Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli. Am. J. Primatol. 74:299314, 2012. (c) 2011 Wiley Periodicals, Inc.

Distribution, ecology, life history, genetic variation, and risk of extinction of nonhuman primates from Costa Rica

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.

Field methods for capture and measurement of three monkey species in Costa Rica.

A total of 54 free-ranging monkeys were captured and marked in Santa Rosa National Park, Costa Rica, during May 1985, and an additional 17 were captured during March 1986. The animals were darted using a blowpipe or a CO2 gun. The drugs used were Ketaset, Sernylan and Telazol. Ketaset was effective for Cebus capucinus but unsuccessful for Alouatta palliata and Ateles geoffroyi. Sernylan was successful for A. geoffroyi and A. palliata but is no longer commercially available. Telazol proved to be an excellent alternative capture drug for both A. palliata and A. geoffroyi.

Stable isotope ratios indicate diet and habitat use in New World monkeys.

This paper demonstrates the use of stable isotope ratios of carbon and nitrogen in animal tissue for indicating aspects of species behavioral strategy. We analyzed hair from individuals representing four species of New World monkeys (Alouatta palliata, the mantled howler; Ateles geoffroyi, the spider monkey; Cebus capucinus, the capuchin; and Brachyteles arachnoides, the woolly-spider monkey or muriqui) for delta 13C and delta 15N using previously developed methods. There are no significant differences in either carbon or nitrogen ratios between sexes, sampling year, or year of analysis. Seasonal differences in delta 13C reached a low level of significance but do not affect general patterns. Variation within species was similar to that recorded previously within single individuals. The omega 13C data show a bimodal distribution with significant difference between the means. The two monkey populations living in an evergreen forest were similar to each other and different from the other two monkey populations that inhabited dry, deciduous forests. This bimodal distribution is independent of any particular species' diet and reflects the level of leaf cover in the two types of forest. The delta 15N data display three significantly different modes. The omnivorous capuchins were most positive reflecting a trophic level offset. The spider monkeys and the muriquis were similar to one another and significantly more positive than the howlers. This distribution among totally herbivorous species correlates with the ingestion of legumes by the howler monkey population. In combination, these data indicate that museum-curated primate material can be analyzed to yield information on forest cover and diet in populations and species lacking behavioral data.

Characterization of Opsin Gene Alleles Affecting Color Vision in a Wild Population of Titi Monkeys (Callicebus brunneus)

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus. Am. J. Primatol. 73:189-196, 2011. (C) 2010 Wiley-Liss, Inc.

A Mechanical Analysis of Suspensory Locomotion in Primates and Other Mammals

For primates, and other arboreal mammals, adopting suspensory locomotion represents one of the strategies an animal can use to prevent toppling off a thin support during arboreal movement and foraging. While numerous studies have reported the incidence of suspensory locomotion in a broad phylogenetic sample of mammals, little research has explored what mechanical transitions must occur in order for an animal to successfully adopt suspensory locomotion. Additionally, many primate species are capable of adopting a highly specialized form of suspensory locomotion referred to as arm-swinging, but few scenarios have been posited to explain how arm-swinging initially evolved. This study takes a comparative experimental approach to explore the mechanics of below branch quadrupedal locomotion in primates and other mammals to determine whether above and below branch quadrupedal locomotion represent neuromuscular mirrors of each other, and whether the patterns below branch quadrupedal locomotion are similar across taxa. Also, this study explores whether the nature of the flexible coupling between the forelimb and hindlimb observed in primates is a uniquely primate feature, and investigates the possibility that this mechanism could be responsible for the evolution of arm-swinging.

To address these research goals, kinetic, kinematic, and spatiotemporal gait variables were collected from five species of primate (Cebus capucinus, Daubentonia madagascariensis, Lemur catta, Propithecus coquereli, and Varecia variegata) walking quadrupedally above and below branches. Data from these primate species were compared to data collected from three species of non-primate mammals (Choloepus didactylus, Pteropus vampyrus, and Desmodus rotundus) and to three species of arm-swinging primate (Hylobates moloch, Ateles fusciceps, and Pygathrix nemaeus) to determine how varying forms of suspensory locomotion relate to each other and across taxa.

From the data collected in this study it is evident the specialized gait characteristics present during above branch quadrupedal locomotion in primates are not observed when walking below branches. Instead, gait mechanics closely replicate the characteristic walking patterns of non-primate mammals, with the exception that primates demonstrate an altered limb loading pattern during below branch quadrupedal locomotion, in which the forelimb becomes the primary propulsive and weight-bearing limb; a pattern similar to what is observed during arm-swinging. It is likely that below branch quadrupedal locomotion represents a “mechanical release” from the challenges of moving on top of thin arboreal supports. Additionally, it is possible, that arm-swinging could have evolved from an anatomically-generalized arboreal primate that began to forage and locomote below branches. During these suspensory bouts, weight would have been shifted away from the hindlimbs towards forelimbs, and as the frequency of these boats increased the reliance of the forelimb as the sole form of weight support would have also increased. This form of functional decoupling may have released the hindlimbs from their weight-bearing role during suspensory locomotion, and eventually arm-swinging would have replaced below branch quadrupedal locomotion as the primary mode of suspensory locomotion observed in some primate species. This study provides the first experimental evidence supporting the hypothetical link between below branch quadrupedal locomotion and arm-swinging in primates.

Food Competition in a Semi-Free-Ranging Cebus apella Group

The competitive regime faced by individuals is fundamental to modelling the evolution of social organization. In this paper, we assess the relative importance of contest and scramble food competition on the social dynamics of a provisioned semi-free-ranging Cebus apella group (n=18). Individuals competed directly for provisioned and clumped foods. Effects of indirect competition were apparent with individuals foraging in different areas and with increased group dispersion during periods of low food abundance. We suggest that both forms of competition can act simultaneously and to some extent synergistically in their influence on social dynamics; the combination of social and ecological opportunities for competition and how those opportunities are exploited both influence the nature of the relationships within social groups of primates and underlie the evolved social structure. Copyright (c) 2008 S. Karger AG, Basel

Immunocytochemical characterization of the pregeniculate nucleus and distribution of retinal and neuropeptide Y terminals in the suprachiasmatic nucleus of the Cebus monkey

Circadian rhythms generated by the suprachiasmatic nucleus (SCN) are modulated by photic and non-photic stimuli. In rodents, direct photic stimuli reach the SCN mainly through the retinohypothalamic tract (RHT), whereas indirect photic stimuli are mainly conveyed by the geniculohypothalamic tract (GHT). In rodents, retinal cells form a pathway that reaches the intergeniculate leaflet (IGL) where they establish synapses with neurons that express neuropeptide Y (NPY), hence forming the GHT projecting to the SCN. In contrast to the RHT, which has been well described in primates, data regarding the presence or absence of the IGL and GHT in primates are contradictory. Some studies have suggested that an area of the pregeniculate nucleus (PGN) of primates might be homologous to the IGL of rodents, but additional anatomical and functional studies on primate species are necessary to confirm this hypothesis. Therefore, this study investigated the main histochemical characteristics of the PGN and the possible existence of the GHT in the SCN of the primate Cebus, comparing the distribution of NPY immunoreactivity, serotonin (5-HT) immunoreactivity and retinal terminal fibers in these two structures. The results show that a collection of cell bodies containing NPY and serotonergic immunoreactivity and retinal innervations are present within a zone that might be homologous to the IGL of rodents. The SCN also receives dense retinal innervations and we observed an atypical distribution of NPY- and 5-HT-immunoreactive fibers without regionalization in the ventral part of the nucleus as described for other species. These data may reflect morphological differences in the structures involved in the regulation of circadian rhythms among species and support the hypothesis that the GHT is present in some higher primates (diurnal animals). (C) 2009 Elsevier B.V. All rights reserved.

Evidence of reciprocal connections between the dorsal raphe nucleus and the retina in the monkey Cebus apella

Possible connections between the retina and the raphe nuclei were investigated in the monkey Cebus apella by intraocular injection of cholera toxin B subunit (CTb). CTb-positive fibers were seen in the lateral region of the dorsal raphe nucleus (DR) on the side contralateral to the injection, and a few labeled perikarya were observed in the lateral portion of the DR on the ipsilateral side. Our findings suggest that direct and reciprocal connections between the retina and DR may exist in Cebus apella. These connections might be part of an important pathway through which the light/dark cycle influences the Activity and/or functional status of raphe neurons, with potential effects on a broad set of neural and behavioral circuits. (c) 2007 Elsevier Ireland Ltd. All rights reserved.

Rod bipolar cells in the retina of the capuchin monkey (Cebus apella): Characterization and distribution

Rod bipolar cells in Cebus apella monkey retina were identified by an antibody against the alpha isoform of protein kinase C (PKC alpha). which has been shown to selectively identify rod bipolars in two other primates and various mammals. Vertical sections were used to confirm the identity of these cells by their characteristic morphology of dendrites and axons. Their topographic distribution was assessed in horizontal sections; counts taken along the dorsal, ventral, nasal, and temporal quadrants. The density of rod bipolar cells increased from 500 to 2900 cells/mm(2) at 1 mm from the fovea to reach a peak of 10,000-12,000 cellss/mm(2) at 4 mm, approximately 5 deg of eccentricity, and then gradually decreased toward retinal periphery to values of 5000 cells/mm(2) or less. Rod to rod bipolar density ratio remained between 10 and 20 across most of the retinal extension. The number of rod bipolar cells per retina was 6,360,000 +/- 387,433 (mean +/- S.D., n = 6). The anti-PKC alpha antibody has shown to be a good marker of rod bipolar cells of Cebus, and the cell distribution is similar to that described for other primates. In spite of the difference in the central retina, the density variation of rod bipolar cells in the Cebus and Macaca as well as the convergence from rod to rod bipolar cells are Generally similar, suggesting that both retinae stabilize similar sensitivity (as measured by rod density) and convergence.

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp, thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.

Distribuição e conservação do macaco-prego (Cebus nigritus - Goldfuss, 1809) e documentação do conhecimento ecológico local na região do Parque Estadual de Itapeva e arredores, Rio Grande do Sul e Santa Catarina, Brasil

A falta de informações sobre a distribuição e status do macaco-prego (Cebus nigritus) no Estado do Rio Grande do Sul e Santa Catarina, Brasil, dificulta os trabalhos de conservação da espécie. Estudos sobre as relações das populações humanas locais com os animais silvestres são raros, porém interessantes, pois através destes estudos torna-se possível reconhecer o conhecimento e as atitudes dessas populações frente a estes animais. O presente estudo visa contribuir com informações sobre a distribuição de C. nigritus e o conhecimento ecológico local sobre a mastofauna na região do Parque Estadual de Itapeva (PEVA) e arredores, Rio Grande do Sul e Santa Catarina, Brasil. De junho de 2004 a fevereiro de 2006, foram realizadas entrevistas e coletados relatos da população residente no entorno de 36 fragmentos, os quais indicaram: a) presença de C. nigritus em 20 fragmentos; b) ausência do mesmo em 16; c) captura, caça e suplementação alimentar como principais atividades humanas afetando a espécie. De outubro de 2004 a fevereiro de 2006, foram realizadas expedições a campo, nas quais a presença da espécie foi confirmada em 13 fragmentos e o fornecimento de alimentação de origem antrópica foi registrado em dois destes. A interação de C. nigritus com cultivos foi citada por moradores para sete fragmentos, porém não se obteve o registro da mesma em nenhum deles. Oito métricas relacionadas à área, forma, isolamento e matriz dos 36 fragmentos foram analisadas. Para três dessas métricas (área, índice da forma e índice de proximidade) a diferença entre fragmentos onde a espécie está presente e fragmentos onde está ausente foi significativa. A análise multivariada das oito medidas também apresentou diferença significativa entre esses dois grupos de fragmentos. A dinâmica de sobrevivência de C. nigritus na região estudada é complexa e provavelmente a manutenção de suas populações seja dependente do conjunto de fragmentos na paisagem, sendo possível que as mesmas constituam uma metapopulação. Através de visitas a instituições mantenedoras de C. nigritus em cativeiro no Rio Grande do Sul e de informações obtidas através de instrumentos de mídia popular e de divulgação científica, foi realizado um levantamento sobre: a) condições oferecidas em cativeiro; b) ações, em nivel regional, de apreensão e soltura por órgãos de fiscalização ambiental. As principais deficiências nas condições de cativeiro foram a dieta oferecida, a superlotação e a falta de enriquecimento ambiental nos recintos. Parece comum a relocação, sem planejamento e monitoramento, por instituições mantenedoras e órgãos de fiscalização ambiental. Com relação ao conhecimento da população local sobre a mastofauna da região do PEVA e arredores, os resultados revelaram que a comunidade analisada sabe reconhecer as espécies que compunham e/ou ainda compõem a mastofauna local e possui alguns conhecimentos a respeito da biologia geral destes animais. Ainda, as entrevistas e relatos demonstraram que a situação de ocorrência e abundância dessas espécies, no passado e no presente, está relacionada à: pressão de caça, pressão de captura, destruição do habitat e construção da rodovia RS-389. Assim sendo, atividades cruciais para um programa de conservação das populações remanescentes da fauna silvestre incluem: a) o desenvolvimento de ações de educação ambiental na região do PEVA e arredores; b) a revisão do status regional de conservação de C. nigritus; c) a criação e manutenção de unidades de conservação e corredores ecológicos; d) a inibição eficaz do comércio ilegal de animais silvestres; e) a capacitação dos agentes fiscalizadores dos órgãos ambientais para a realização adequada de relocações. Ainda, ressalta-se a importância de considerar os conhecimentos da população humana local no planejamento de ações conservacionistas como passo fundamental para que estas obtenham sucesso.

Behavioral study of Cebus nigritus (Goldfuss, 1809) (Primates, Cebidae) in captivity

The objective of this study was to describe the behavior of Cebus nigritus kept in captivity. The work, carried out during the month of March 2008 at "Dr. Belrio Guimaraes Brandao" County Zoo in GarYa- SP and Monte Alegre Farm Ecological Park in Telemaco Borba- PR, included 48 hours of observations, divided equally in four daytime periods. The behavioral catalogue used was constituted of different categories such as: foraging, feeding, locomotion, rest, social interaction, physical care, alertness, manipulation of things, reproductive behavior and stereotyped behavior. Animals showed activities of foraging, feeding, and locomotion and social interaction in low percentages in the two morning periods; however, their frequencies increased in the afternoon. Other activities like physical care, alertness and stereotyped behavior appeared mainly in the two morning periods, but were reduced in the afternoon. The rest category was more evident early morning and late afternoon. Since the stereotypical behavior presented high percentages, this study recommends that the number of individuals be diversiied in the social organization of the groups and that environment enriching activities be developed in captivity, creating situations similar to the animal's natural habitat.

Hierarquia de dominância durante a obtenção de Alimento em cebus apella e cebus libidinosus em Cativeiro

The analysis of the index of hierarchy and structural models of the formation of groups allowed to establish the hierarchical position of members of two groups of the genus Cebus. By the analyses of the hierarchical positions and the application of tests to obtain a food resource (TORA), we know the difference between these groups and groups in the wild. The results show a high ranking for both Cebus apella, as well as Cebus libidinosus. The results have enabled us to establish that the hierarchical structure in groups of Cebus in captivity: a) can be fixed and rigid different from highly flexible hierarchical structure studied in groups of wild b) even which similar hierarchy indices, there are differences in the hierarchical structure presents between C. apella and C. libidinosus in captivity c) hierarchy directly influence the behavioral patterns of obtaining food in Cebus