves 2001;Fragaszy et al. 2004;Rylands et al. 2005), which is consistent with the geographic origin in Rio de Janeiro state (Lynch Alfaro et al. 2014). The intrapopulation variation observed also corresponds to that described for S. nigritus in a population from São Paulo state, Brazil (Vieira and Oliveira 2014), although the reddish color on the belly and back and the white fur on the belly, described in that population, was not observed. ...
The black-horned capuchin (Sapajus nigritus) is a neotropical primate with wide distribution from southeastern Brazil to northeastern Argentina. Although this species has been described with coat pattern variation, even with intrapopulational differences, and characterized as having the greatest genetic diversity among Sapajus species, there are still few studies on natural populations that contribute to the knowledge of this intraspecific variability. We examined individuals from an as yet unstudied population of Ilha da Marambaia, Rio de Janeiro (RJ) state, Brazil, compared with published data for S. nigritus. We sought to confirm the species through phenotypic and genetic characterization using C-banding and fluorescence in situ hybridization with #11qHe+/21WCP probes for chromosomal constitutive heterochromatin (He+) patterns, and cytochrome c oxidase I and II gene sequences for phylogenetic analysis. The coat presented two color patterns, varying from brown to blackish on the body, yellow to brown on the chest, and white to yellow on the face, besides the presence and shape of the tufts on the head, corresponding to S. nigritus. He+ was identified in pairs 4, 12, 13 and 17, and less consistently in pairs 6, 19 and 21, already described for this species. While most Sapajus species have a large He+ block, here pair 11 was identified without extracentromeric He+, the same as reported for S. nigritus from Argentina. Molecular analysis showed divergence of this population from other S. nigritus sequences, reinforcing a trend already demonstrated when samples from RJ are compared with the rest of the distribution, which may represent an evolutionary deviation.
... Habitual use of tools, and stone tools in particular, is considered one of the defining behavioural differences between Cebus and Sapajus [45]. The near absence of tool use in gracile capuchins is puzzling as they are otherwise highly innovative [42] and have a wide array of social [46] and foraging traditions [35,47,48] which are socially learned [36,49]. ...
... It is also possible that differences in tool use rates might be influenced by ranging patterns. Gracile capuchins have larger home ranges than robust capuchins, on average (reviewed in [45,77]), and thus might be able to access a more diverse set of food items that do not require tool use compared to robust capuchins. However, it is also possible that groups of robust capuchins are just more capable of extracting resources out of a smaller area due to morphological specializations such as thicker enamel and larger molars [16]. ...
... imitator) from their Atlantic congeners (C. capucinus) [16,45,132]. ...
Habitual reliance on tool use is a marked behavioural difference between wild robust (genus Sapajus) and gracile (genus Cebus) capuchin monkeys. Despite being well studied and having a rich repertoire of social and extractive foraging traditions, Cebus sp. rarely use tools and have never been observed using stone tools. By contrast, habitual tool use by Sapajus is widespread. We review theory and discuss factors which might explain these differences in patterns of tool use between Cebus and Sapajus. We then report the first case of habitual stone tool use in a gracile capuchin: a population of white-faced capuchins (Cebus capucinus imitator) in Coiba National Park, Panama who habitually rely on hammerstone and anvil tool use to access structurally protected food items in coastal areas including Terminalia catappa seeds, hermit crabs, marine snails, terrestrial crabs and other items. This behaviour has persisted on one island in Coiba National Park since at least 2004. From 1 year of camera trapping, we found that stone tool use is strongly male-biased. Of the 205 camera trap days where tool use was recorded, adult females were never observed to use stone tools, although they were frequently recorded at the sites and engaged in scrounging behaviour. Stone tool use occurs year-round in this population; over half of all identifiable individuals were observed participating. At the most active tool use site, 83.2% of days where capuchins were sighted corresponded with tool use. Capuchins inhabiting the Coiba archipelago are highly terrestrial, under decreased predation pressure and potentially experience resource limitation compared to mainland populations—three conditions considered important for the evolution of stone tool use. White-faced capuchin tool use in Coiba National Park thus offers unique opportunities to explore the ecological drivers and evolutionary underpinnings of stone tool use in a comparative within- and between-species context.
... Ruiz-García et al. (2012) sugirieron que la mezcla de los haplogrupos se generó a partir de poblaciones pequeñas que inicialmente estaban sujetas a una intensa deriva genética durante la finalización del puente terrestre de Panamá y los cambios climáticos en el cuaternario; cuando poblaciones se expandieron y entremezclaron. Lynch et al. (2014) sugieren ser conservador en el sentido de no errar al dividir taxones en demasiadas especies/subespecies diferentes, ya que aún no se sabe lo suficiente sobre los monos capuchinos. Sin embargo, C. imitator es el más estudiado de este grupo en campo a corto y largo plazo, con una rica literatura sobre el comportamiento social y de alimentación, a diferencia de C. capucinus que carece de estudios de campo en Colombia (Lynch et al., 2014). ...
... Lynch et al. (2014) sugieren ser conservador en el sentido de no errar al dividir taxones en demasiadas especies/subespecies diferentes, ya que aún no se sabe lo suficiente sobre los monos capuchinos. Sin embargo, C. imitator es el más estudiado de este grupo en campo a corto y largo plazo, con una rica literatura sobre el comportamiento social y de alimentación, a diferencia de C. capucinus que carece de estudios de campo en Colombia (Lynch et al., 2014). Dicho esto, algunos estudios siguen reconociendo a C. capucinus para Centroamérica haciendo referencia a C. c. imitator (por ejemplo, Melin et al., 2017y Tinsley et al., 2020; en cambio otros autores aceptaron el cambio y reconocen a C. imitator (por ejemplo, Rodríguez-Herrera et al., 2014;Bernal-Valle et al., 2020y Pinel, 2020. ...
... The blond capuchin monkey (Sapajus flavius) is a critically endangered species that occupies Atlantic forest fragments in northeast Brazil (Oliveira and Langguth 2006; 1 3 IUCN 2015). The fragments are found in human-altered landscapes, and the matrix surrounding the forest patches is dominated by a sugarcane agroecosystem of industry plantations or by crops that are traditionally farmed (Lynch-Alfaro et al. 2014). The species has only approximately 2000 individuals left, with little data available regarding blond capuchin feeding habits, demography, or social dynamics. ...
... In their review of the conservation status of the genus, Lynch-Alfaro et al. (2014) list 53 sites where research on Cebus (17) and Sapajus (35) occurs. While human-monkey conflicts are registered in sites located near traditional crop areas (Siemers 2000;Sabbatini et al. 2008;McKinney 2011), major conflicts are not commonly described for fragments bordered by agroecosystems or stockbreeding activities (but see Pagno et al. 2015). ...
Shifting to fallback food (FBF) consumption and crop raiding are behavioral adjustments that support primates’ ability to endure in human-altered habitats. Nutritional models predict that the consumption of preferred foods leads to increased competition, while consumption of staple fallback foods results in decreased competition. We analyzed the competitive regime faced by individuals in a group of 133 blond capuchin monkeys (Sapajus flavius), an endangered species that inhabits a 270-ha fragment of Atlantic forest in northeast Brazil. During the study year, quantitative analyses show that fruits were a preferred food, while sugarcane was used as a staple FBF. As predicted by primate fallback foraging models, the consumption of sugarcane helped the group to survive in this fragment by providing these animals with half of the food they consumed throughout the year. Contrary to predictions, group dispersion increased with greater fruit abundance, while direct competition peaked during the consumption of sugarcane. We suggest that, although it is abundant and scattered in the area, the long handling time required to process sugarcane before consumption facilitates the direct competition. Overall, the pattern found indicates that consumption of a staple FBF does not directly translate into decreased competition and increased stability of social groups in forest fragments.
... La taxonomía del capuchino ecuatoriano desde mucho tiempo atrás ha sido controversial, por un lado el taxón ha sido tratado como una subespecie del complejo de Cebus albifrons (Hershkovitz 1949;Emmons & Albuja 1992;Albuja 2002;Ruiz-García 2010) y por otra parte como una especie distinta (Rylands & Mittermeier 2013;Lynch-Alfaro et al. 2014;Cervera et al. 2015;Cornejo & de la Torre 2015). De las 41 localidades de registro del capuchino ecuatoriano por lo menos en 10 del territorio ecuatoriano dejó de existir este primate, ya que en la actualidad son zonas con poblaciones humanas. ...
... Para la conservación de este primate será determinante la labor que se realicen en las áreas protegidas, tanto estatales como de los gobiernos autónomos descentralizados y las privadas, para el mejoramiento de las condiciones ecológicas de los bosques y el establecimiento posterior de la conectividad entre ellos. Las actividades enlistadas en la iniciativa de conservación propuesta por Lynch-Alfaro et al. (2014), la cual contempla acciones como las evaluaciones rápidas del capuchino ecuatoriano en áreas sin estudios previos o el estudio de las poblaciones en áreas de interés, el desarrollo de métodos estandarizados que permitan el análisis de las poblaciones en las diferentes áreas de distribución, la creación y mantenimiento de un acceso abierto a una página web para los datos de este primate y la creación de una red de acción internacional para la difusión de los resultados de las investigaciones del capuchino ecuatoriano, de ser implementadas seguramente tendrán resultados positivos para la conservación a largo plazo de este primate. ...
... Hybridization of capuchin species has been documented in the wild at geographic points of contact (Martins et al., 2017;Rylands et al., 2005) and in captivity (Lynch- Alfaro et al., 2014), particularly in Sapajus species. Hybridization can introduce variation in primate skull size and shape from parent to hybrid offspring as has been shown in baboons (Ackermann et al., 2006), macaques (Schillaci et al., 2005), T A B L E 2 Multivariate multiple regression results for three separate models to examine skull growth (size = age rank × genus), skull shape development (shape = age rank × genus), and ontogenetic allometry of skull shape (shape = size × genus) in Sapajus and Cebus. ...
The ontogeny of feeding is characterized by shifting functional demands concurrent with changes in craniofacial anatomy; relationships between these factors will look different in primates with disparate feeding behaviors during development. This study examines the ontogeny of skull morphology and jaw leverage in tufted ( Sapajus ) and untufted ( Cebus ) capuchin monkeys. Unlike Cebus , Sapajus have a mechanically challenging diet and behavioral observations of juvenile Sapajus suggest these foods are exploited early in development. Landmarks were placed on three‐dimensional surface models of an ontogenetic series of Sapajus and Cebus skulls ( n = 53) and used to generate shape data and jaw‐leverage estimates across the tooth row for three jaw‐closing muscles (temporalis, masseter, medial pterygoid) as well as a weighted combined estimate. Using geometric morphometric methods, we found that skull shape diverges early and shape is significantly different between Sapajus and Cebus throughout ontogeny. Additionally, jaw leverage varies with age and position on the tooth row and is greater in Sapajus compared to Cebus when calculated at the permanent dentition. We used two‐block partial least squares analyses to identify covariance between skull shape and each of our jaw muscle leverage estimates. Sapajus , but not Cebus , has significant covariance between all leverage estimates at the anterior dentition. Our findings show that Sapajus and Cebus exhibit distinct craniofacial morphologies early in ontogeny and strong covariance between leverage estimates and craniofacial shape in Sapajus . These results are consistent with prior behavioral and comparative work suggesting these differences are a function of selection for exploiting mechanically challenging foods in Sapajus , and further emphasize that these differences appear quite early in ontogeny. This research builds on prior work that has highlighted the importance of understanding ontogeny for interpreting adult morphology.
... Until the year 2012, all capuchin monkeys were identified as Cebus. Taxonomic revisions have since divided this group into two genera: Cebus and Sapajus (Lynch-Alfaro et al., 2012) but the name Cebus is sometimes still used for all capuchin species, including Sapajus species (Lynch-Alfaro et al., 2014). The form used for taxonomic identification of samples collected as part of the Brazilian national surveillance program has not been updated recently, and so Sapajus is not yet included on the form. ...
Epidemics have significant impacts on primate populations. In 2016, yellow fever spread rapidly to the most densely populated states of Brazil, resulting in the death of hundreds of humans and thousands of nonhuman primates. The Yellow Fever Surveillance Program (Programa de Vigilância da Febre Amarela) implemented by the Brazilian government was designed to prevent and control yellow fever outbreaks. In 2020, the regional reference laboratory at the Oswaldo Cruz Institute in Rio de Janeiro state in Brazil, responsible for yellow fever diagnosis, gave us access to 24 DNA samples from capuchin monkeys, which had tested negative for yellow fever virus. The samples were all from sites in Brazil where Sapajus nigritus is the only species of capuchin monkey present. We attempted to sequence two mitochondrial molecular markers commonly used for Cebidae, but five samples did not amplify. In this study, we performed additional DNA amplification and the Basic Local Alignment Search Tool (BLAST) to confirm the species identity of the 19 samples, which amplified and identify the taxon of the five samples that had failed to amplify. Among the 19 samples correctly identified as Sapajus, one was not Sapajus nigritus but another Sapajus species. Of the five samples that previously failed to amplify, three were similar to Callicebus nigrifrons, one was similar to Alouatta guariba clamitans, and one failed to amplify successfully for any marker. These findings show an error rate of 5/24 (21%) in the original taxonomic identification. Misidentification occurred at the genus level as well as the species level. Our findings highlight the importance of precise taxonomic classification in obtaining reliable data on the consequences of the yellow fever epidemic for primates.
... This demonstrates the ecological flexibility of the species, but also highlights the opportunities for human-wildlife conflict (Pardini et al. 2009(Pardini et al. , 2010Thornton et al. 2011). The use of plantations and other cultivated resources brings primates into direct conflict with farmers, and the increased proximity to human settlements exposes them to further risk of capture, disease transfer, electrocution, and attack by domestic animals (Lynch Alfaro et al. 2014). ...
The southern black-horned capuchin, Sapajus nigritus cucullatus, is considered Near Threatened on the IUCN Red List and Vulnerable in Argentina. The species is mainly threatened by habitat loss and fragmentation. The aim of this study was to compare range size, group size, and density in S. n. cucullatus groups between areas of continuous and fragmented habitat in the Atlantic Forest in Argentina. The study was carried out in two areas in northern Misiones province, one continuous and one anthropogenic fragment. Fieldwork was carried out for 5 days each month from November 2019 to March 2020 and from November 2020 to March 2021. SARS-CoV-2 restrictions meant we could not survey in the intervening period. Group counts were made on existing trails and subsequent group follows. We georeferenced encounters and follows to estimate home range sizes. We calculated density based on home range modeling using 100% minimum convex polygons (MCP), and compared these using generalized linear models (GLM). Smaller groups and lower density of S. n. cucullatus were found in continuous forest, with group sizes between 12 and 23 individuals, and density of 0.14 ind/ha, whereas in the fragmented forest, group sizes were between 32 and 36, with density of 0.62 ind/ha (n = 107; zero-inflated negative binomial regression [ZINB], p < 0.05). The higher density in forest fragments may be due to reduced dispersal ability. This work highlights data on species plasticity that could contribute to the development of conservation management strategies for S. n. cucullatus and its habitat.
... (17) Several conflicts related to human-animal interactions have been described, either through direct contact with human food or through invasion of residential and cultivated areas. (8,(20)(21)(22) There is general agreement among researchers on the urgent need for studies of capuchin monkey groups living in areas not previously studied and subject to fragmentation and urbanization, (23) as a tool for understanding their behavioral flexibility, (17) placing the behavioral ecology of these primates as a research priority. ...
Urban growth and human impacts on the environment have forced animals to adjust to habitat fragmentation and reduced home ranges. Capuchin monkeys are known for their great social and behavioral flexibility, occupying even highly urbanized environments in a way that the time budget of this primate in synanthropic situation may be affected by the area they inhabit. This study aims to analyze the activity budget of a group of Sapajus nigritus living in an anthropized area, 1) comparing the behavioral frequencies in urbanized areas and forest fragments; 2) comparing behavioral frequencies in different sex-age classes. During the study, the number of individuals ranged from 35 to 40 individuals identified based on sex-age classes. Behavioral data were collected using the instantaneous scan sampling method, for two minutes with eight-minute intervals. We obtained 319 scans over 28 days, distributed between November 2021 and June 2022, with eight hours per day. We compared the behaviors different areas and between sex-age classes using the Kruskal-Wallis’s test. Overall, the group performed a higher frequency of traveling (21.22%), followed by foraging (18.07%), feeding (16.57%) and vigilance (15.61%). The frequency of behaviors varied between areas, with vigilance, social, resting, interaction with humans and self-activity more frequent in urbanized areas compared to forest fragments. We also found variation between the sex-age classes, primarily with juveniles foraging more and adults performing more vigilance. The differences in the behaviors performed by the group express the behavioral flexibility of S. nigritus, adapting its activity pattern according to the area occupied.
... Capuchin monkeys (genera Cebus and Sapajus) are a useful animal model to study several aspects of social evolution due to their phylogenetic association with humans, chimpanzees, and Old World monkeys (Lynch Alfaro et al., 2014). This taxonomic group is interesting to study cooperation since this is a critical behaviour to gain and protect ecological and reproductive resources in the wild, including care of their offspring (Perry, 2012). ...
Food-sharing is a cooperative behaviour related to the transfer of resources between conspecifics, and it is considered a complex prosocial behaviour because of its associated costs. It is more likely that an individual cooperates with closely related kin (e.g., in food sharing), and particularly with close maternal kin. In female philopatric species, such as Cebus spp ., mother–offspring bonds likely explain patterns of maternal kin biases. On the other hand, the explanation of the evolution of food-sharing among non-kin is diverse. Capuchin monkeys (genera Cebus and Sapajus ) are interesting to study cooperation since this is a critical behaviour to gain and protect ecological and reproductive resources in the wild, including care of their offspring. We performed an experimental protocol to induce behavioural observations with a provisioning technique using chicken eggs in a wild group of white-faced capuchin monkeys ( Cebus versicolor ). We aimed to test whether this white-faced capuchin monkeys engaged in food-sharing in the wild, describing the pattern of this cooperative behaviour. Furthermore, we also described some conditions that might affect this behaviour. We observed that these capuchins shared the eggs in passive exchanges, meaning that possessors let other individuals to eat from their egg. Our results further suggest that these exchanges may be due to mainly maternal kin biases. This study offers a preliminary observation of a little-studied capuchin species in the wild and adds information about how cooperation works in the wild.
... However, we do not know whether our recent observations were of subgroups, or of cohesive groups that are smaller in size ( and that temporary changes or subgrouping behavior tend to occur in very large groups, but in periods of greatest food scarcity in the region (Janson et al., 2012). Thus, more investigations are needed regarding density and home ranges, but especially on demographic data, as these are essential for status evaluations (Lynch Alfaro et al., 2014). ...
We investigated demographic changes in three primate species (Alouatta guariba, Sapajus nigritus, and Callithrix flaviceps) at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala, Caratinga, Minas Gerais, Brazil, following a yellow fever outbreak (YFO) by comparing their population sizes before (2015) and after the outbreak (2017-2018), and by monitoring the size, composition, and reproductive status of groups from 2017 to 2021. Comparisons of pre- and post-YFO census data indicate the A. guariba population declined by 86.6%, from an estimated minimum of 522 individuals to 70 individuals. However, by October 2021, the population had grown to at least 86 individuals, with an adult sex ratio (N = 53) that was female-biased (0.61). Eleven of the 13 groups being monitored systematically were reproductively active with high survivorship to 12 months of age. S. nigritus declined by 40%, from 377 to 226 individuals. The sex ratio of 33 adult S. nigritus is also female-biased (0.71), and at least 8 of 15 groups being monitored are reproductively active. C. flaviceps declined by 80%, from 85 individuals to the 15-17 individuals observed from 2017 to 2021. The female-biased adult sex ratio and presence of infants and juveniles in the A. guariba and S. nigritus groups are encouraging signs, but there is still great concern, especially for C. flaviceps. Continued monitoring of the demographics of these primates is needed as their persistence appears to still be at risk.
... First, capuchins inhabit a wide variety of niches and exhibit a high degree of ecological flexibility (28), thereby making them a particularly interesting taxon in which to examine the effects of ecological variability on health and immune function. Second, their arboreal nature and small body sizes complicate many traditional methods of health monitoring (2,29). Capuchins are also susceptible to intense anthropogenic encroachment due to predicted expansion of intensive agriculture in the neotropics (30) putting them at increased risk of exposure to disease through contact with humans (31,32) and livestock (33). ...
Non-invasive health monitoring is advantageous for wild and captive primate populations because it reduces the need for traditional invasive techniques (i.e., anesthetization) that can be stressful and potentially harmful for individuals. The biomarker neopterin is an emerging tool in primatology to measure immune activation and immunosenescence, however, most neopterin studies have focused on catarrhine species with little comparative work examining neopterin and health in platyrrhines. To address this gap, we validated a commercially available enzyme-linked immunosorbent assay (ELISA) to measure urinary neopterin in two types of capuchin monkeys, a wild population of white-faced capuchins (Cebus imitator) and a socially housed captive colony of tufted capuchins (Sapajus apella). We analytically validated methods for measuring urinary neopterin in two capuchin populations and demonstrated that two commonly-used methods to control for urine concentration—creatinine and specific gravity (SG)—produced highly concordant results. We also biologically validated these methods by examining variation in neopterin levels based on environment (captive and wild) and age, and changes in levels associated with immune-response. We found that neopterin increased after immune perturbation (rabies vaccine booster), varied by environmental condition, and mirrored expected trends in immune system ontogeny. Our results improve understanding of the innate immune system in platyrrhine species and suggest neopterin may be useful for non-invasive health monitoring in both captive and wild primates.
... Alfaro et al. 2012 [1] proposed the use of Sapajus for tufted (brown; robust) capuchins and suggested that the genus Cebus be restricted to only the untufted (gracile) capuchins. A roundtable of capuchin researchers held at the International Primatological Society Congress in 2012 adopted the use of the term Sapajus as an urgent research priority, calling for the immediate end of the name Cebus apella [9]. ...
Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus. Further, all tufted capuchins were assigned to a single species, Cebus apella, despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus, with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins (Cebus imitator; [Cebus_imitator_1.0] and Sapajus apella [GSC_monkey_1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. Reported here are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.
... We investigated the effect of human pressure gradients and habitat on animal behavior in a remote population of primates. Using large-headed capuchins, Sapajus macrocephalus, as a study species, we also address the lack of behavioral studies on wild Amazonian Sapajus species (Lynch Alfaro et al., 2014) and provide information on the possible impact of observer effects in future studies. Primates are quick to adapt to new situations (Jack et al., 2008;Kalbitzer & Chapman, 2018), so they are anticipated to adapt to varying levels of human pressure gradients at a scale that can be investigated in a short-term behavioral study. ...
Human observers often are present when researchers record animal behavior, which can create observer effects. These effects are rarely explicitly investigated, often due to the assumption that the study animal is habituated to or unaffected by a human’s presence. We investigated the effect of human pressure gradients on a remote population of large-headed capuchins, Sapajus macrocephalus , looking specifically at the effects of number of observers, distance to observers, and distance to the research base. We conducted this study over 4 months in the Pacaya-Samiria Nature Reserve, Peru, and collected 199 two-minute focal samples of capuchin behavior. We found that capuchin monkeys fed less when human observers were closer to the focal individual, when more observers were present, and when capuchins were closer to the research base. We found no other consistent differences in capuchin monkey behavior across the measured human pressure gradients, although capuchins directed a high proportion of their vigilance toward humans (29% in adults and 47% in infants). Our results support the hypothesis that human pressure gradients influence animal behavior. Given the proportion of human directed vigilance, we recommend that all studies that use human observers to record animal behavior consider human-directed vigilance, record the number of observers, as well as the observer-focal animal distance, to check for these effects.
... Capuchins also often form mixed species associations with other primates, especially in their Amazonian range [30]. Sociality can be hierarchical among males and females and additionally features parallel male dispersal across groups [31][32][33][34]. Such social behavior in animals can increase the occurrence of pathogen transmission [35,36]. ...
The major histocompatibility complex (MHC) is an important gene complex contributing to adaptive immunity. Studies of platyrrhine MHC have focused on identifying experimental models of immune system function in the equivalent Human Leukocyte Antigen (HLA). These genes have thus been explored primarily in captive platyrrhine individuals from research colonies. However, investigations of standing MHC variation and evolution in wild populations are essential to understanding its role in immunity, sociality and ecology. Capuchins are a promising model group exhibiting the greatest habitat diversity, widest diet breadth and arguably the most social complexity among platyrrhines, together likely resulting in varied immunological challenges. We use high-throughput sequencing to characterize polymorphism in four Class II DR and DQ exons for the first time in seven capuchin species. We find evidence for at least three copies for DQ genes and at least five for DRB, with possible additional unrecovered diversity. Our data also reveal common genotypes that are inherited across our most widely sampled population, Cebus imitator in Sector Santa Rosa, Costa Rica. Notably, phylogenetic analyses reveal that platyrrhine DQA sequences form a monophyletic group to the exclusion of all Catarrhini sequences examined. This result is inconsistent with the trans-species hypothesis for MHC evolution across infraorders in Primates and provides further evidence for the independent origin of current MHC genetic diversity in Platyrrhini. Identical allele sharing across cebid species, and more rarely genera, however, does underscore the complexity of MHC gene evolution and the need for more comprehensive assessments of allelic diversity and genome structure.
... Both species are listed as 'near threatened' by the IUCN Red List of Threatened Species and both are known to occupy habitats disturbed by agricultural practices Melo, Fialho, et al., 2015). It is possible that anthropogenic hybridization could result in the loss of genetic and phenotypic diversity among robust capuchin species (Lynch Alfaro et al., 2014;Martins et al., 2017). A morphological analysis of hybrid robust capuchins would establish if phenotypic diversity is impacted by hybridization. ...
To better understand the impact of hybridization on development and morphology, I analyze an understudied phenotype in hybrid morphology research: tooth shape. I apply a 2D geometric morphometric approach to compare variation in first upper molar cusp tip positions and crown outline shape among 31 crested capuchins (Sapajus nigritus), 37 bearded capuchins (S. libidinosus), and 44 hybrids (S. nigritus x S. libidinosus). A principal components analysis shows that group membership accounts for a significantly greater proportion of variance along the first major axis of M1 shape variation than does allometry. While most hybrids have S. nigritus-like M1s, several possess a transgressive M1 shape not observed in either parental species. Procrustes distances are greater in hybrids compared to the parental capuchins, and two-block partial least squares analyses show that hybrids exhibit weaker integration between cusp tip positions and crown outline shape. These results demonstrate that hybridization generates novel M1 shapes and support the hypothesis that destabilized development results in elevated phenotypic variance in hybrids. Further studies of dental shape in hybrid primates will generate important data for on-going efforts to detect potential hybrids in the hominin fossil record and to understand the evolutionary outcomes of anthropogenic hybridization.
... Although quite wide ranging, the species is nonetheless subject to habitat reduction, loss and degradation, besides fire, rural settlements, increasing road and agriculture matrix, predation by exotic species, hunting and gathering across its range. Another threat is hybridization with congeneric species (Lynch Alfaro et al. 2014). The species is considered a crop pest in some areas (in sugar cane and pine plantations). ...
... Studying developmental processes and personality on an endangered species helps the implementation of appropriate conservation management plans (Lynch Alfaro, Izar, & Ferreira, 2014;Malange, Izar, & Japyassú, 2016). ...
Animal personality is defined as consistent individual differences across time and situations, but little is known about how or when those differences are established during development. Likewise, several studies described the personality structure of adult capuchin monkeys, without assessing the ontogeny of these personality traits. We analyzed the behavioral repertoire of 12 wild infants (9 males, 3 females) yellow‐breasted capuchin monkeys (Sapajus xanthosternos), in Una Biological Reserve (Bahia, Brazil). Each infant was observed and filmed weekly from birth until 36 months, through daily focal sampling. We analyzed the behavior of each individual in 10 developmental points. By means of component reduction (principal component analysis), we obtained four behavioral traits: Sociability, Anxiety, Openness, and Activity. We investigated whether there were developmental effects on those traits by fitting regression models for the effect of time on behavioral traits, controlling for monkey identity, sex, and cohort. Sociability (decreasing) and Anxiety (increasing) changed significantly along development. By means of repeatability analysis, we did not find intra‐individual consistency across time in those traits, so we cannot discriminate stable personality traits in early ontogeny. Our results show that the personality structure of capuchin monkeys is not established during early development, in agreement with the literature on human personality.
Research Highlights
• Four behavioral traits for young wild yellow‐breasted capuchin monkeys were described: Sociability, Anxiety, Openness, and Activity.
• The behavioral traits were not stable across the first 3 years (36 months) of life.
• Personality structure of capuchin monkeys is not yet established during early development.
• Opposite developmental tendencies on Sociability (decreasing along development) and Anxiety (increasing) were detected.
... Assessing previously unstudied capuchin populations has been identified as a research priority for capuchin conservation by the International Primatological Society (Lynch Alfaro et al. 2014). Here we report the presence of the critically endangered Ecuadorian white-fronted capuchin in a new location using remote cameras. ...
The Ecuadorian white-fronted capuchin (Cebus aequatorialis) is classified as Critically Endangered (CR) on the IUCN Red List at both international and national levels in Ecuador, and the majority of detections have been recorded from direct observation. In this work, we report the occurrence of this species in a new location in the Coastal Region of Ecuador recorded by remote cameras. Overall, eight separate detections were recorded by three unique cameras from 19 Aug to 10 Dec 2016, over seven individual days, with a detection rate of 1.4 records per 1000 camera days. One additional detection was recorded in a brief remote camera survey conducted in January and February 2018. Only two direct observations were recorded in many visits to the study area over the past several years, suggesting that the use of remote cameras could be an effective method to detect the occurrence of Ecuadorian white-fronted capuchin, particularly in tropical dry forests with low tree coverage.
... Recent studies of birds and primates specialized in seasonally flooded forests show a consistent pattern of past isolation between western and eastern lineages, with evidence of recent contact in central Amazonia 37 or expansion from west to east 38 . Fish species diversity along the Amazon basin corroborates the long-time persistence of aquatic environments in the west, with high species richness, endemism, and similarity in species composition among western sub-basins 31,39 . ...
The Amazonian landscape evolution is the result of the combined effect of Andean tectonism, climate and the Earth’s interior dynamics. To reconstruct the landscape evolution and its influence on paleoenvironmental variations within Amazonia since the Oligocene, we conducted numerical experiments that incorporate different surface and geodynamic processes, reproducing many paleogeographic features as inferred from the sedimentary record. We show that the evolution of the drainage pattern gradually reduced the area of sedimentation derived from the Guiana and Brazilian shields while expanded the Andean derived deposits during the Miocene, affecting the nutrient availability. First order biotic habitats were inferred from these paleogeographical reconstructions, showing an eastward expansion of várzea and terra firme forests and consequent retraction of igapó forests, with a millennial-scale reconfiguration of a mosaic of habitats in the lowlands. We conclude that this dynamism probably guided the observed patterns of speciation in the most biodiverse biome on Earth.
... These are the first reports of molecular diagnosis using primary samples in those species. In the case of the blond capuchins, a critically endangered species, identification of this agent is important, since these specimens were part of a reproduction program for ex situ conservation (LYNCH ALFARO et al., 2014;FERREIRA et al., 2015;IUCN, 2018). ...
Recent genetic population studies on Toxoplasma gondii in Brazil have shown large genetic variability. The objective of the present study was to isolate and genotypically characterize T. gondii from free-ranging and captive wild mammals and birds in Pernambuco state, Brazil. Fragments of heart, brain, skeletal muscle and diaphragm tissue from 71 birds and 34 mammals, which were either free-ranging or captive, were collected. Samples from 32 of these animals were subjected to bioassays in mice. Samples from the remaining 73 animals underwent biomolecular diagnosis, using PCR technique, targeting a repetitive DNA fragment of 529 bp in T. gondii. A non-virulent isolate (TgButstBrPE1) was obtained from a free-ranging striated heron (Butorides striata) and, based on primary samples, seven animals were found to be positive. The primary samples and the isolate obtained were subjected to PCR-RFLP using the markers SAG1, 5’3’SAG2, alt.SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1, Apico and CS3. ToxoDB-RFLP genotype #13 from the striated heron isolate and Type BrIII genotype from a captive otter ( Lontra longicaudis) (PS-TgLonloBrPE1) were obtained. The present study describes the first isolation and genotypic characterization of T. gondii in free-ranging striated heron, and the first genotypic characterization of T. gondii in a captive otter.
... The health of primates in fragments also affects their persistence. Capuchins (Cebus and Sapajus) living in forest fragments are more exposed to pathogens from domesticated animals, and may face reduced dietary variability (Lynch Alfaro, Izar, & Ferreira, 2014). The proximity of habitat fragments to urban zones can potentially increase risk of predation by domesticated dogs, as documented for the masked titi (Callicebus personatus) and the brown howler monkeys (Alouatta guariba; Chiarello, 2003 Martins, Lynch Alfaro, and Rylands (2017). ...
Habitat loss is one of the main threats to biodiversity. Fragmentation resulting from this process may restrict available habitat for primates, limiting their persistence in a given region. In this study, we aimed to quantify deforestation and fragmentation by identifying forest remnants capable of maintaining populations of the endangered crested capuchin monkey (Sapajus robustus) within its distributional limits in the states of Bahia, Espírito Santo, and Minas Gerais, Brazil. We used Landsat images from 1985 to 2010 to generate three time‐interval mosaics classified by natural and non‐natural vegetation. We then calculated the size of the forest remnants and the distance of each fragment of natural vegetation to its nearest neighbor. Between the first (1985–1990) and second (1995–2000) mosaics there was a vegetation loss of 41.4%, and between the second and third (2005–2010) mosaics there was a natural vegetation gain of 1%. The third mosaic showed smaller and more isolated fragments in comparison to the first mosaic. Across the three periods, Bahia was the state with the highest rate of deforestation. While Espírito Santo had fewer identified forest remnants, it retained the most natural vegetation within these small fragments. The landscape within the currently recognized distributional limits of the crested capuchin monkey is dominated by agriculture and livestock. Both decreasing fragment size and increasing species isolation by distance between fragments can negatively affect primate populations, increasing their risk of extinction. Isolation makes it difficult for migration and recolonization events to occur. Therefore, habitat restoration should be prioritized to reduce isolation between populations. Our findings may serve as a resource for future conservation efforts and management of the crested capuchin monkey.
... Stone tool use has been observed in the wild in all well-studied robust capuchins species including black-striped capuchins, Sapajus libidinosus (Ottoni and Mannu, 2001;Fragaszy et al., 2004a;Mendes et al., 2015); yellow-breasted capuchins, Sapajus xanthosternos (Canale et al., 2009); blonde capuchins, (Sapajus flaviius) (Ferreira et al., 2009); black-horned capuchins, Sapajus nigritus (Rocha et al., 1998); and black-capped capuchins, Sapajus apella (Boinski et al., 2000) (based off of taxonomic resources, they are not required. Habitual use of tools, and stone tools in particular, is considered one of the defining behavioral differences between Cebus and Sapajus (Lynch Alfaro et al., 2014). The near absence of tool use in gracile capuchins is puzzling as they are otherwise highly innovative and have a wide array of social (Perry et al., 2003) and foraging traditions (Chapman and Fedigan, 1990;Panger et al., 2002b;O'Malley and Fedigan, 2005) which are socially learned (Perry, 2009;Barrett et al., 2017). ...
Habitual reliance on tool use is a marked behavioral difference between wild robust (genus Sapajus ) and gracile (genus Cebus ) capuchin monkeys. Despite being well studied and having a rich repertoire of social and extractive foraging traditions, Cebus sp have rarely been observed engaging in tool use and have never been reported to use stone tools. In contrast, habitual tool use and stone-tool use by Sapajus is widespread. We discuss factors which might explain these differences in patterns of tool use between Cebus and Sapajus . We then report the first case of habitual stone-tool use in a gracile capuchin: a population of white-faced capuchins ( Cebus capucinus imitator ) in Coiba National Park, Panama who habitually rely on hammerstone and anvil tool use to access structurally protected food items in coastal areas including Terminalia catappa } seeds, hermit crabs, marine snails, terrestrial crabs, and other items. This behavior has persisted on one island in Coiba National Park since at least 2004. From one year of camera trapping, we found that stone tool use is strongly male-biased. Of the 205 unique camera-trap-days where tool use was recorded, adult females were never observed to use stone-tools, although they were frequently recorded at the sites and engaged in scrounging behavior. Stone-tool use occurs year-round in this population, and over half of all identifiable individuals were observed participating. At the most active tool use site, 83.2% of days where capuchins were sighted corresponded with tool use. Capuchins inhabiting the Coiba archipelago are highly terrestrial, under decreased predation pressure and potentially experience resource limitation compared to mainland populations-- three conditions considered important for the evolution of stone tool use. White-faced capuchin tool use in Coiba National Park thus offers unique opportunities to explore the ecological drivers and evolutionary underpinnings of stone tool use in a comparative within- and between-species context.
... As shown in Supplementary Table S1, most sampled animals were robust capuchin monkeys (genus Sapajus, family Cebidae). Due to frequent hybridization events between different Sapajus species ( Figure 1B) and due to animal trafficking over long distances, not all species could be unambiguously identified [18]. An adult female capuchin monkey kept in an animal shelter for about one year before sampling tested positive in a broadly reactive and highly sensitive Hepadnaviridae PCR assay [7], whereas all other animals were PCR-negative. ...
Background & aims:
All known hepatitis B virus (HBV) genotypes occur in humans and hominoid Old World nonhuman primates (NHP). The divergent Woolly Monkey HBV (WMHBV) forms another orthohepadnavirus species. The evolutionary origins of HBV are unclear.
Methods:
We analyzed sera from 124 Brazilian monkeys collected during 2012-2016 for hepadnaviruses using molecular and serological tools and conducted evolutionary analyses.
Results:
We identified a novel orthohepadnavirus species in capuchin monkeys (CMHBV). We found CMHBV-specific antibodies in five animals and high CMHBV concentrations in one animal. Non-inflammatory, probably chronic infection was consistent with an intact preCore domain, low genetic variability, core deletions in deep sequencing, and no elevated liver enzymes. Cross-reactivity of antisera against surface antigens suggested antigenic relatedness of HBV, CMHBV and WMHBV. Infection-determining CMHBV surface peptides bound to the human HBV receptor (hNTCP), but preferentially interacted with the capuchin monkey receptor homologue. CMHBV and WMHBV pseudotypes infected human hepatoma cells via the hNTCP and were poorly neutralized by HBV vaccine-derived antibodies, suggesting cross-species infections may be possible. Ancestral state reconstructions and sequence distance comparisons associated HBV with humans, whereas primate hepadnaviruses as a whole were projected to NHP ancestors. Co-phylogenetic analyses yielded evidence for co-speciation of hepadnaviruses and New World NHP. Bayesian hypothesis testing yielded strong support for an association of the HBV stem lineage with hominoid ancestors. Neither CMHBV, nor WMHBV were likely ancestors of the divergent human HBV genotypes F/H found in American natives.
Conclusions:
Our data suggest ancestral co-speciation of hepadnaviruses and NHP and an Old World origin of the divergent HBV genotypes F/H. Identification of a novel primate hepadnavirus offers new perspectives for urgently needed animal models of chronic hepatitis B.
Lay summary:
The origins of HBV are unclear. The new orthohepadnavirus species from Brazilian capuchin monkeys resembled HBV in elicited infection patterns and could infect human liver cells using the same receptor as HBV. Evolutionary analyses suggested that primate HBV-related viruses might have emerged in African ancestors of New World monkeys millions of years ago. HBV was associated with hominoid primates including humans and apes, suggesting evolutionary origins of HBV before the formation of humans. HBV genotypes found in American natives were divergent from those found in American monkeys, and likely introduced along prehistoric human migration. Our results elucidate the evolutionary origins and dispersal of primate HBV, identify a new orthohepadnavirus reservoir and enable new perspectives for animal models of hepatitis B.
In species under sexual selection, morphological and behavioral traits strongly influence reproduction, which ultimately affects copulation rates and reproductive success. One of the most conspicuous traits are the sexual size dimorphism, such as the permanent or transient enlargement of males, as in the case of squirrel monkeys. In this study, we unveil some key aspects of the “fatted male phenomenon” in four captive groups of Amazonian Collins’ squirrel monkey. We examined their reproductive behavior, dominance, and network power to investigate whether male fattening enhances their copulatory success and to find the presence of pre-copulatory sexual selection factors. Our results show that males in fatted condition increased their copulation rate and displayed higher levels of aggression towards females and other males. We did not find any evidence of greater female tolerance, receptivity, or attraction to fattened males, nor did we find any influence of the fattening condition on the social dominance of males. The evidence suggests that pre-copulatory sexual selection operates in two simultaneous ways in this species. For fatted males, it operates through the imposition on females. In contrast, the affiliative network positions allow the non-fatted males to stay socially closer to females, thus allowing them to achieve successful copulation and some degree of reproductive success. Our study provides strong evidence for two alternative male reproductive strategies that may explain the persistence of fatted and non-fatted phenotypes across generations, and suggests that a variety of male strategies may be used by males of different vertebrate species.
The coastal province of Manabí Ecuador has some of the highest rates of deforestation in Latin America, and remaining fragments are home to two primate species threatened with extinction – the mantled howler monkey (Alouatta palliata aequatorialis), and the Ecuadorian white-fronted capuchin (Cebus aequatorialis). Manabí is also reputed to contain the greatest concentration of Guadua angustifolia bamboo in the country, and the development of a sustainable bamboo economy is being promoted by some as a solution to the social and environmental issues that plague the region.
This thesis uses an ethnoprimatological approach to explore the messiness of conviviality, or “living with”, in human and nonhuman worlds, through an investigation of lived realities and interrelationships between people, non-human primates, and bamboo in the Pacoche Wildlife Refuge of coastal Ecuador. Starting from the premise that participants’ relationships with the nonhuman are embodied in historically situated experiences, and political-economic and social contexts that are constantly in flux, and based on findings generated by a mixed methods approach, this thesis uncovers the many meanings and values associated with bamboo, as an everyday raw material, a cause for contention with local authorities, a “green” commodity, an important part of cultural heritage and identity, and a vital component of primate habitats.
Findings also reveal that unraveling the complex power structures embedded within conservation politics can expose new ways of seeing and thinking about conservation that prioritize local knowledge and existing relationships between humans and nonhumans as active agents in shaping forest ecosystems. Ultimately, this thesis argues for a community-based conservation model aligned with principles of convivial conservation, where local residents are integral participants in the conservation process.
Conversion of primate forest habitat is a global concern with significant implications for primate populations. Although the geospatial Extent of Occurrence (EOO) data provided for primates by the International Union for the Conservation of Nature are widely used, they do not accurately reflect the existing extent of primate species because of ongoing habitat loss. We focused on four capuchin monkey species (Sapajus apella, S. flavius, S, libidinosus, and S. xanthosternos), all native to North and Northeastern Brazil, to prioritize research by the Capuchin Action Network. We refined the EOOs for the four primate species using MapBiomas land cover data. We accounted for areas of agriculture, urban, and mining and updated the EOOs of the four species. Additionally, we evaluated the Conservation Units in each EOO. Conservation Units are protected areas critical to mitigating habitat loss in Brazil. Our results show that S. apella has lost the smallest amount of its EOO (13%), while S. flavius has lost the most (77%). Agriculture was the leading cause of land cover change, followed by urbanization and mining. We provide an updated EOO for the four capuchin species and highlight the need for conservation efforts to address the challenges posed by human activities in the capuchin species’ habitats.
In this chapter, we consider pathways to work for a future for Amazonia where both humans and other mammals flourish and the rainforest is protected. First we briefly review the tens of millions of years it has taken to develop the current diversity of mammalian fauna living in Amazonia. Humans are a very recent mam-malian arrival to Amazonia at about 10,000 years ago. A second wave of humans intruded into the Americas starting at ~500 years ago, resulting in widespread geno-cide of Indigenous Peoples and one onset of the Anthropocene epoch. We review the current state of research and conservation concerns for nonhuman mammalian taxa in Brazilian Amazonia. We emphasize that the utilization and transformation of Amazonian land and resources continue to be driven by the export of energy and goods to other regions of Brazil and, notably, to international markets, putting the mammalian taxa at risk. We suggest priorities for conservation interventions in Brazilian Amazonia, including Indigenous Land demarcation; valuing of local com
Many primate species are threatened by the pet trade, and rehabilitated monkeys require suitable habitats for release back into the wild. The process of identifying suitable release sites involves finding areas with adequate resources and minimizing negative impacts on resident species and human populations. To address this challenge, this study was designed to identify and map suitable areas for the reintroduction of bearded capuchin monkeys (Sapajus libidinosus) into the Caatinga biome in northeastern Brazil. We used a multicriteria decision analysis (MCDA) to identify suitable release areas. Using a species distribution model, we located suitable habitats for seven species of vegetation that are vital resources during the dry season: Syagrus romanzoffiana, Attalea speciosa, Syagrus oleracea, Commiphora leptophloeos, Manihot epruinosa, Pilosocereus pachycladus, and Tacinga inamoena. We then created an MCDA by using vegetation suitability, water availability, proximity to protected areas, and distance from roads and cities as key variables. To increase accessibility, we coded the results into a Google Earth Engine app, allowing for easy and free access to researchers and others interested in capuchin monkey conservation. The resulting suitability maps cover the entire Caatinga biome, providing a valuable tool for conservation efforts by simplifying the initial step of locating potential release sites. This study demonstrates the application of geospatial tools in mapping suitable habitats for the translocation and release of rehabilitated primates at a time when biodiversity loss, the exotic pet trade, land use change, and climate change are threatening nonhuman primates worldwide.
Handedness is a fundamental human trait, although recent research, especially on nonhuman primates, has shown that it is displayed by other animals as well (e.g., chimpanzees, gorillas). In this study, we explore hand preference in wild crab-eating tufted capuchin monkeys (Sapajus libidinosus) inhabiting a mangrove forest located on the coastal area of Northeast Brazil (Maranhão State). Tufted capuchin monkeys at our site use facultatively wooden tools to crack open crabs. We observed hand preference in 12 subjects who spontaneously participated in experiment sessions, in which we provided crabs and tools on wooden platforms. We recorded (using events and bouts) two unimanual tasks, (tool or crab) grabbing and (tool or crab) pounding, and one bimanual task, crab pulling, where one hand kept the crab in place while the other pulled off parts of the crab. Hand preference increased with greater strength needed to perform the task and its complexity. While only 17%-25% of capuchins showed hand preference during grabbing, 44%-64% showed hand preference during pounding, and most subjects 64%-80% displayed a right-hand preference when performing the bimanual task, for which all lateralized individuals were right-handed. Hand preference did not vary between adults and juvenile individuals and was not consistent across tasks. Group-level hand preference was found only for the bimanual task, for which all lateralized individuals were right-handed. Our findings are in concordance with those of other primate studies showing the emergence of hemispheric specialization for bimanual actions, highlight the importance of conducting such studies on diverse type of tasks, and show the feasibility to conduct experimental manipulation under natural conditions.
Global and spatially explicit information about the interaction between habitat and wildlife species is critical to enhancing conservation efforts. Despite the recognized importance of mangrove forests to non-human primates, the relationship between the two lacks understanding. To counter this, we created the MangPrim-21 database to map and measure the locations of interactions between all non-human primates and all mangrove forests globally. We report our findings across the global, national, and local scales for all inventoried non-human primates and all inventoried mangrove forests. Globally, we find that half of all non-primates potentially use mangrove forests, and more than half of the global mangrove forest falls within the delineated range of at least one non-human primate species. Nationally, we find that Indonesia, Madagascar, Brazil, Cameroon, and Malaysia likely have the most non-human primate and mangrove forest interactions. At the subnational level, we find that several discrete locations in Kalimantan are critical to both mangrove forests and non-human primates. The MangPrim-21 database provides a globally consistent and locally applicable database of non-human primate and mangrove forest interactions. The results presented have broader implications for non-human primate and mangrove conservation and global actions to protect both. Additionally, our results raise questions about the idea that non-human primates primarily use mangrove forests as a refuge from human encroachment and habitat degradation.
Primate tool use is of great interest but has been reported only in a limited number of species. Here we report tool use in crested capuchin monkeys (Sapajus robustus), an almost completely unstudied robust capuchin species. Crested capuchins and their sister species, the yellow-breasted capuchin, diverged from a common ancestor over 2 million years ago, so this study fills a significant gap in understanding of tool use capacity and variation within the robust capuchin monkey radiation. Our study group was a captive population of seven individuals at the Santa Ana Zoo in California. The monkeys were given no prior training, and they were provided with a variety of enrichment items, including materials that could be used as tools as well as hard-to-access resources, for open-ended interactions. In 54 observation hours, monkeys performed eleven tool use actions: digging, hammering, probing, raking, sponging, striking, sweeping, throwing, waving, wedging, and wiping. We observed tool modification, serial tool use, and social learning opportunities, including monkeys' direct observation of tool use and tolerated scrounging of foods obtained through tool use. We also observed significant individual skew in tool use frequency, with one individual using tools daily, and two individuals never using tools during the study. While crested capuchins have never been reported to use tools in the wild, our findings provide evidence for the species' capacity and propensity for tool use, highlighting the urgent need for research on this understudied, endangered primate. By providing detailed data on clearly identified S. robustus individuals, this study marks an effort to counteract the overgeneralization in the captive literature in referring to any robust capuchins of unknown provenance or ancestry as Cebus apella, a practice that obfuscates potential differences among species in tool use performance and repertoire in one of the only species-rich tool-using genera in the world.
The Anthropocene brought an accelerated risk of extinction for species across the globe. However, extinction proneness is not even across groups. Past and current events show large-sized mammals at greater extinction risk than smaller ones. For practical reasons, conservation actions tend to focus on the species level; therefore, well-founded species limits are pivotal. Since 2005, the number of known mammal species is about 20% higher but largely due to taxonomic discoveries in small-sized taxa. Here we review the recent taxonomic advances on medium- and large-sized mammals (MLM) from the Neotropics, and discuss misperceptions concerning the taxonomy stability in this group and how this may hinder proper conservation actions. We advocate that apparent taxonomic inertia toward large-sized mammals is partly related to limited systematic inquiry rather than representing an accurate knowledge of their diversity. Fortunately, this scenario has slowly changed in recent years. Linked to integrative analyses that took place during the 21st century, the Neotropical region represents a major example of recent growth in MLM diversity. Taxonomic novelties were found in eight orders of MLM and occurred across taxonomic ranks, from family to subspecies. Most changes comprise subspecies or synonyms elevated to full species, but new taxa of Artiodactyla, Carnivora, Lagomorpha, Pilosa, Primates, Perissodactyla, and large rodents have also been discovered. Recent reshuffles in MLM classification clearly illustrate the risk that bias in taxonomy studies can bring to conservation. Considering the new findings, some species previously labeled as “least concern” for conservation, stand now in some level of threat. This appraisal challenges the misperception of MLM as well-known and shows that taxonomy is a conservation issue.
The knowledge of anatomy and imaging exams emerges as an important tool in the study of evolutionary processes of a species, in the elaboration of diagnosis, and the successful choice of the appropriate clinical and surgical procedures. Therefore, this study aims to describe the osteology of the hind limb of Sapajus libidinosus by means of gross, radiographic, and tomographic images. Four cadavers were used in the macroscopic analysis and five animals for the imaging exams, of which four were eventually euthanized and added to the macroscopic study. For imaging exams, they were kept anesthetized. All bones of the hind limb were documented, their structures were described, and compared with data in the literature from human and nonhuman primates. We have performed Student's t test for independent samples. There was no statistical difference between the sexes regarding the length of the hind limb bones. The coxal bone was largely well described using imaging methods. A small penile bone was present at the tip of the penis and it could be identified by all analysis methods. The femur, as well as the tibia and fibula, were not well portrayed in their proximal and distal epiphyses by radiography (Rx). However, they were well identified on tomography. No third trochanter was observed in the femur and the patella had a triangular shape. All the structures described by gross anatomy of the tarsus and metatarsus could be identified by Rx and tomography. More subtle structures, such as the popliteal notch on the tibia, and the gluteal tuberosity pectineal line and facies aspera on the coxal bone, were not identified by medical imaging. S. libidinosus presented anatomical characteristics that were similar to those of larger New World and Old World monkeys, including man. This suggests it's value as an experimental model for studies in recent primates.
Saimiri are neotropical primates with seasonal reproduction, males develop a seasonal fattening condition that has been suggested as a pre-copulatory sexual selection strategy. Furthermore, females mate with multiple males in the same season. This could also favor the evolution of a postcopulatory sexual strategy by sperm competition. In this study, we tested the hypothesis that there is a relationship between the fatted condition and advantageous seminal characteristics in Saimiri collinsi and evaluated its implications for sperm competition. Adult males (N = 10), aged 5–15 years, housed in mixed or only-male groups, were analyzed from June, 2015 to July, 2016. Measurements of weight, axilla, and arm skinfold, and testicular volume were taken monthly, and semen was collected by electroejaculation. A fattening index was developed to quantify and identify fatted males, biometrics, and seminal parameters were compared between the non-fatted and fatted conditions. The fatted males present a larger testicular volume. This is related to the increase in spermatogenic activity necessary to sustain a high ejaculation frequency during the mating season. An increase in seminal volume and in frequency of semen coagulation were detected in fatted males, advantages related to sperm protection in the female reproductive tract. Age and social context were not significant sources of variation for both morphological and seminal traits. A decrease in response from the fatted males in obtaining semen and an increase in the frequency of azoospermic ejaculates were observed. These unexpected results may be due to intense reproductive activities in a short period. The fattening phenomenon has many implications in the sexual selection of squirrel monkeys, and they are still not entirely unveiled. Our results corroborate the idea that, in S. collinsi, the fatted male condition is related to sexual selection, and we found evidence suggesting it may be also expressed by a post-copulatory component, sperm competition.
Highlights
• The fatted males (Saimiri collinsi) have important advantages in the production and survival of sperm, with increased fertilization probability.
• The fatted male presents a testicular and seminal volume greater than that of non-fatted males, which is a strong indicator that in fatted males where sperm competition is intense, characteristics that increase the success of fertilization are positively selected.
• During the fattening period in S. collinsi, the more frequent appearance of coagulation degrees II and III can reveal an adaptation that provides an advantage to gametes, increasing their chance of fertilization in periods when sperm competition increases.
Capuchin monkeys (genera Cebus and Sapajus) show a wide range distribution, from Honduras to Argentina. The aim of this work was to evaluate the genetic and phenotypic variability of captive specimens putatively belonging to S. cay (SCY) and S. nigritus (SNI) at their southernmost distribution limit. Forty-four individuals held in five captive centers from Argentina were analyzed based on external morphology, karyology and DNA sequences of mitochondrial control region (mtDNA-CR). Three morphotypes associated with their probable geographical origin in SCY and a single morphotype in SNI were found. For SCY we could associate each morphotype with the most frequent karyotype. SNI showed a single phenotype and a homogenous karyotype. Heterochromatin showed geographical patterns within species. A 515-bp mtDNA-CR fragment was sequenced, defining fourteen haplotypes at 59 polymorphic sites. A network constructed with our 14 haplotypes and other 77 from S. apella, S. macrocephalus, S. cay and S. nigritus from bibliography revealed some phylogeographic signals. Our SCY and SNI samples rendered four groups that differed in multiple mutational steps, with SCY being more similar to S. apella than to S. macrocephalus. Also, we identified two genetic divergent SCY groups: samples from NOA and from NEA with high mitochondrial diversity. Our results highlight the relevance of using complementary genetic tools throughout the distribution ranges of SCY and SNI for a better assessment of their diversity.
An updated and annotated checklist of mammals occurring in Brazil is presented. A total of 751 native species, distributed in 249 genera, 51 families and 11 orders were recorded to the country. The Brazilian mammalian fauna shows an elevated rate of endemism (30%; 223 species). Among the species evaluated by IUCN (668 species; 90%), a total of 80 (10.6% of total mammalian fauna) are Threatened, 28 (3.9%) are considered as Near Threatened, two species (0.3%) are presumable Extinct, 96 (12.8%) are considered with Defi cient Data for conservation and 462 (61.6%) are considered as Least Concern. Fifteen new species were described since the last national compilation (published in 2017), which associated to new records to the country and synonimizations resulted in an increment of 30 species. Eight non-native species were introduced to the country, including the recently established Asiatic cervids Rusa unicolor (sambar) and Axis axis (chital). Seven native species (fi ve primates and two hystricomorph rodents) have been translocated from their areas of natural occurrence to other areas inside the country.
Across the globe, primates are threatened by human activities. This is especially true for species found in tropical dry forests, which remain largely unprotected. Our ability to predict primate abundance in the face of human activity depends on different species' sensitivities as well as on the characteristics of the forest itself. We studied plant and primate distribution and abundance in the Taboga Forest, a 516-ha tropical dry forest surrounded by agricultural fields in northwestern Costa Rica. We found that the density of white-faced capuchins (Cebus capucinus) at Taboga is 2-6 times higher than reported for other long-term white-faced capuchin sites. Using plant transects, we also found relatively high species richness, diversity, and equitability compared with other tropical dry forests. Edge transects (i.e., within 100 m from the forest boundary) differed from interior transects in two ways: (a) tree species associated with dry forest succession were well-established in the edge and (b) canopy cover in the edge was maintained year-round, while the interior forest was deciduous. Sighting rates for capuchins were higher near water sources but did not vary between the edge and interior forest. For comparison, we also found the same to be true for the only other primate in the Taboga Forest, mantled howler monkeys (Alouatta palliata). Year-round access to water might explain why some primate species can flourish even alongside anthropogenic disturbance. Forest fragments like Taboga may support high densities of some species because they provide a mosaic of habitats and key resources that buffer adverse ecological conditions.
Natural Sapajus libidinosus populations are in continuous decline due to fragmentation, habitat loss and the illegal pet trade. They live in Caatinga scrub forests, which already lost over 50% of their original cover. The lack of studies on S. libidinosus population genetics means that we do not know how they are being affected by this striking habitat loss and other anthropogenic disturbances. Polymorphic markers are not available for the study of S. libidinosus diversity and population genetics. Thus, here we aimed to test the transferability of 14 microsatellite markers to S. libidinosus. These microsatellites were previously isolated from Cebus capucinus (white-faced capuchin), species belonging to the same subfamily (Cebinae) as the study species. We found that six of the tested microsatellite markers (tetra-nucleotide) were cross-amplified in our target species. All loci were polymorphic. The number of alleles varied from 4 to 7 and the expected heterozygosity ranged from 0.588 to 0.869. The microsatellite markers transferred to S. libidinosus and characterised in our study will be a valuable tool to evaluate the genetic variability of both wild and captive populations. They will considerably reduce the costs of microsatellite isolations, helping to prioritise currently limited research and conservation budgets in Brazil.
Across the globe, primate species and habitats are threatened by human activity. This is especially true for species found in tropical dry forests, which are widely distributed and comprise diverse habitats that remain largely unprotected. Evidence suggests that some primate species endemic to tropical dry forests may be more sensitive to anthropogenic disturbance than others, but our ability to predict primate abundance in the face of disturbance also depends on the specific variables for each site. Here, we consider the factors that explain the high density of white-faced capuchins ( Cebus capucinus ) found in the Taboga Forest, Costa Rica, a relatively small fragment of tropical dry forest surrounded by agricultural fields. Our analyses suggest that, for capuchins (and potentially for mantled howler monkeys, Alouatta palliata ), the size and disturbance of a forest fragment may matter less than the composition and availability of key resources, like above-ground water. Group sightings for both species were higher near permanent water sources, but group sightings did not vary between edge and interior forest. These findings help explain why some primate species can flourish even alongside anthropogenic disturbance and thus carry important implications for conservation efforts. Smaller forest fragments, like Taboga, may be able to support high densities of some species because they provide a mosaic of habitats and key resources that buffer adverse ecological conditions. Future studies will assess the extent to which primates in the Taboga Forest rely on the canals versus the river and will consider how the high density of capuchins in Taboga influences ranging patterns, home range overlap, and the frequency and intensity of intergroup encounters.
RESEARCH HIGHLIGHTS
Here we introduce a new white-faced capuchin study site in the Taboga Forest, Costa Rica, a fragmented tropical dry forest.
Forest fragments like Taboga may support high primate densities because they provide a mosaic of habitats and key resources.
The Upper Paraná Atlantic Forest of Eastern Paraguay has been devastated by the encroachment of vast monocultures of soybean plantations. What little remains of the Paraguayan Atlantic Forest exists as small, isolated fragments in a matrix environment of soy fields, cattle ranches and human settlements. The hooded capuchin (Sapajus cay) is the only representative of its genus in Paraguay and little is known about its socioecology. This charismatic species is an excellent flagship species; appealing to the public, and the only primate that is almost completely restricted to the Atlantic Forest. Feeding and social ecological models will determine the effect of food availability on sociality. A spatial ecological model of range use, range overlap and territoriality will be developed to determine minimum forest fragment size sufficient to support multiple groups of hooded capuchins. Levels of disturbance will be categorised through detailed habitat surveys and the use of the forest strata in areas of different disturbance will indicate the monkeys’ ability to adapt to degraded areas. Ethnoprimatological surveys will evaluate local knowledge of, and attitudes towards, primates in communities surrounding protected areas and to investigate the levels of anthropogenic pressures, such as hunting and logging, on primates in San Rafael National Park. Understanding the ecological needs of this species in fragmented and degraded forest, while promoting their need for conservation to the general public, will allow the development of a conservation strategy, which could be beneficial in the long term to the numerous other species of the Paraguayan Atlantic Forest.
Primates play an important role in ecosystem functioning and offer critical insights into human evolution, biology, behavior, and emerging infectious diseases. There are 26 primate species in the Atlantic Forests of South America, 19 of them endemic. We compiled a dataset of 5,472 georeferenced locations of 26 native and 1 introduced primate species, as hybrids in the genera Callithrix and Alouatta. The dataset includes 700 primate communities, 8,121 single species occurrences and 714 estimates of primate population sizes, covering most natural forest types of the tropical and subtropical Atlantic Forest of Brazil, Paraguay and Argentina and some other biomes. On average, primate communities of the Atlantic Forest harbor 2±1 species (range=1‐6). However, about 40% of primate communities contain only one species. Alouatta guariba (N=2,188 records) and Sapajus nigritus (N=1,127) were the species with the most records. Callicebus barbarabrownae (N=35), Leontopithecus caissara (N=38), and Sapajus libidinosus (N=41) were the species with the least records. Recorded primate densities varied from 0.004 individuals/km² (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km² (Alouatta caraya in Santiago, Rio Grande do Sul, Brazil). Our dataset reflects disparity between the numerous primate census conducted in the Atlantic Forest, in contrast to the scarcity of estimates of population sizes and densities. With these data, researchers can develop different macroecological and regional level studies, focusing on communities, populations, species co‐occurrence and distribution patterns. Moreover, the data can also be used to assess the consequences of fragmentation, defaunation, and disease outbreaks on different ecological processes, such as trophic cascades, species invasion or extinction, and community dynamics. There are no copyright restrictions. Please cite this Data Paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.
Captive environments are relatively less complex as compared to wild, and consequently contain less stimuli for any animal within them, which may be stressful. One approach to mitigate stress in captive animals is the application of environmental enrichment techniques. Capuchin monkeys are among the most common primates in captivity, therefore, evaluating the efficacy of environmental enrichment techniques for these species is important. In this study, we evaluated the effects of natural material as environmental enrichment for Sapajus spp. We performed a comparative study of the behavior of seven individuals when their enclosure was non-enriched and enriched with bamboo, leaf-litter and bromeliads. Our results suggested that activities such as body care and affiliative interactions were less frequent when environmentally enriching objects were placed in their enclosure. They also spent more time in object manipulation, and monitoring behavior significantly reduced during these periods. Of the three materials used, we consider bamboo the most efficient enrichment material, since it remained in the enclosure longer and so attracted capuchin attention for a more extended period, and significantly modified their behavior.
The International Code of Zoological Nomenclature allows the naming of new species without a type specimen ever having been preserved. This practice causes problems and is undesirable because if related, cryptic, sibling species are encountered later, it may not be possible either to allocate them with certainty to the earlier named species, or to determine them to be something different.
We hypothesised that examination of the instances in which mammalian species were named without preserved types would reveal certain problems that are not unique to them, but are encountered more frequently than when types are preserved. We also thought the Code's stipulation that preserved types are not required in the case of specimens that are no longer ‘extant’ would present special problems hitherto unremarked upon in the literature.
We conducted a review of cases involving putative new species of mammal named since 1900. These were analysed to see what special problems they present and the frequency of such problems.
We found that the Code's waiver of the requirement that a type specimen be deposited in a collection if the specimen is no longer extant presents numerous problems—in particular, that a living‐at‐large type specimen can still be ‘extant’ even if its whereabouts are unknown at certain times and/or it may no longer be alive. Illustrations alone being used to designate type specimens is especially problematic, owing to mammals’ lack of meristic and other obvious distinguishing external characters. Hoaxes, the difficulty in determining that they are hoaxes, and various errors of taxonomic allocation appear to be especially common with names without preserved types. The Code should be revised to require preserved specimens as types for new names. Tissue samples alone for DNA analysis are not ideal for serving this purpose, but should be allowed to meet the requirement.
A good understanding (categorization) of the diversity and distribution of the tufted capuchin monkeys (Cebus) has proved to be extraordinarily intractable. Its lack is now hampering conservation efforts, for, despite them being, in general, wide-ranging and adaptable, their forests are being destroyed to the extent that many populations are now evidently seriously threatened. Conservation measures require that we know better their diversity not only to protect them in the wild but also to establish captive breeding programs. In this paper, we present some notes which resulted from our analysis of a recent published hypothesis regarding their systematics by C. P. Groves, in his influential synthesis Primate Taxonomy (2001). We are not presenting another hypothesis (taxonomy), but review aspects of some of the names and synonyms of Groves' taxonomy, and briefly discuss its concordance with the results of a largely unpublished PhD thesis of tufted capuchin systematics completed by Cecilia Torres de Assumpção in 1983.
Geographically isolated from other C. albifrons taxa found east of the Andes, the Ecuadorian capuchin (Cebus albifrons aequatorialis) is a Critically Endangered primate that survives in a small number of localities in western Ecuador and extreme northern Peru. We assessed 11 forested areas in western Ecuador to determine presence/absence using a combination of on-foot searching and interviews with local informants. C. a. aequatorialis were present at seven of the sites surveyed, four of which represent new presence localities. We carried out extensive censuses of five small, private reserves to obtain estimates of population density and demographic information. We also examined home range characteristics and habitat selection at one well-studied site. Population densities based on absolute counts at these sites ranged from 2-22 individuals/km 2 (median = 2.4). Jauneche, a 138 ha isolated fragment reserve with 22 individuals/km 2 , was a clear outlier. Although we observed some solitary individuals, C. a. aequatorialis live predominantly in multi-male multi-female social groups, with a mean group size of 13.9 (range 5-20). The composition of social groups was typical for Cebus: adult females outnumbered adult males slightly, and groups exhibited relatively high immature to adult female ratios (mean = 1.5). Home ranges were unusually large for the genus (507 – 561 ha). The capuchins exhibited strongest selection for mature forest near streams, although they also used degraded forest frequently. C. a. aequatorialis faces critical threats in the form of habitat loss, hunting, and harassment by farmers, but we suggest that some remaining populations have the potential to grow if effective protection can be established.
A good understanding (categorization) of the diversity and distribution of the tufted capuchin monkeys (Cebus) has proved to be extraordinarily intractable. Its lack is now hampering conservation efforts, for, despite them being, in general, wide-ranging and adaptable, their forests are being destroyed to the extent that many populations are now evidently seriously threatened. Conservation measures require that we know better their diversity not only to protect them in the wild but also to establish captive breeding programs. In this paper, we present some notes which resulted from our analysis of a recent published hypothesis regarding their systematics by C. P. Groves, in his influential synthesis Primate Taxonomy (2001). We are not presenting another hypothesis (taxonomy), but review aspects of some of the names and synonyms of Groves’ taxonomy, and briefly discuss its concordance with the results of a largely unpublished PhD thesis of tufted capuchin systematics completed by Cecília Torres de Assumpção in 1983.
A breeding programme for Yellow-breasted capuchin Cebus xanthosternos was initiated at the Rio de Janeiro Primate Centre [Centro de Primatologia do Rio de Janeiro (CPRJ)], Brazil, in 1980 when this monkey was considered highly threatened. In 1987, a field survey concluded that an urgent measure that should be taken to save the species was the expansion of the breeding programme at the CPRJ and the extension of the programme to other collections with expertise in breeding New World primates. Mulhouse Zoo, France, proposed that CPRJ should expand the breeding programme to Europe and that the participating zoos should be asked to fund in situ conservation. The breeding programme began in Europe in 1990 at Mulhouse Zoo. At the end of 2010, there were 140 Yellow-breasted capuchins at 21 European zoos. Since 2002, in situ conservation actions have provided important information about wild populations. The largest forest fragments, scattered across c. 470 000 km2 over Atlantic Forest, Cerrado and Caatinga, were visited, and wild groups were monitored in three of them. The findings from these studies help us to understand the basic ecology of this primate and to build a conservation action plan for the future.
A history of some details the author's research in eastern Colombia is presented for the last 27 years since 1977 in Vichada, Vaupés, Amazonas and most recently in Meta up to the present. Some comments are made about each research project in the context of primatology and some hypotheses and ideas of the author are presented about species, populations and other groups of mammals in the country. Especially discussed are aspects of Cebus albifrons and its relation to Sapajus (=Cebus) apella (a new taxonomic change) and the primates Calli cebus lugens, Alouatta seniculus, Lagothrix lagothricha, Cacajao melanocephalus, Callicebus caquetensis and Callicebus ornatus.
Naturalistic studies on tool use by nonhuman primates have focused almost exclusively on Old World monkeys or hominoids. We studied the cracking of Syagrus nuts with the aid of stones by a group of semifree-ranging capuchins living in a reforested area (Tietê Ecological Park, São Paulo, Brazil). Our data are from direct observation and from mapping nut-cracking site utilization. All adults, subadults and juveniles (plus one infant) crack nuts, but individual differences in frequency and proficiency are marked. Juveniles do most of the nut-cracking, but adults are, on average, more efficient; the frequency of inept stone manipulation decreases with age. About 10% of the nut-cracking episodes were watched by other individuals—mostly infants and juveniles, suggesting a role for observational learning, even if restricted to stimulus en-hancement. KEY WORDS: capuchin; foraging; tool use. Experimental studies and naturalistic observations on the use of tools by nonhuman primates brought important insights on the evolution of primate cognition and challenged the notion of the unique nature of human techno-logical capacities. Until recently, the studies were focused almost exclusively on Old World monkeys or apes (McGrew, 1992). Reports on the spontaneous use of tools by capuchins, date back to the writings of Gonzalo Fer andez de Oviedo in 1526 (cited by Urbani, 1998),
Personality has important links to health, social status, and life history outcomes (e.g. longevity and reproductive success). Human facial morphology appears to signal aspects of one’s personality to others, raising questions about the evolutionary origins of such associations (e.g. signals of mate quality). Studies in non-human primates may help to achieve this goal: for instance, facial width-to-height ratio (fWHR) in the male face has been associated with dominance not only in humans but also in capuchin monkeys. Here we test the association of personality (assertiveness, openness, attentiveness, neuroticism, and sociability) with fWHR, face width/lower-face height, and lower face/face height ratio in 64 capuchins (Sapajus apella). In a structural model of personality and facial metrics, fWHR was associated with assertiveness, while lower face/face height ratio was associated with neuroticism (erratic vs. stable behaviour) and attentiveness (helpfulness vs. distractibility). Facial morphology thus appears to associate with three personality domains, which may act as a signal of status in capuchins.
The morphological systematics of the tufted capuchins is confusing. In an attempt
to clarify the complex systematics and phylogeography of this taxon, we provide a first
molecular analysis. We obtained mitochondrial cytochrome oxidase II (mtCOII) gene sequences
from 49 tufted capuchins that had exact geographic origins from diverse lineages
in Colombia, Peru, Bolivia, French Guyana, Brazil, Argentina and Paraguay and
that belonged to clearly recognized morphological taxa. This project had 4 main findings:
(1) we determined 2 established and related taxa in the northern Amazon River
area, which we named C. a. apella and C. a. fatuellus . C. a. apella is distributed from
French Guyana until, at least, the Negro River in the northern Brazilian Amazon, whereas
C. a. fatuellus is distributed throughout the Colombian Eastern Llanos and the northern
Colombian Amazon. We also determined 2 other southern C. apella taxa, which we
named C. a. macrodon and C. a. cay . C. a. macrodon has a western and southern Amazon
distribution, while C. a. cay has a more southern distribution outside the Amazon basin.
(2) In the upper Amazon basin, there is a unique lineage (C. a. macrocephalus) with 1
widely distributed haplotype. The 4 morphological subspecies ( C. a. maranonis, C. a.
macrocephalus , C. a. peruanus, C. a. pallidus) , and maybe a fifth unknown subspecies,
described in this area were molecularly undifferentiated at least for the mitochondrial
gene analyzed. (3) Our molecular analysis determined that 1 individual of C. robustus fell
into the lineage of C. a. macrocephalus . Therefore, this form does not receive any specific name. (4) The animals classified a priori as C. nigritus and C. xanthosternos (because
of their morphological phenotypes and by their geographical origins) were clearly differentiated
from the other specimens analyzed with the molecular marker employed.
Therefore, we consider that these 2 lineages could be assigned the status of full species
following the biological species definition. (5) In 2001, Groves described 4 tufted capuchin
species (C. apella, C. libidinosus, C. nigritus and C. xanthosternos) , while Silva Jr. determined
7 species (C. apella, C. macrocephalus, C. libidinosus, C. cay, C. nigritus , C. robustus
and C. xanthosternos) . The tests of Swofford-Olsen-Waddell-Hillis, of Shimodaira and
Hasegawa and of Templeton did not fit with either of these two classificatory schemes,
although Groves’ scheme was better with regard to our data than that of Silva Jr. (6) All
the temporal splits among the tufted capuchin taxa studied were estimated to have occurred
during the last phase of the Pleistocene by using the � statistic applied to the
median joining haplotype network.
Capuchin monkeys (Sapajus spp.) in captive settings frequently manipulate and throw objects. In the wild, they may push or drop stones and sticks toward targets during inter- or intraspecific threat displays. In addition, female capuchin monkeys exhibit a broad repertoire of behaviors during their proceptive period, including facial expressions, vocalizations, stereotyped body postures, and touch-and-run behavior. This study reports stone throwing as a newly-described communicative behavior during the proceptive display of females in a group of bearded capuchin monkeys (S. libidinosus) in Serra da Capivara National Park, Brazil. During a two-year study, three females from one group were seen throwing stones at males during their proceptive phase. After this period, three other females in the same group exhibited the same behavior. Although it may be possible that this pattern is the result of several independent innovations by each female, the apparent absence of this behavior in other groups leads us to suggest that we have documented the diffusion of a new behavioral trait or tradition within this capuchin social group.
Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC metabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing "field extracts" for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest.
Capuchin monkeys occupy a wide range of habitats where they feed on fruits, arthropods, and vertebrates. Their large home ranges (80-900 ha) suggest that living in forest fragments may challenge their adaptability. We identified and quantified the main food items of Cebus libidinosus Spix, 1823 in forests fragments (100 ha) in southeastern Brazil. We recorded the feeding activities of two groups using scan sampling over a 13-month period. The diet was composed of fruits, crops, animal prey, seeds, plant matter and undetermined. Fruit was eaten more in the wet season than in the dry season,and maize and sugar-cane-consumption peaked in the early dry season. The proportion of fruit in the diet was positively correlated with fruiting intensity of zoochorous trees. The plant diet included 54 species, with maize, Rhamnidium elaeocarpus, Acrocomia aculeata, Guazuma ulmifolia and Cariniana, being most important. Although dietary composition and diversity were similar to capuchins in larger forest fragments, feeding on crops attained higher percentages at times when zoochorous fruit production was low in fragments.
Cebus olivaceus were studied in C Venezuela. Animals of both sexes were classed as infants during their 1st year, and juveniles until they reached 6 yr of age. Females reach sexual maturity at this time, while males were classed as subadults until they reached full adult size at age 12. Adulthood lasts at least 30 yr in females, at least 24 yr in males. Age-sex class specific mortality and fecundity rates generated a life table which indicated that the population was increasing (r=0.087) between 1977-1986. On average, non-adults made up 60% of a group; this percentage increased with group size. The strong female-biased adult sex ratio (1:4.4) was a consequence of a biased birth sex ratio (1:1.9), higher female than male survivorship especially between ages 3-7 when males were dispersing, and a pronounced sexual bimaturism. -from Author
A-503 contact-hr study of a 35-member group ofCebus albifrons was conducted in eastern Colombia in 1977 and 1978. The group had a female: male socionomic sex ratio of 2.5:1 and used a
home range of 110–120 ha which overlapped the home range of another group ofC. albifrons about 20–30 ha. The animals spent about 80% of their foraging time eating plant material and about 20% of their foraging
time eating animal materials. A birth peak at the end of the dry season extending into the wet season was indicated by data
available. Attempted predation was recorded by the mustelidEira barbara and the black-and-white hawk-eagleSpizastur melanoleucus. Some association was observed with the red howler monkeyAlouatta seniculus. The group at times spent more than half the day foraging and traveling on the ground, exhibiting a level of terrestriality
not reported for other New World primates.
The present study evaluated the efficacy of an adapted version of the Mollon-Reffin test for the behavioral investigation of color vision in capuchin monkeys. Ten tufted capuchin monkeys (Sapajus spp., formerly referred to as Cebus apella) had their DNA analyzed and were characterized as the following: one trichromat female, seven deuteranope dichromats (six males and one female), and two protanope males, one of which was identified as an "ML protanope." For their behavioral characterization, all of the subjects were tested at three regions of the Commission International de l'Eclairage (CIE) 1976 u'v' diagram, with each test consisting of 20 chromatic variation vectors that were radially distributed around the chromaticity point set as the test background. The phenotypes inferred from the behavioral data were in complete agreement with those predicted from the genetic analysis, with the threshold distribution clearly differentiating between trichromats and dichromats and the estimated confusion lines characteristically converging for deuteranopes and the "classic" protanope. The discrimination pattern of the ML protanope was intermediate between protan and deutan, with confusion lines horizontally oriented and parallel to each other. The observed phenotypic differentiation confirmed the efficacy of the Mollon-Reffin test paradigm as a useful tool for evaluating color discrimination in nonhuman primates. Especially noteworthy was the demonstration of behavioral segregation between the "classic" and "ML" protanopes, suggesting identifiable behavioral consequences of even slight variations in the spectral sensitivity of M/L photopigments in dichromats.
Delaying gratification involves 2 components: (1) delay choice (selecting a delayed reward over an immediate one) and (2) delay maintenance (sustaining the decision to delay gratification even if the immediate reward is available during the delay). Two tasks most commonly have explored these components in primates: the intertemporal choice task and the accumulation task. It is unclear whether these tasks provide equivalent measures of delay of gratification. Here, we compared the performance on the intertemporal choice task and the accumulation task of capuchin monkeys (Cebus apella) belonging to 2 study populations. We found only limited evidence of a significant correlation in performance. Consequently, in contrast to what is often assumed, our data provide only partial support for the hypothesis that these tasks provide equivalent measures of delay of gratification. (PsycINFO Database Record (c) 2013 APA, all rights reserved).
Humans can use hand tools smoothly and effectively in varying circumstances; in other words, skillfully. A few other species of primates crack encased foods using hammer tools and anvils. Are they skilled? Positioning the food on the anvil so that it does not fall off when struck is a component of skilled cracking. We discovered that bearded capuchin monkeys deliberately place palm nuts in a relatively stable position on the anvil before striking them. In the first experiment, we marked the meridians of palm nuts where they stopped when rolled on a flat surface ("Stop meridian"). We videotaped monkeys as they cracked these nuts on an anvil. In playback we coded the position of the Stop meridian prior to each strike. Monkeys typically knocked the nuts on the anvil a few times before releasing them in a pit. They positioned the nuts so that the Stop meridian was within 30 degrees of vertical with respect to gravity more often than expected, and the nuts rarely moved after the monkeys released them. In the second experiment, 14 blindfolded people (7 men) asked to position marked nuts on an anvil as if to crack them reliably placed them with the Stop meridian in the same position as the monkeys did. In the third experiment, two people judged that palm nuts are most bilaterally symmetric along a meridian on, or close to, the Stop meridian. Thus the monkeys reliably placed the more symmetrical side of the nuts against the side of the pit, and the nuts reliably remained stationary when released. Monkeys apparently used information gained from knocking the nut to achieve this position. Thus, monkeys place the nuts skillfully, strategically managing the fit between the variable nuts and pits in the anvil, and skilled placement depends upon information generated by manual action.
In most experimental work on animal cognition, researchers attempt to control for multiple interacting variables by training subjects prior to testing, allowing subjects to participate voluntarily, and providing subjects with food rewards. However, do such methods encourage selection bias from subjects' personalities? In this study, we trained eighteen zoo-housed capuchin monkeys (Sapajus apella) for two experiments, under conditions of positive reinforcement (i.e. food rewards) and free-choice participation. Using a combination of behavioral and rater-based methods, we identified and validated five personality dimensions in these capuchins (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness). Scores on Openness were positively related to individual differences in monkey task participation, reflecting previous work showing that such individuals are often more active, curious, and willing to engage in testing. We also found a negative relationship between scores on Assertiveness and performance on tasks, which may reflect the trade-offs between speed and accuracy in these animals' decision-making. Highly Assertive individuals (the most sociable within monkey groups) may also prioritize social interactions over engaging in research. Lastly, monkeys that consistently participated and performed well on both tasks showed significantly higher Openness and lower Assertiveness compared to others, mirroring relationships found between personality, participation, and performance among all participants. Participation and performance during training was clearly biased toward individuals with particular personalities (i.e. high Openness, low Assertiveness). Results are discussed in light of the need for careful interpretation of comparative data on animal cognition and the need for researchers to take personality selection bias more seriously.
The aim of this study was to evaluate whether an in vitro culture (IVC) medium containing either or not β-mercaptoethanol (BME), bone morphogenetic protein 4 (BMP4), or pregnant mare serum gonadotrophin (PMSG) could be able to promote the development of capuchin monkeys' preantral follicles enclosed in ovarian cortical strips. Follicular viability after IVC was similar to control (89.32%). Primordial follicle recruitment to primary stage was not reached with IVC, but the rate of secondary follicle formation was increased in the medium supplemented with BME, BMP4, and PMSG (44.86%) when compared to IVC control (9.20%). In the medium supplemented with BME, BMP4, and PMSG, contrary to other media, anti-müllerian hormone-messenger RNA (mRNA) expression in ovarian tissue was upregulated (3.4-fold), while that of growth differentiation factor-9 was maintained. The BMP4-mRNA expression, however, appeared downregulated in all cultured tissues. Our findings show a favorable effect of BME, BMP4, and PMSG on the in vitro development of secondary follicles from capuchin monkeys.
O tráfico de animais silvestres representa uma ameaça às populações naturais pelo impacto da perseguição e retirada de indivíduos da natureza, e, ainda, pelos riscos de estabelecimento de populações invasoras e disseminação de patógenos por meio de
solturas inadequadas. Este tipo de crime ambiental também é coresponsável
pela superlotação dos Centros de Triagem de Animais Silvestres (Cetas) do Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (Ibama) e conveniados. No presente estudo procurou-se analisar a origem, o destino e os táxons de primatas
brasileiros no tráfico nacional a partir dos registros de espécimes ingressos em Cetas ou Núcleos de Fauna (Nufaus). Aqueles espécimes de táxons exóticos à Unidade Federativa (UF) do Cetas receptor foram inferidos como oriundos de tráfico interestadual. Entre 1999 e 2006, 4.631 primatas dos 18 gêneros que ocorrem no Brasil, ingressaram em 53 Cetas e Nufaus de todas as UF do País, sendo Callithrix (54,2%) e Cebus (28,1%) os mais freqüentes. Dos espécimes identificados em nível de espécie/subespécie, Callithrix jacchus (24,2%) foi a espécie mais freqüente, seguida por Cebus apella (23,1%), Callithrix
penicillata (18,0%) e Callithrix geoffroyi (13,0%). Pelo menos 27,3% dos espécimes pertenciam a 31 táxons exóticos à UF receptora. Aquelas mesmas espécies mais freqüentemente receptadas em Cetas somaram 87,6% do total de indivíduos identificados dentre os exóticos, sendo, portanto, inferidos como os mais comuns no tráfico interestadual. As regiões que mais contribuíram com espécimes exóticos foram Norte
(49,6%) e Nordeste (28,1%), a maioria nativa dos biomas Amazônia (49,9%) e Mata Atlântica (31,1%). Os presentes dados corroboram uma rota preponderante de tráfico interestadual de primatas no sentido norte-sul, com relativamente baixa presença de espécies ameaçadas (<5%), e destacada parcela (45,1%) de espécies potencialmente
invasoras. Apesar de pressupor-se que a maioria dos animais traficados morra ou não seja interceptada, e do reconhecimento dos problemas de identificação taxonômica, os dados do presente estudo apresentam um panorama da composição taxonômica do tráfico nacional de primatas, suas principais origens e destinos.
The wildlife trafficking is a threat to natural populations because of the impact of persecution and removal of individuals from nature, and also the risk of establishment of invasive populations and spread of pathogens through improper releases. This type of environmental crime is also jointly responsible for the overcrowding of Screening Centers of Wild Animals (Cetas) of the Brazilian Institute of Environment and Renewable Natural Resources (Ibama) and associated institutions. The present study sought to examine the origin, destination and taxa of Brazilian primates in the national trafficking from the records of specimens ingress in Cetas or Fauna Nucleus (Nufaus). Those specimens which were from exotic taxa to the Federative Unit (FU) of the receptor Cetas were inferred as coming from interstate trafficking. Between 1999 and 2006, 4,631 primates of the 18 genera that occur in Brazil, entered into 53 Cetas and Nufaus and all FU in the country, being Callithrix (54.2%) and Cebus (28.1%) the most frequent. Specimens identified at the species / subspecies level, Callithrix jacchus (24.2%) was the most frequent species, followed by Cebus (23.1%), Callithrix penicillata (18.0%) and Callithrix geoffroyi (13.0 %). At least 27.3% of the specimens belonged to 31 taxa exotic to the receiving FU. Those same species most frequently received at the Cetas totaled 87.6% of all individuals identified among the exotic ones and are therefore inferred to be the most common in interstate traffic. Regions that contributed most with exotic specimens were Northern (49.6%) and Northeast (28.1%), the majority of native Amazonian biomes (49.9%) and Atlantic Rainforest (31.1%). The present data support a dominant route of interstate trafficking of primates in north-south direction, with relatively low presence of endangered species (<5%), and a substantial portion (45.1%) of potentially invasive species. Although it is assumed that the majority of trafficked animals die or are not intercepted, and the recognition of the problems of taxonomic identification, the data from this study provide an overview of the taxonomic composition of the domestic trafficking of primates, its origins and destinations.
Skilled motor actions are associated with handedness and neuroanatomical specializations in humans. Recent reports have documented similar neuroanatomical asymmetries and their relationship to hand preference in some nonhuman primate species, including chimpanzees and capuchin monkeys. We investigated whether capuchins displayed significant hand preferences for a tool-use task and whether such preferences were associated with motor-processing regions of the brain. Handedness data on a dipping tool-use task and high-resolution 3T MRI scans were collected from 15 monkeys. Capuchins displayed a significant group-level left-hand preference for this type of tool use, and handedness was associated with asymmetry of the primary motor cortex. Left-hand preferent individuals displayed a deeper central sulcus in the right hemisphere. Our results suggest that capuchins show an underlying right-hemisphere bias for skilled movement. Am. J. Primatol. 00:1-6, 2012. © 2012 Wiley Periodicals, Inc.
1 Grupo de Investigación en Biología Evolutiva (GIBE), Laboratorio 46, 4 • piso, Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad de Buenos Aires (UBA), Pabellón II -Ciudad Universitaria, Abstract The karyotype of the neotropical primate genus Cebus (Platyrrhini: Cebidae), considered the most ancestral one, shows the greatest amount of heterochromatin described among Platyrrhini genera. Banding techniques and restriction enzyme digestion have previously revealed great variability of quantity and composition of heterochromatin in this genus. In this context, we use fluorescence in situ hybridization (FISH) to analyse this genomic region and discuss its possible role in the diversification of Cebus. We used a heterochromatin probe for chromosome 11 of Cebus libidinosus (11qHe+ CLI probe), obtained by chro-mosome microdissection. Twenty-six specimens belonging to the families Atelidae, Cebidae, Callitrichidae and Pithecidae (Platyrrhini) were studied. Fourteen out of 26 specimens were Cebus (Cebidae) individuals of C. libidinosus, C. xanthoster-nos, C. apella, C. nigritus, C. albifrons, C. kaapori and C. olivaceus. In Cebus specimens, we found 6 to 22 positive signals located in interstitial and telomeric positions along the different species. No hybridization signal was observed among the remaining Ceboidea species, thus reinforcing the idea of a Cebus-specific heterochromatin composed of a complex system of repetitive sequences. Analysis of the heterochromatin of Cebus (Primates, Platyrrhini) by micro-FISH and banding pattern comparisons.
The geographic distribution of two congeneric monkeys (Cebus albifrons and C. apella) was studied in El Tuparro National Park in the llanos of eastern Colombia. Extensive trips were undertaken by land and river to collect 268 precisely located groups of these two species. The distributions of these monkeys were generally mutually exclusive and parapatric, contrasting with their known sympatry in closed-canopy rainforest farther to the south. The replacement of one species by the other was abrupt along the northern water courses in the park; however, the two species' ranges partially overlapped and contained islands of sympatry towards the southern parts of the park, where forests are more extensive. Along the rivers, C. albifrons was found in seasonally inundated forests and woodlands that were seldom entered by C. apella. Such inundatable vegetation was extensive in downriver sites in the typically flat llanos geography of this part of Colombia. Although some differential use of habitat was demonstrated, many forests containing the two species seemed essentially identical so that historical precedence, competition, or both may also be posited to partially explain the distributions, although this remains to be demonstrated.
In this chapter, we review some of the benefits and challenges of long-term primate field studies. We define long-term studies as those that cover a significant part of the study species' life cycle; in reality, many studies have already extended over multiple generations. We first provide a brief overview of the historical beginnings of modern primate field studies, most of which lay in the 1950s and early 1960s. Next, we identify a number of biological constraints and scientific questions that necessitate and justify a long-term approach to studying wild primate populations. Most research questions in this context are related to fitness determinants and outcomes and can be broadly classified as addressing either aspects of behavior, life history and demography, or the possible interactions among them. Positive side effects of long-term field projects on the conservation of the study site or the study species have recently become additional important reasons for the continuation of these projects. Studying individually known primates over years and decades also poses some unique challenges, however, especially with respect to data management and funding. We close this chapter by summarizing some of the unique insights about primate social systems and life history only made possible by the long-term nature of the studies, focusing on the chapters making up the remainder of this volume. © Springer-Verlag Berlin Heidelberg 2012. All rights are reserved.
Cebus and Saimiri, together with Callicebus and Aotus, represent four genera of New World monkeys whose unresolved taxonomic position has served to muddle platyrrhine cladistics. Their affinities remain somewhat problematic (Schneider and Rosenberger, this volume), although we argue that in the past 20 years, new molecular, genetic, morphological and behavioral analyses have narrowed the range of possible explanations regarding Cebus and Saimiri, in particular. Here, we attempt to clarify cebine evolutionary relationships and outline some interesting and relevant directions for future studies in behavior and ecology.
Animals kept in captivity are reliant on humans for their care and welfare. Enclosure design, and choice of group mates as well as routine husbandry events such as feeding, cleaning, and health care are in the hands of human keepers. It is therefore important to understand how external human-related husbandry events affect daily behaviour routines for animals, to help promote good welfare. Predictability (or lack thereof) of these routines can have profound effects on behaviours of captive animals. This study investigates whether providing a reliable predictable signal indicating entry into indoor brown capuchin (Sapajus apella) enclosures can increase welfare. All day focal follows of 12 zoo-housed capuchins were performed, recording behaviour in relation to husbandry events. The Baseline data show that unreliable sounds of door openings and closings outside the enclosure increase anxiety-related behaviours such as self-scratching, vigilance and jerky motions, and that the capuchins were startled by keepers entering the enclosure. A reliable signal (knocking) was subsequently introduced before enclosure entry and the monkeys given two weeks to associate the signal prior to Treatment condition data collection. The results indicate that the anxiety-related behaviours were reduced in the Treatment condition compared to Baseline frequencies. We conclude that making certain husbandry events reliable and predictable through the introduction of a unique signal can have a significant positive impact on the welfare of animals. Such an approach is not time consuming and costs nothing to implement, yet can result in significant advancements in animal welfare that can be implemented in a wide range of captive settings.
Conservation actions that effectively and efficiently target single, highly threatened species require current data on the species’ geographic distribution and environmental associations. The Ecuadorian capuchin (Cebus albifrons aequatorialis) is a critically endangered primate found only in the fragmented forests of western Ecuador and northern Peru, which are among the world’s most severely threatened ecosystems. We use the MAXENT species distribution modeling method to model the potential distribution and environmental associations of Cebus albifrons aequatorialis, using all known presence localities recorded within the last 2 decades as well as 13 climate, topography, vegetation, and land-use data sets covering the entire geographic range of the subspecies. The environmental conditions that our model predicted to be ideal for supporting Cebus albifrons aequatorialis included ≥20% tree cover, mild temperature seasonality, annual precipitation
Critical remarks by the late Dr. G. H. H. Tate (1954) regarding my identification of Cebus apella Linnaeus seem to be founded on a misunderstanding of the significance of certain external characters of the species and a misinterpretation of the terminology used for indicating those characters.
The original figure and description of Simia apella Linnaeus, 1766, reproduced by Tate (1954, Pl. 1) refers quite correctly to the animal all authors have held to be Cebus apella . My 1949 characterization of Cebus apella is based on the same figure as well as on large series of specimens from various museums and others accumulated by Dr. Remington Kellogg for his study of the species Cebus apella .
The basis for the difference of opinion is that Tate (1954: 415) points to one animal but holds in mind a totally different one when he states that C. apella is “an uncrested species and that the name appeared to be applicable to the common gray-brown species inhabiting the Guiana region, which Hershkovitz (p. 332 [1949]) refers to C. nigrivittatus castaneus .” Tate goes on to say (p. 417) that comparisons of the picture of the original C. apella “with the apella of Hershkovitz (1949: 325, Fig. 52) will, I think, forever still any doubt that Linnaeus had before him an uncrested Cebus monkey when he described Simia apella .”
Tate's concept of crested and uncrested species of Cebus is based solely on cranial characters and primarily on the presence or absence of a sagittal crest on the skull of the adult male (cf. Tate, 1939:210). Neither sex nor cranial characters of the original Simia apella are placed in evidence. Obviously, Tate confused his own term crested , referring to cranial characters, with his and my term, “tufted,” referring to …
The Ka'apor capuchin, Cebus kaapori, is perhaps the most endangered primate of the Brazilian Amazon. Endemic to a region with extreme intensification of habitat-degrading activities, it survives in remnant populations in a completely fragmented landscape. Before now, the only data available were isolated observations of feeding, locality records, and information on population densities and group size obtained during census. Here we present the first data on the activity budget, diet, and daily path length of the species, and compare our preliminary results with those for other capuchin monkeys. A group of nine Ka'apor capuchins was monitored over a period of four months during the dry season in the Goianésia do Pará municipality, Pará, Brazil. We used instantaneous scan sampling (n = 4,647 scans) to construct an activity budget for the monkeys, and we identified the plants in their diet to species level (n = 41 plant taxa), allowing us to compare dietary overlap with other gracile capuchin species, as well as with the robust capuchin (Sapajus spp.), a potential competitor present throughout the range of the Ka'apor capuchin. Like other species of gracile capuchins, C. kaapori was highly frugivorous, with the vast majority of the feeding records of arils and fruit pulp (74%), supplemented by arthropods (13%) and seeds (10%), although diet composition was highly variable across months. The group used a total area of 62.4 ha during the study period, and average daily path length was 2,173 m (±400 m), with the entire home range utilized in every month of the study. We found significant overlap in the diet of the Ka'apor capuchin and Sapajus, highlighting the urgency to increase knowledge of the ecological needs of C. kaapori and understand synergistic effects of sympatry with competitive species, increasing forest fragmentation, and widespread human impact on C. kaapori sustainability. Am. J. Primatol. © 2014 Wiley Periodicals, Inc.
Between-group contest competition and the relative importance of male resource defence have recently been suggested to have been previously underestimated. When males contribute to the defence of group-controlled resources, the quality of the home range may depend on the resource-holding potential of resident males. Among Argentine tufted capuchin monkeys, resident males defend access to high-quality food resources. Here I investigate consequences of this male-male cooperation for intergroup dominance relationships and home range quality. I recorded ranging behaviour for four habituated groups in Iguazu National Park to identify home ranges and core areas, and measured the availability of food species within botanical plots placed in these areas. I recorded the location and outcome of intergroup encounters and fitted predictive models using generalized estimating equations to assess the relative importance of male group size and location on the outcome, before performing linear mixed-effects modelling to identify long-term benefits of winning encounters. Relative male group size was the most important factor in determining the winner of encounters, outweighing the competitive advantage of ownership. The density of food species within the core area was not affected by the group's competitive ability, but core area size increased with male group size. Moreover, dominant groups were better able to defend their core area, and adjusting for the degree of home range overlap revealed that dominant groups may have higher per capita access to food. These results suggest that male-male cooperation in defence of food resources could ultimately increase female reproductive success. (c) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Brown capuchins (Cebus apella) at Raleighvallen Nature Preserve in Suriname have recently been discovered to exhibit object manipulation abilities in foraging, specifically frequent substrate use and a remarkable episode of tool use. The food items being processed with these exceptional skills are numerous species of morphologically diverse, thickly husked fruits, with fruit walls impenetrable even to the powerful jaws of C. apella. These fruit taxa, many in the Lecythidaceae, the Brazil nut family, are rare in Western Amazonia and Central America, regions in which capuchins have been most often studied. Based on extensive qualitative observations, we provide a preliminary description of this phenomenon within a natural history perspective.
The manipulative skills of brown capuchins in Suriname are poised to upheave current understandings of tool use and object manipulation in capuchins. Moreover, the implications of these findings for the cognitive evolution of human and nonhuman primates are significant. The capacity to use tools is considered one of the major achievements of our species and figures deeply in explanations for the origin of human intelligence and behavior. Many hold that tool and object manipulation, language, social skills, and morphology are linked in primate evolution. Given that unusually complex social and communication skills are not evident in capuchins, the proposed connection between the evolution of tool use, language, and social skills in human evolution is thereby weakened. Instead, our observations in Suriname support a paradigm premised on the concept of functionally and evolutionarily distinct brain modules, [tool use. evolution of intelligence, cognitive domain, chimpanzees, seedpredation]
Observations onCebus capucinus in 10 forests in Chiriqui, Panama, are reported. Troop size ranged from two to five in small forests to 20 or more in large
forests. A 10 week study was conducted in a coastal forest that contained a troop of 27 to 30Cebus. The troop’s daily path length was approximately 1.6 to 2.5 km and their home range was between 32 and 40 ha. TheCebus usually spent 50 to 70% of their day foraging and traveling. On one occasion, aCebus attacked anIguana, wrestled with it, eventually broke off 30 to 40 cm of its tail, and ate meat from the tail. The relations betweenCebus andSaimiri oerstedii, Alouatta palliata, and man are described.
Wild brown capuchins (Cebus apella) in Raleighvallen, Suriname forage on larvae hidden inside bamboo stalks via searching and extractive behaviours. We found that developing proficiency at obtaining larvae from bamboo stalks extends through several years of juvenescence. Older juveniles pass through a transition from a juvenile pattern to an adult pattern of foraging efficiency and diet selection. Whereas most studies have investigated the contribution of direct interactions between a naïve individual and a competent forager on the acquisition of foraging expertise, we focused on indirect social influence through foraging artefacts left in the habitat by conspecifics. Young individuals foraged at bamboo stalks more often shortly after than shortly before encountering bamboo segments previously opened by foragers to extract larvae. We discuss this result in terms of stimulus enhancement and social facilitation. In capuchins, learning how to forage on difficult foods does not necessarily occur in the presence of other group members, and social influences can be delayed in time and separate in space from others. This study provides an original view on how the gradual acquisition of foraging competence in brown capuchins is aided jointly by physical maturation and indirect social input that provides opportunities to practice appropriate foraging actions.
Male primates may immigrate into groups by peacefully joining the residents and taking up low-ranking positions in the hierarchy, or they may enter by force, challenging the resident males and attempting to drive them from high rank or from the group. Here we address the questions of how, when, and why immigrating male white-faced capuchins (C. capucinus) at Santa Rosa replace the former resident males of our groups, rather than simply joining them. We present data on 15 male replacements in 6 study groups tracked from 1984 through March 2004. During 11 aggressive takeovers, resident males were nearly always outnumbered by coalitions of invading males; lone resident males were particularly vulnerable. Both residents and invaders were wounded and infants often perished during or soon after takeovers. Male replacements also occur when resident males abandon their groups and males from neighboring groups 'waltz in' to become resident. Three such 'waltz in' replacements occurred during the study period. If we combine takeovers with 'waltz in' cases, replacements occur about every 4 years in our study groups, almost invariably during the dry season months of January to April, about 3-6 months before the annual peak in conceptions. In the years that groups are subject to takeovers, group composition includes significantly lower proportions of adult males than in no-takeover years. We conclude that: (1) the mechanism of male replacement is usually aggressive takeover, but sometimes abandonment of the group by prior resident males occurs; and (2) aggressive takeovers are more likely to happen when the group is vulnerable because it has a lower proportion of adult males, particularly when all co-resident males have emigrated, leaving only the alpha male in residence. Our long-term study shows that adult males need coalition partners not only to gain entry to a group but also to maintain their membership within it.
The study of primate socio-ecology is in transition. The general hypothesis that ecology affects social behavior is still accepted, but there has been much recent debate over how it does so and the extent to which other factors, such as sexual conflict and phylogeny, are responsible for some patterns of primate sociality. The most important general finding in socio-ecology from the past three decades has been the recognition of distinct kinds of food competition and their effects on social relationships. Indirect or scramble competition limits group size but has relatively little affect on social relationships, whereas aggressive or contest competition between group members promotes kin-based alliances. The benefits of living in groups are being reevaluated - lowering of predation risk in larger groups is widely assumed, but supporting data are sometimes difficult to evaluate. Whatever the benefits of group living, they fail to explain a distinctive primate feature: prolonged social relationships between the sexes even outside of the breeding period. Recently, infanticide by males has been suggested as the main reason females may seek out or tolerate permanent association with males in most primate species. Evaluating the relative contributions of food competition, predation risk, and infanticide avoidance in structuring primate social relationships remains a challenge for the future. Meanwhile, it is important to recognize that species may not show adaptive behavior when their environment changes rapidly. This limitation may become an important aspect of future primate studies as tropical habitats the world over become increasingly influenced by human activity.
In Parque Nacional Manuel Antonio, Costa Rica, an adult male Cebus capucinus was observed repeatedly hitting a venomous snake (Bothropsasper) with a branch. Initially a large dead branch overhanging the snake had been broken off in the course of aggressive displays to the snake by the adult and two subadult males. The snake's escape was apparently prevented by the weight of the fallen branch and possibly by the injuries caused by its fall. This is the first direct observation of a capuchin monkey in a natural habitat using a tool.
White-faced capuchins (Cebus capucinus) reside in multimale–multifemale groups charac-terized by female philopatry and frequent male dispersal. However, over the years we have observed five females immigrate into our study groups and 23 disappear/emigrate. We exam-ined long-term demographic and behavioural data on three groups of C. capucinus residing in Santa Rosa, Costa Rica, between 1986 and 2007. During this time, 56 females resided in our study groups and as of June 2007, 23 were still present, ten were confirmed/presumed dead and 23 were missing. Here we review the circumstances surrounding the five immigra-tions and 23 missing females and evaluate three main hypotheses to explain female dispersal in a female philopatric species: inbreeding avoidance, reduction of intragroup feeding com-petition and infanticide avoidance. The two main predictions of the inbreeding avoidance hypothesis were not supported by our study; male tenure did not exceed female age at first birth and the majority of dispersers were parous females. The reduction in intragroup feeding competition hypothesis received moderate support; dispersing/disappearing females tend to leave during the dry season and they have fewer matrilineal kin than females remaining in their natal group. Our data were most consistent with the infanticide avoidance hypothesis in that females are more likely to disperse/disappear during years with male replacements, a time when infant deaths are also more common. These data provide further evidence of the large impact that the movement and actions of adult male white-faced capuchins have on the lives of females in this species.
and Summary
The mating system of wild brown capuchin monkeys, Cebus apella , was studied during four years in Peruvian rainforest. The most striking feature of estrus is active continuous solicitation of males by females. During the first three to four days, the female continuously follows the dominant male of the group, approaching him with grimaces, distinctive vocalizations, and submissive‐like postures. Although the female frequently attempts to initiate copulations by touching the male and running away, he rarely copulates with her more than once a day. On the next to last day of estrus, the female no longer follows the dominant male closely, and begins to solicit copulations from subordinate males. The dominant male then begins following the female and aggressively preventing other males from approaching her; during the remainder of the estrous period, male‐male aggression is infrequent compared to other polygamous primates. After another half a day, the dominant male stops following the estrous female, who then rapidly solicits and copulates with up to six subordinate males in a single day. Estrous behaviors disappear after 5 to 6 days.
The frequency and intensity of female pre‐ and post‐copulatory behaviors are significantly greater with dominant than subordinate males. Copulation duration is significantly longer in dominant males than subordinates. The dominant male has a greater frequency of copulation than any subordinate male and furthermore may have almost exclusive access to the female during the most probable days of ovulation.
The strong active solicitation by the female of the dominant male may be explained by direct benefits that she or her offspring might receive from him. Because the dominant male controls access to many food sources during periods when food is scarce, his tolerance of a particular female or her offspring could be an important component of fitness for them. It may be possible to extend this correlation between ecology and mating system to other primate species.
Zusammenfassung
Während der ersten drei oder vier Brunsttage folgen weibliche Kapuzineraffen ( Cebus apella ) ununterbrochen dem dominanten Männchen ihrer Gruppe und nähern sich ihm mit besonderen Gesichtsausdrücken, Lautgebungen und Gesten. Das dominante Männchen kopuliert mit einem Weibchen selten öfter als einmal pro Tag, auch wenn es häufiger zur Paarung aufgefordert wird, indem das Weibchen ihn berührt und wegläuft. Etwa ab dem vierten Brunsttag folgt das Weibchen dem dominanten Männchen nicht mehr, sondern beginnt rangtiefere Männchen zur Kopulation aufzufordern. Jetzt aber folgt ihm das dominante Männchen und hindert andere Männchen daran, sich dem Weibchen zu nähern. Am Ende des vierten Tages jedoch hört das dominante Männchen auf, dem Weibchen zu folgen. Darauf kann das brünstige Weibchen bis zu 6mal am Tag rangtiefere Männchen zur Paarung auffordern. Das typische Brunstverhalten endet nach vier bis sechs Tagen.
Das brünstige Weibchen zieht das dominante Männchen den rangtieferen Männchen vor (in der Häufigkeit und Intensität der Kopulationsaufforderungen). Die Paarung mit einem dominanten Männchen dauert signifikant länger als die mit einem untergeordneten Männchen. Das dominante Männchen kopuliert häufiger als jedes andere Männchen und hat den alleinigen Zugang zum Weibchen während der Tage mit der höchsten Ovulationswahrscheinlichkeit.
Vorteile, die das Weibchen oder deren Nachkommen gewinnen, könnten die ausgeprägte Paarungsaufforderung an das dominante Männchen erklären. Da das dominante Männchen den Zugang zu vielen Futterquellen beherrscht, könnte die Duldung eines bestimmten Weibchens und seiner Nachkommen stark zu deren Fitness beitragen. Möglicherweise können die Paarungssysteme anderer Primaten ebenfalls mit deren Ökologie in Zusammenhang gebracht werden.