Differential habitat use byCebus apella andSaimiri sciureus in central surinam

Cebus apella, the black-capped or tufted capuchin, andSaimiri sciureus, the squirrel monkey, are frequently found in mixed species feeding and foraging groups throughout tropical South America and have been reported previously to show marked differences in techniques of insect foraging. Individuals of these taxa observed in central Surinam show numerous additional species-specific differences in other aspects of habitat utilization including gross dietary preferences, utilization of forest strata, locomotor behavior and arboreal support preferences.Cebus apella is more frugivorous, frequents the middle and lower levels of the main canopy, is predominantly quadrupedal and moves on medium-sized arboreal supports. By contrast, the smallerSaimiri sciureus is more insectivorous, frequents the lower strata of the forest, is more saltatory and moves on the smallest arboreal supports. Many of these differences in habitat use are interrelated and accord with patterns of habitat use seen in other primate taxa. The differences betweenCebus apella andSaimiri sciureus also accord with the types of behavioral differences frequently associated with differences in body size.     

Canine Dimorphism and Interspecific Canine Form in Cebus

I investigated canine dimorphism and interspecific canine form in adult specimens from 4 capuchin species (Cebus albifrons, C. apella, C. capucinus, and C. olivaceus). I used various univariate and multivariate statistics, which are based on 6 variables, to test several hypotheses that are based upon the finding that canine dimorphism is strongly associated with intermale competition in platyrrhines (Kay et al., 1988), Greenfield (1992a), Plavcan and van Schaik (1992, 1994). Results from the indices of canine dimorphism and the unpaired t-tests corroborate the prediction that males of each species possess significantly larger canines than those of females. Large male canines are especially prominent in 2 variables, maxillary and mandibular canine height. Greene's t-test (1989) does not support the prediction that Cebus apella and C. olivaceus possess a larger degree of canine dimorphism relative to C. albifrons and C. capucinus. No interspecific differences in degree of canine dimorphism are indicated by this test. Results of the discriminant function analyses (DFA) do not find that Cebus apella and C. olivaceus possess different canine form relative to C. albifrons and C. capucinus as predicted. However, Cebus apella is differentiated from the untufted capuchins (C. albifrons, C. capucinus, and C. olivaceus) by the DFA. I suggest that intermale competition is the primary selective force underlying the observed morphological patterns; however, it does not explain all the variation associated with canine dimorphism in Cebus.     

Chromosome comparison among five species of platyrrhini (Alouatta caraya,Aotus azarae,Callithrix jacchus,Cebus apella,andSaimiri sciureus)

Karyotypes of 82 individuals from five Platyrrhini species (Alouatta caraya, Aotus azarae, Callithrix jacchus, Cebus apella, andSaimiri sciureus) were studied and compared using a G-banding technique. Cytogenetic analysis showed full chromosome or full arm homologies among these geographically neighbouring species. A small number of chromosomal rearrangements (inversions, deletions, and translocations) could be detected among these taxa. These five species are closely related in chromosomal evolution. An interesting correspondance was found betweenCebus apella chromosomes and those of the other four species.Alouatta caraya andCebus apella are the closest species.Callithrix jacchus andAotus azarae would have the most separated karyotypes.     

Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus)

There are potential advantages of housing primates in mixed species exhibits for both the visiting public and the primates themselves. If the primates naturally associate in the wild, it may be more educational and enjoyable for the public to view. Increases in social complexity and stimulation may be enriching for the primates. However, mixed species exhibits might also create welfare problems such as stress from interspecific aggression. We present data on the behavior of single and mixed species groups of capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus) housed at the Living Links to Human Evolution Research Centre in the Royal Zoological Society of Scotland's Edinburgh Zoo. These species associate in the wild, gaining foraging benefits and decreased predation. But Cebus are also predators themselves with potential risks for the smaller Saimiri. To study their living together we took scan samples at ≥15 min intervals on single (n=109) and mixed species groups (n=152), and all occurrences of intraspecific aggression and interspecific interactions were recorded. We found no evidence of chronic stress and Saimiri actively chose to associate with Cebus. On 79% of scans, the two species simultaneously occupied the same part of their enclosure. No vertical displacement was observed. Interspecific interactions were common (>2.5/hr), and equally divided among mildly aggressive, neutral, and affiliative interactions such as play. Only one aggressive interaction involved physical contact and was non‐injurious. Aggressive interactions were mostly (65%) displacements and vocal exchanges, initiated almost equally by Cebus and Saimiri. Modifications to the enclosure were successful in reducing these mildly aggressive interactions with affiliative interactions increasing in frequency and diversity. Our data suggest that in carefully designed, large enclosures, naturally associating monkeys are able to live harmoniously and are enriched by each other. Am. J. Primatol. 72:33–47, 2010. © 2009 Wiley‐Liss, Inc.     

Influence of Fruit Availability on Ecological Overlap among Four Neotropical Primates at Tinigua National Park,Colombia1

Data on fruit abundance and ecological overlap among Ateles belzebuth, Lagothrix lagothricha, Cebus apella, andAlouatta seniculus were gathered during 13 months at Tinigua National Park (Colombia), in an effort to test the following hypotheses concerning competition for fruits. Coexistence is possible because: (1) during periods when fruit availability is limited, the species utilize different resources; and (2) the species have different fruit preferences independent of fruit production in the forest. Differences were found in resource use (diet and habitat) for all four species. Despite these differences, all four devoted large proportions of time feeding on fruit. Fruit abundance influenced their activity patterns. Ninety percent of all interspecific aggressive interactions (TV = 69) were seen in fruiting trees. The first hypothesis was best supported, given that all species significantly increased their intake of the vegetative parts of plants during periods of fruit scarcity. Fruit partitioning during periods of scarcity was observed clearly only for one pair of species (C. apella and L. lagothricha). In general, the second hypothesis was not supported as a mechanism for reducing competition because most fruit species were consumed by more than one primate species. Fruit preferences, however, may be particularly important in explaining differences in niche overlap between the most ecologically similar species: A. belzebuth relied heavily on the fruits of one palm species (Oenocarpus bataud) during periods of fruit scarcity and abundance, while L. lagothricha completely ignored this fruit.     

Milk composition of captive tufted capuchins (Cebus apella)

Little is known about the milk composition of nonhuman primates, and it has never been examined in capuchin monkeys (genus Cebus). This article reports on the macronutrient milk composition (fat, crude protein (CP), lactose, dry matter (DM), and total gross energy (GE)) of captive housed tufted capuchins (Cebus apella) (n=8). C. apella milk averaged 5.22% fat, 2.40% CP, 6.94% lactose, 16.48% DM, and 0.89 kcal/g. Fat was the most variable macronutrient and was significantly higher in samples collected after 2 months of lactation. To explore the adaptive significance of C. apella milk composition, results were compared with data on milk composition from a closely related cebid, Saimiri boliviensis boliviensis, and another large‐brained anthropoid, Homo sapiens. C. apella milk was only significantly different from Saimiri milk in CP and the proportion of energy from CP. Compared with human milk, C. apella milk was lower in lactose but higher in fat, CP, DM, GE, and the proportion of energy from CP. Results from this small dataset suggest that among anthropoid primates, the macronutrient composition of milk is influenced by phylogeny, may vary relative to infant growth rates, but may not be related in any direct way to relative brain size. Am. J. Primatol. 72:81–86, 2010. © 2009 Wiley‐Liss, Inc.     

Assessing habitat utilization by neotropical primates: a new approach

This study aims to ascertain habitat utilization, in relation to forest structural variation, by a multi-species group of primates in tropical lowland rainforest in Southeast Peru during dry season. A new approach to assessing habitat utilization was used. Habitat variation was described by structural and indicator variables collected in quadrats along transects through a study area within Terra Firme and Floodplain forest. Variables were grouped into ‘factors’ accounting for most of the variation by means of a Principal Components Analysis (PCA). Presence or absence of the primates within the quadrats, assessed by repeat transect surveys, was taken to indicate habitat preferences. Discrimination between the habitat and forest structure in areas of primate presence as opposed to absence was carried out by means of Discriminant Function Analysis (DFA). This highlighted patterns in most utilized habitat. Vertical utilization of the forest was also assessed along with presence in bamboo and general activity on encounter. Suggestions of habitat preference and utilization are made for each of the six sympatric species studied, based on significantly discriminating habitat factors, vertical stratification on encounter and relationships with bamboo.Saguinus fuscicollis andCebus moloch appeared as habitat generalists.Cebus apella, Saimiri sciureus, andAotus spp., exhibited varying degrees of preference for habitat factors suggesting disturbed forest,Cebus albifrons was more generalistic but with a possible association with primary, naturally disturbed forest.C. appella was encountered in Terra Firme forest significantly more than in Floodplain. ForS. sciureus, C. moloch, andC. apella, upper understory was the most utilized forest layer, forC. albifrons, middle canopy and forS. sciureus andAotus spp., lower understory. Both positive and negative relationships with bamboo were highlighted. Significant positive relationships betweenAotus spp., and bamboo suggest dense bamboo stands provide important daytime resting sites for this nocturnal species.C. moloch was also shown to utilize bamboo whereasS. fuscicollis appeared to actively avoid it. High levels of conformity with past studies in terms of habitat utilization patterns described for the species studied supports the conclusion that the methods used in this study provide an effective means of assessing primate habitat utilization within complex habitat.     

Craniodental biomechanics and dietary toughness in the genus Cebus

The tufted capuchin (Cebus apella) has been used in a number of comparative studies to represent a primate with craniofacial morphology indicative of hard-object feeding. Researchers have specifically referred to the tufted capuchin as a seed predator. Craniofacial features exhibited by the tufted capuchin, such as thick cortical bone in the mandibular corpus and symphysis, and a broad face associated with large masticatory muscles, permit the production and dissipation of relatively high masticatory forces. These morphologies, however, cannot distinguish between the tufted capuchin's propensity to exert higher forces when opening food with its anterior dentition or with its cheek teeth. It is also unclear whether these are adaptations for biting or chewing foods. This study uses a constrained lever model to compare the masticatory adaptations of C. apella to other cebids and atelids. Results show that the temporalis and masseter muscles in C. apella and C. olivaceus are more anteriorly positioned relative to nine other platyrrhine taxa. This condition, which appears to be ancestral among the Cebinae, increases force production at the incisors and canines while compromising third molar function. Cebus apella, has exaggerated this pattern. Field data on dietary toughness show that both capuchins typically select foods of low toughness, but on occasion, C. apella ingests food items of exceptional toughness. Thus, C. apella appears to maintain these biomechanical relationships by producing particularly high but relatively infrequent bite forces, particularly at the incisors and canines. However, adaptations for anterior dental use do not tightly constrain the diet of Cebus apella. This approach can be used to clarify the dietary adaptations of fossil taxa.     

Polymorphic microsatellite loci for the mustached tamarin (Saguinus mystax) and their cross‐species amplification in other New World monkeys

We isolated and characterized 10 polymorphic microsatellite loci for the mustached and cotton‐top tamarin (Saguinus mystax and S. oedipus) and also tested their applicability in other New World monkey genera. Six loci proved to be variable in Cebus apella and Saimiri sciureus/S. boliviensis, respectively. We also show that faeces‐derived DNA is suitable for polymerase chain reaction (PCR) analyses of a primate taxon that gives birth to twins with individuals exhibiting a haematopoetic chimaerism. The microsatellite fingerprint patterns do not display a complex mixture of the PCR‐products derived from the alleles of both dizygotic twins, but exhibit the constitutive alleles of one sibling only.     

Foods and feeding behavior of wild black-capped capuchin (Cebus apella)

Having various kinds of food in its food repertoire, the capuchin (Cebus apella) fed mainly on fruit and insects. Feeding behavior varied according to the kind of food and such behaviors were effective ones performed by the capuchin, which seems to know well both the nature of the plants and habits of the animals it eats. It can also be said that they are highly intellectual ones. In addition, because of the strong relationship between the capuchin's feeding behavior and its habitat, it can be concluded that its behavioral activities were adaptive ones formed by its own positive action.     

Fallback foraging as a way of life: Using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly “specialized” taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods. Am J Phys Anthropol 140:687–699, 2009. © 2009 Wiley-Liss, Inc.     

Intraspecific and interspecific competition induces density‐dependent habitat niche shifts in an endangered steppe bird

Interspecific competition is a dominant force in animal communities that induces niche shifts in ecological and evolutionary time. If competition occurs, niche expansion can be expected when the competitor disappears because resources previously inaccessible due to competitive constraints can then be exploited (i.e., ecological release). Here, we aimed to determine the potential effects of interspecific competition between the little bustard (Tetrax tetrax) and the great bustard (Otis tarda) using a multidimensional niche approach with habitat distribution data. We explored whether the degree of niche overlap between the species was a density‐dependent function of interspecific competition. We then looked for evidences of ecological release by comparing measures of niche breadth and position of the little bustard between allopatric and sympatric situations. Furthermore, we evaluated whether niche shifts could depend not only on the presence of great bustard but also on the density of little and great bustards. The habitat niches of these bustard species partially overlapped when co‐occurring, but we found no relationship between degree of overlap and great bustard density. In the presence of the competitor, little bustard's niche was displaced toward increased use of the species' primary habitat. Little bustard's niche breadth decreased proportionally with great bustard density in sympatric sites, in consistence with theory. Overall, our results suggest that density‐dependent variation in little bustard's niche is the outcome of interspecific competition with the great bustard. The use of computational tools like kernel density estimators to obtain multidimensional niches should bring novel insights on how species' ecological niches behave under the effects of interspecific competition in ecological communities.     

Observations onCebus capucinus in Southwestern Panama

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.     

Social behavior of the wild black-capped Capuchin (Cebus apella)

The author undertook a field survey of the capuchin (Cebus apella) lasting 60 days from December 1976 to January 1977, and determined the basic daily activity of its groups and spacing of group members in the day time. Furthermore, based on studies of various types of interactions between individuals of the groups, he was able to show that (1) decisive rank orders exist both among adults and among sub-adults of both sexes; (2) grooming at the resting time is peculiar to adult males; (3) with quite mild agonistic interactions being maintained, a high tolerance exists between the group members; (4) alpha males represent individuals which can be called leaders of groups; and (5) a strong psychological or spiritual bond exists among the adult males, which can be termed a “male-bond.” Furthermore, according to comparative studies on some adjoining groups, it was found that the group structure is strongly influenced by the individuality or character of the adult males of each group. The present findings are generally in agreement with those forC. apella studied by the author and other researchers in other localities. It can be safely said therefore that these findings are probably common to this species of monkey. Based on a comparison with findings for three other species ofCebus, the author attempts to clarify the points of difference betweenC. apella and these three other species ofCebus from the viewpoint of behavioral science and sociology.     

Observations on two types of neotropical primate intertaxa associations

During a socioecological field study of Colombian spider monkeys, data were collected on spatial associations and social and ecological interactions among free-ranging Ateles belzebuth, Alouatta seniculus, Cebus apella, and Saimiri sciureus. The most frequently observed associations occurred between groups of squirrel and capuchin monkeys. Saimiri-Cebus associations were seen at all times of day and year, but no intertaxa play, passive body contact, or grooming interactions were observed. The Saimiri-Cebus association was paralleled by one between Saimiri and the small hawk, Harpagus bidentatus, and sometimes other insectivorous birds. These associations may be based in part on a complex balance of both mutual and one-sided foraging advantages. Less frequent associations between Ateles and Alouatta were based on mutual attraction to specific fruiting trees or contacts occurring on travel routes. Unlike the more frequently observed associations between Saimiri and Cebus, those between Ateles and Alouatta included both positive and negative interactions; for example, mutual play, grooming, and olfactory investigation as well as threats, chases, and supplantations.     

Divergent habitat use of two urban lizard species

Faunal responses to anthropogenic habitat modification represent an important aspect of global change. In Puerto Rico, two species of arboreal lizard, Anolis cristatellus and A. stratulus, are commonly encountered in urban areas, yet seem to use the urban habitat in different ways. In this study, we quantified differences in habitat use between these two species in an urban setting. For each species, we measured habitat use and preference, and the niche space of each taxon, with respect to manmade features of the urban environment. To measure niche space of these species in an urban environment, we collected data from a total of six urban sites across four different municipalities on the island of Puerto Rico. We quantified relative abundance of both species, their habitat use, and the available habitat in the environment to measure both microhabitat preference in an urban setting, as well as niche partitioning between the two different lizards. Overall, we found that the two species utilize different portions of the urban habitat. Anolis stratulus tends to use more “natural” portions of the urban environment (i.e., trees and other cultivated vegetation), whereas A. cristatellus more frequently uses anthropogenic structures. We also found that aspects of habitat discrimination in urban areas mirror a pattern measured in prior studies for forested sites in which A. stratulus was found to perch higher than A. cristatellus and preferred lower temperatures and greater canopy cover. In our study, we found that the multivariate niche space occupied by A. stratulus did not differ from the available niche space in natural portions of the urban environment and in turn represented a subset of the niche space occupied by A. cristatellus. The unique niche space occupied by A. cristatellus corresponds to manmade aspects of the urban environment generally not utilized by A. stratulus. Our results demonstrate that some species are merely tolerant of urbanization while others utilize urban habitats in novel ways. This finding has implications for long‐term persistence in urban habitats and suggests that loss of natural habitat elements may lead to nonrandom species extirpations as urbanization intensifies.     

Protein electrophoretic variability in Saimiri and the question of its species status

An electrophoretic survey of 15 protein systems (22 loci) was employed to determine the genetic relationships among 9 populations (441 individuals) of South American squirrel monkeys (Saimiri sciureus sciureus, S. sciureus boliviensis, and S. sciureus ustus). Genetic markers capable of differentiating the second from the two other taxa were observed mainly in the ADA and GPI systems. Heterogeneity for ADA and CA2 between populations from opposite banks of the Jamari river was verified in S. sciureus ustus. The average heterozygosities ranged from 3% to 5%, the lowest being in S. sciureus sciureus and the highest in S. sciureus boliviensis. Low genetic distances (D = 0.001?0.057) were observed between populations within taxa or between S. sciureus sciureus and S. sciureus ustus. But both differed to a larger extent from S. sciureus boliviensis (D = 0.11 in both comparisons). There is a positive correlation between the genetic and geographic distance matrices. The three taxa are more clearly separated (D = 0.76–0.77) from the outgroup used for comparison (Cebus apella). Our data suggest that there is only one large, polytypic species of squirrel monkeys in South America, S. sciureus, forming a contiguous ring of geographical races or subspecies. Two of the most differentiated forms meet at the Peruvian Amazonia where natural hybrids and secondary intergradation have been reported. © 1993 Wiley-Liss, Inc.     

Schistosoma haematobium: experimental infection in capuchin monkey, Cebus apella

South American capuchin monkeys (Cebus apella) have been included in a series of nonhuman primates under evaluation for their potential use as models in a study of the basic biology of Schistosoma haematobium. Emphasis has been given to involvement of the urogenital system, a prominent feature of infection in man. Preliminary observations on Cebus apella with moderate numbers of S. haematobium from Iran showed that there may be serious involvement of the urogenital system with development of pronounced hydronephrosis accompanied by pathobiological alteration of the urinary bladder, ureters, and kidneys. There were heavy deposits of parasite eggs in the major viscera.     

Primate diversity,habitat preferences,and population density estimates in Noel Kempff Mercado National Park,Santa Cruz Department,Bolivia

This report documents primate communities at two sites within Noel Kempff Mercado National Park in northeastern Santa Cruz Department, Bolivia. Diurnal line transects and incidental observations were employed to survey two field sites, Lago Caiman and Las Gamas, providing information on primate diversity, habitat preferences, relative abundance, and population density. Primate diversity at both sites was not particularly high, with six observed species: Callithrix argentata melanura, Aotus azarae, Cebus apella, Alouatta caraya, A. Seniculus, and Ateles paniscus chamek. Cebus showed no significant habitat preferences at Lago Caiman and was also more generalist in use of forest strata, whereas Ateles clearly preferred the upper levels of structurally tall forest. Callithrix argentata melanura was rarely encountered during surveys at Lago Caiman, where it preferred low vine forest. Both species of Alouatta showed restricted habitat use and were sympatric in Igapo forest in the Lago Caiman area. The most abundant primate at both field sites was Ateles, with density estimates reaching 32.1 individuals/km² in the lowland forest at Lago Caiman, compared to 14.1 individuals/km² for Cebus. Both Ateles and Cebus were absent from smaller patches of gallery forest at Las Gamas. These densities are compared with estimates from other Neotropical sites. The diversity of habitats and their different floristic composition may account for the numerical dominance of Ateles within the primate communities at both sites. Am. J. Primatol. 46:197–211, 1998. © 1998 Wiley-Liss, Inc.     

The skin of primates. XXXIX. The skin of the white-browed capuchin (Cebus albifrons)

The skin of the white-browed capuchin (Cebus albifrons), although basically similar to that of the squirrel monkey (Saimiri sciureus), contains several outstanding peculiarities: (1) both the epidermis and dermis of the general body surface are devoid of melanotic melanocytes; (2) the skin of the prehensile tail has no modified, glabrous friction surface; (3) the prehensile surface of the tail has no specialized nerve end-organs; (4) cholinesterase-positive, papillary nerve end-organs rest beneath the epidermal ridges of volar skin; and (5) both the clear cells and dark cells of the eccrine glands contain glycogen but neither shows phosphorylase activity.