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1.  In-Group Conformity Sustains Different Foraging Traditions in Capuchin Monkeys (Cebus apella) 
PLoS ONE  2009;4(11):e7858.
Decades of research have revealed rich cultural repertoires encompassing multiple traditions in wild great apes, a picture crucially complemented by experimental simulations with captive apes. Studies with wild capuchin monkeys, the most encephalized simian species, have indicated a New World convergence on these cultural phenomena, involving multiple traditions and tool use. However, experimental studies to date are in conflict with such findings in concluding that capuchins, like other monkeys, show minimal capacities for social learning.
Methodology/Principal Findings
Here we report a new experimental approach in which the alpha male of each of two groups of capuchins was trained to open an artificial foraging device in a quite different way, using either a slide or lift action, then reunited with his group. In each group a majority of monkeys, 8 of 11 and 13 of 14, subsequently mastered the task. Seventeen of the successful 21 monkeys discovered the alternative action to that seeded in the group, performing it a median of 4 times. Nevertheless, all 21 primarily adopted the technique seeded by their group's alpha male. Median proportions of slide versus lift were 0.96 for the group seeded with slide versus 0. 01 for the group seeded with lift.
These results suggest a striking effect of social conformity in learned behavioral techniques, consistent with field reports of capuchin traditions and convergent on the only other species in which such cultural phenomena have been reported, chimpanzees and humans.
PMCID: PMC2773420  PMID: 19924242
2.  Social traditions and social learning in capuchin monkeys (Cebus) 
Capuchin monkeys (genus Cebus) have evolutionarily converged with humans and chimpanzees in a number of ways, including large brain size, omnivory and extractive foraging, extensive cooperation and coalitionary behaviour and a reliance on social learning. Recent research has documented a richer repertoire of group-specific social conventions in the coalition-prone Cebus capucinus than in any other non-human primate species; these social rituals appear designed to test the strength of social bonds. Such diverse social conventions have not yet been noted in Cebus apella, despite extensive observation at multiple sites. The more robust and widely distributed C. apella is notable for the diversity of its tool-use repertoire, particularly in marginal habitats. Although C. capucinus does not often use tools, white-faced capuchins do specialize in foods requiring multi-step processing, and there are often multiple techniques used by different individuals within the same social group. Immatures preferentially observe foragers who are eating rare foods and hard-to-process foods. Young foragers, especially females, tend to adopt the same foraging techniques as their close associates.
PMCID: PMC3049088  PMID: 21357221
capuchins; social traditions; social conventions; Cebus; social learning
3.  Stone Throwing as a Sexual Display in Wild Female Bearded Capuchin Monkeys, Sapajus libidinosus 
PLoS ONE  2013;8(11):e79535.
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.
PMCID: PMC3836890  PMID: 24278147
4.  Comparative Anatomy of the Hind Limb Vessels of the Bearded Capuchins (Sapajus libidinosus) with Apes, Baboons, and Cebus capucinus: With Comments on the Vessels' Role in Bipedalism 
BioMed Research International  2013;2013:737358.
Capuchin monkeys are known to exhibit sporadic bipedalism while performing specific tasks, such as cracking nuts. The bipedal posture and locomotion cause an increase in the metabolic cost and therefore increased blood supply to lower limbs is necessary. Here, we present a detailed anatomical description of the capuchin arteries and veins of the pelvic limb of Sapajus libidinosus in comparison with other primates. The arterial pattern of the bearded capuchin hind limb is more similar to other quadrupedal Cebus species. Similarities were also found to the pattern observed in the quadruped Papio, which is probably due to a comparable pelvis and the presence of the tail. Sapajus' traits show fewer similarities when compared to great apes and modern humans. Moreover, the bearded capuchin showed unique patterns for the femoral and the short saphenous veins. Although this species switches easily from quadrupedal to bipedal postures, our results indicate that the bearded capuchin has no specific or differential features that support extended bipedal posture and locomotion. Thus, the explanation for the behavioral differences found among capuchin genera probably includes other aspects of their physiology.
PMCID: PMC3874347  PMID: 24396829
5.  Hormonal correlates of male life history stages in wild white-faced capuchin monkeys (Cebus capucinus) 
Much attention has been paid to hormonal variation in relation to male dominance status and reproductive seasonality, but we know relatively little about how hormones vary across life history stages. Here we examine fecal testosterone (fT), dihydrotestosterone (fDHT), and glucocorticoid (fGC) profiles across male life history stages in wild white-faced capuchins (Cebus capucinus). Study subjects included 37 males residing in three habituated social groups in the Área de Conservacíon Guanacaste, Costa Rica. Male life history stages included infant (0 to <12 months; N = 3), early juvenile (1 to <3 years; N = 10), late juvenile (3 to <6 years; N = 9), subadult (6 to <10 years; N = 8), subordinate adult (≥10 years; N = 3), and alpha adult (≥ 10 years; N = 4, including one recently deposed alpha). Life history stage was a significant predictor of fT; levels were low throughout the infant and juvenile phases, doubled in subadult and subordinate adults, and were highest for alpha males. Life history stage was not a significant predictor of fDHT, fDHT:fT, or fGC levels. Puberty in white-faced capuchins appears to begin in earnest during the subadult male phase, indicated by the first significant rise in fT. Given their high fT levels and exaggerated secondary sexual characteristics, we argue that alpha adult males represent a distinctive life history stage not experienced by all male capuchins. This study is the first to physiologically validate observable male life history stages using patterns of hormone excretion in wild Neotropical primates, with evidence for a strong association between fT levels and life history stage.
PMCID: PMC3894788  PMID: 24184868
Testosterone; Dihydrotestosterone (DHT); Glucocorticoids; Male development; Puberty; Dominance
6.  Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes) 
Biology Letters  2009;5(3):293-296.
Adopting the approach taken with New Caledonian crows (Corvus moneduloides), we present evidence of design complexity in one of the termite-fishing tools of chimpanzees (Pan troglodytes) in the Goualougo Triangle, Republic of Congo. Prior to termite fishing, chimpanzees applied a set of deliberate, distinguishable actions to modify herb stems to fashion a brush-tipped probe, which is different from the form of fishing tools used by chimpanzees in East and West Africa. This means that ‘brush-tipped fishing probes’, unlike ‘brush sticks’, are not a by-product of use but a deliberate design feature absent in other chimpanzee populations. The specialized modifications to prepare the tool for termite fishing, measures taken to repair non-functional brushes and appropriate orientation of the modified end suggest that these wild chimpanzees are attentive to tool modifications. We also conducted experimental trials that showed that a brush-tipped probe is more effective in gathering insects than an unmodified fishing probe. Based on these findings, we suggest that chimpanzees in the Congo Basin have developed an improved fishing probe design.
PMCID: PMC2679919  PMID: 19324641
tool use; tool modification; cognitive template
7.  What limits tool use in nonhuman primates? Insights from tufted capuchin monkeys (Sapajus spp.) and chimpanzees (Pan troglodytes) aligning three-dimensional objects to a surface 
Animal cognition  2013;17(1):10.1007/s10071-013-0643-x.
Perceptuomotor functions that support using hand tools can be examined in other manipulation tasks, such as alignment of objects to surfaces. We examined tufted capuchin monkeys’ and chimpanzees’ performance at aligning objects to surfaces while managing one or two spatial relations to do so. We presented 6 subjects of each species with a single stick to place into a groove, two sticks of equal length to place into two grooves, or two sticks joined as a T to place into a T-shaped groove. Tufted capuchins and chimpanzees performed equivalently on these tasks, aligning the straight stick to within 22.5° of parallel to the groove in approximately half of their attempts to place it, and taking more attempts to place the T stick than two straight sticks. The findings provide strong evidence that tufted capuchins and chimpanzees do not reliably align even one prominent axial feature of an object to a surface, and that managing two concurrent allocentric spatial relations in an alignment problem is significantly more challenging to them than managing two sequential relations. In contrast, humans from two years of age display very different perceptuomotor abilities in a similar task: they align sticks to a groove reliably on each attempt, and they readily manage two allocentric spatial relations concurrently. Limitations in aligning objects and in managing two or more relations at a time significantly constrain how nonhuman primates can use hand tools.
PMCID: PMC3855185  PMID: 23820935
tool use; spatial reasoning; Sapajus; Pan troglodytes; alignment; posting task
8.  Anatomical Analysis of Thumb Opponency Movement in the Capuchin Monkey (Sapajus sp) 
PLoS ONE  2014;9(2):e87288.
Capuchin monkeys present a wide variety of manipulatory skills and make routine use of tools both in captivity and in the wild. Efficient handling of objects in this genus has led several investigators to assume near-human thumb movements despite the lack of anatomical studies. Here we perform an anatomical analysis of muscles and bones in the capuchin hand. Trapezo-metacarpal joint surfaces observed in capuchins indicate that medial rotation of metacarpal I is either absent or very limited. Overall, bone structural arrangement and thumb position relative to the other digits and the hand’s palm suggest that capuchins are unable to perform any kind of thumb opponency, but rather a ‘lateral pinch’ movement. Although the capuchin hand apparatus bears other features necessary for complex tool use, the lack thumb opposition movements suggests that a developed cognitive and motor nervous system may be even more important for high manipulatory skills than traditionally held.
PMCID: PMC3911977  PMID: 24498307
9.  Age-Related Differences in Corpus Callosum Area of Capuchin Monkeys 
Neuroscience  2011;202:202-208.
Capuchin monkeys (Cebus apella) are New World primates with relatively large brains for their body size. The developmental trajectories of several brain regions – including cortical white matter, frontal lobe white matter, and basal ganglia nuclei – are similar to humans. Additionally, capuchins have independently evolved several behavioral and anatomical characteristics in common with humans and chimpanzees – including complex manipulative abilities, use of tools, and the use of precision grips – making them interesting species for studies of comparative brain morphology and organization. Here we report the first investigation into the development of the corpus callosum and its regional subdivisions in capuchins. Corpus callosum development was quantified using high-resolution structural MRI images from 39 socially reared subjects (male n = 22; female n = 18) ranging in age from 4 days (infancy) – 20 years (middle adulthood). The total area of the corpus callosum and the subdivisions of the genu, rostral midbody, medial midbody, caudal midbody, and splenium were traced from the midsagittal section. Total corpus callosum area displayed significant differences across this time span and was best explained by quadratic growth. Sustained linear growth was observed in the subdivisions of the genu, rostral midbody, and splenium; sustained quadratic growth was seen in the subdivision of the medial midbody. Differences in growth were not detected in the subdivision of the caudal midbody. Females had a larger raw area of the total CC and of the medial midbody and caudal midbody throughout the lifespan. Our results indicate that capuchins show continued white matter development beyond adolescence in regions related to cognitive and motor development.
PMCID: PMC3293371  PMID: 22173013
brain development; Cebus; corpus callosum
10.  How tufted capuchin monkeys (Cebus apella spp) and common chimpanzees (Pan troglodytes) align objects to surfaces: Insights into spatial reasoning and implications for tool use 
American journal of primatology  2011;73(10):1012-1030.
This report addresses phylogenetic variation in a spatial skill that underlies tool use: aligning objects to a feature of a surface. Fragaszy and Cummins-Sebree’s [2005] model of relational spatial reasoning and Skill Development and Perception-Action theories guided the design of the study. We examined how capuchins and chimpanzees place stick objects of varying shapes into matching grooves on a flat surface. Although most individuals aligned the long axis of the object with the matching groove more often than expected by chance, all typically did so with poor precision. Some individuals managed to align a second feature, and only one (a capuchin monkey) achieved above-chance success at aligning three features with matching grooves. Our findings suggest that capuchins and chimpanzees do not reliably align objects along even one axis, and that neither species can reliably or easily master object placement tasks that require managing two or more spatial relations concurrently. Moreover, they did not systematically vary their behavior in a manner that would aid discovery of the affordances of the stick-surface combination beyond sliding the stick along the surface (which may have provided haptic information about the location of the groove). These limitations have profound consequences for the forms of tool use we can expect these individuals to master.
PMCID: PMC3166442  PMID: 21608008
Allocentric; Egocentric; spatial reasoning; object manipulation; alignment; tool use
11.  Wood Litter Consumption by three Species of Nasutitermes Termites in an Area of the Atlantic Coastal Forest in Northeastern Brazil 
Termites constitute a considerable fraction of the animal biomass in tropical forest, but little quantitative data are available that indicates their importance in the processes of wood decomposition. This study evaluated the participation of Nasutitermes corniger (Motschulsky) (Isoptera: Termitidae), N. ephratae (Holmgren), and N. macrocephalus (Silvestri) in the consumption of the wood litter in a remnant area of Atlantic Coastal Forest in northeastern Brazil. The populations of this species were quantified in nests and in decomposing tree trunks, while the rate of wood consumption was determined in the laboratory using wood test-blocks of Clitoria fairchildiana Howard (Fabales: Fabaceae), Cecropia sp. (Urticales: Cecropiaceae), and Protium heptaphyllum (Aublet) Marchand (Sapindales: Burseraceae). The abundance of the three species of termites varied from 40.8 to 462.2 individuals/m2. The average dry wood consumption for the three species was 9.4 mg/g of termites (fresh weight)/day, with N. macrocephalus demonstrating the greatest consumption (12.1 mg/g of termite (fresh weight)/day). Wood consumption by the three species of Nasutitermes was estimated to be 66.9 kg of dry wood /ha/year, corresponding to approximately 2.9% of the annual production of wood-litter in the study area. This consumption, together with that of the other 18 exclusively wood-feeders termite species known to occur in the area, indicates the important participation of termites in removing wood-litter within the Atlantic Coastal Forest domain.
PMCID: PMC3383420  PMID: 20673190
abundance; biomass; consumption rates; decomposition; Isoptera; Neotropical region
12.  Genetic Diversity and Population History of a Critically Endangered Primate, the Northern Muriqui (Brachyteles hypoxanthus) 
PLoS ONE  2011;6(6):e20722.
Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (ΦST = 0.49, ΦCT = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes.
PMCID: PMC3108597  PMID: 21694757
13.  Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp resources from conspecifics 
The use of ‘tactical deception’ is argued to have been important in the cognitive evolution of the order Primates, but systematic studies of active deception in wild non-human primates are scant. This study tests whether wild tufted capuchin monkeys (Cebus apella nigritus) use alarm calls in a functionally deceptive manner to usurp food resources. If capuchins use alarm calls ‘deceptively’, it was predicted that false alarms should be: (i) given by subordinates more than by dominants, (ii) more frequent when food is most contestable, (iii) more frequent when less food is available, and (iv) given when the caller is in a spatial position in which it could increase its feeding success if conspecifics react to the call. These predictions were tested by observing subjects in experimental contexts, in which the amount and distribution of a high-value resource (banana pieces) were manipulated using wooden platforms suspended from tree branches. While false alarms were non-significantly more common when more food was available, the three remaining predictions were supported. These results generally support the hypothesis that alarm calls are used by capuchins to reduce the effects of feeding competition. Whether this is intentional on the part of the caller requires further investigation.
PMCID: PMC2817219  PMID: 19493903
alarm calls; feeding competition; deception; communication; primates; Cebus apella nigritus
14.  Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella) 
It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among ‘generations’ of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.
PMCID: PMC2596191  PMID: 17971322
social learning; tradition; culture; primates; diffusion chains; Cebus apella
15.  Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape 
Journal of human evolution  2009;57(6):710-720.
Cebus apella is renowned for its dietary flexibility and capacity to exploit hard and tough objects. Cebus apella differs from other capuchins in displaying a suite of craniodental features that have been functionally and adaptively linked to their feeding behavior, particularly the generation and dissipation of relatively large jaw forces. We compared fiber architecture of the masseter and temporalis muscles between the tufted capuchin (C. apella; n = 12 ) and two “untufted” capuchins (C. capuchinus, n = 3; C. albifrons, n = 5). These three species share broadly similar diets, but tufted capuchins occasionally exploit mechanically challenging tissues. We tested the hypothesis that C. apella exhibits architectural properties of their jaw muscles that facilitate relatively large forces, including relatively greater physiologic cross-sectional areas (PCSA), more pinnate fibers, and lower ratios of mass to tetanic tension (Mass/P0). Results show some evidence supporting these predictions, as C. apella has relatively greater superficial masseter, whole masseter, and temporalis PCSAs, significantly so only for the temporalis following Bonferroni adjustment. Capuchins did not differ in pinnation angle or Mass/P0. As an architectural trade-off between maximizing muscle force and muscle excursion/contraction velocity, we also tested the hypothesis that C. apella exhibits relatively shorter muscle fibers. Contrary to our prediction, there are no significant differences in relative fiber lengths between tufted and untufted capuchins. Therefore, we attribute the relatively greater PCSAs in C. apella primarily to their larger muscle masses. These findings suggest that relatively large jaw-muscle PCSAs can be added to the suite of masticatory features that have been functionally linked to the exploitation of a more resistant diet by C. apella. By enlarging jaw-muscle mass to increase PCSA, rather than reducing fiber lengths and increasing pinnation, tufted capuchins appear to have increased jaw-muscle and bite forces without markedly compromising muscle excursion and contraction velocity. One performance advantage of this morphology is that it promotes relatively large bite forces at wide jaw gapes, which may be useful for processing large food items along the posterior dentition. We further hypothesize that this morphological pattern may have the ecological benefit of facilitating the dietary diversity seen in Cebus apella. Lastly, the observed feeding on large objects, coupled with a jaw-muscle architecture that facilitates this behavior, raises concerns about utilizing C. apella as an extant behavioral model for hominins that might have specialized on small objects in their diets.
PMCID: PMC3082281  PMID: 19875148
Tufted capuchins; Feeding behavior; Masseter; Temporalis; Fiber length; PCSA; Early hominin diet
16.  Methodological Considerations in the Analysis of Fecal Glucocorticoid Metabolites in Tufted Capuchins (Cebus apella) 
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.
PMCID: PMC3789889  PMID: 24098064
ACTH challenge; Captive welfare; Cortisol; Sapajus; Storage effects; Stress
17.  Conformism in the food processing techniques of white-faced capuchin monkeys (Cebus capucinus) 
Animal Cognition  2009;12(5):705-716.
Researchers of “culture” have long been interested in the role of social learning in establishing patterns of behavioral variation in wild animals, but very few studies examine this issue using a developmental approach. This 7-year study examines the acquisition of techniques used to process Luehea candida fruits in a wild population of white-faced capuchin monkeys, Cebus capucinus, residing in and near Lomas Barbudal Biological Reserve, Costa Rica. The two techniques for extracting seeds (pounding or scrubbing) were approximately equal in efficiency, and subjects experimented with both techniques before settling on one technique—typically the one they most frequently observed. In a sample of 106 subjects that had already settled on a preferred technique, the females adopted the maternal technique significantly more often than expected by chance, but the males did not. Using a longitudinal approach, I examined the acquisition of Luehea processing techniques during the first 5 years of life. Regression analysis revealed that the technique most frequently observed (measured as proportion of Luehea processing bouts observed that used pounding as opposed to scrubbing) significantly predicted the technique adopted by female observers, particularly in the second year of life; the amount of impact of the observed technique on the practiced technique was somewhat less significant for male observers. These results held true for (a) observations of maternal technique only, (b) observations of technique used by all individuals other than the mother, and (c) observations of maternal and non-maternal techniques combined.
Electronic supplementary material
The online version of this article (doi:10.1007/s10071-009-0230-3) contains supplementary material, which is available to authorized users.
PMCID: PMC2728904  PMID: 19455357
Social influence; Cebus capucinus; Food processing; Capuchins; Development
18.  Social Insects Dominate Eastern US Temperate Hardwood Forest Macroinvertebrate Communities in Warmer Regions 
PLoS ONE  2013;8(10):e75843.
Earthworms, termites, and ants are common macroinvertebrates in terrestrial environments, although for most ecosystems data on their abundance and biomass is sparse. Quantifying their areal abundance is a critical first step in understanding their functional importance. We intensively sampled dead wood, litter, and soil in eastern US temperate hardwood forests at four sites, which span much of the latitudinal range of this ecosystem, to estimate the abundance and biomass m−2 of individuals in macroinvertebrate communities. Macroinvertebrates, other than ants and termites, differed only slightly among sites in total abundance and biomass and they were similar in ordinal composition. Termites and ants were the most abundant macroinvertebrates in dead wood, and ants were the most abundant in litter and soil. Ant abundance and biomass m−2 in the southernmost site (Florida) were among the highest values recorded for ants in any ecosystem. Ant and termite biomass and abundance varied greatly across the range, from <1% of the total macroinvertebrate abundance (in the northern sites) to >95% in the southern sites. Our data reveal a pronounced shift to eusocial insect dominance with decreasing latitude in a temperate ecosystem. The extraordinarily high social insect relative abundance outside of the tropics lends support to existing data suggesting that ants, along with termites, are globally the most abundant soil macroinvertebrates, and surpass the majority of other terrestrial animal (vertebrate and invertebrate) groups in biomass m−2. Our results provide a foundation for improving our understanding of the functional role of social insects in regulating ecosystem processes in temperate forest.
PMCID: PMC3792987  PMID: 24116079
19.  A Comparative Assessment of Hand Preference in Captive Red Howler Monkeys, Alouatta seniculus and Yellow-Breasted Capuchin Monkeys, Sapajus xanthosternos 
PLoS ONE  2014;9(10):e107838.
There are two major theories that attempt to explain hand preference in non-human primates–the ‘task complexity’ theory and the ‘postural origins’ theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the ‘niche structure’ hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.
PMCID: PMC4182683  PMID: 25271639
20.  Indigenous utilization of termite mounds and their sustainability in a rice growing village of the central plain of Laos 
The objective of this study was to investigate the indigenous utilization of termite mounds and termites in a rain-fed rice growing village in the central plain of Laos, where rice production is low and varies year-to-year, and to assess the possibility of sustainable termite mound utilization in the future. This research was carried out from 2007 to 2009.
The termites were collected from their mounds and surrounding areas and identified. Twenty villagers were interviewed on their use of termites and their mounds in the village. Sixty-three mounds were measured to determine their dimensions in early March, early July and middle to late November, 2009.
Eleven species of Termitidae were recorded during the survey period. It was found that the villagers use termite mounds as fertilizer for growing rice, vegetable beds and charcoal kilns. The villagers collected termites for food and as feed for breeding fish. Over the survey period, 81% of the mounds surveyed increased in volume; however, the volume was estimated to decrease by 0.114 m3 mound-1 year-1 on average due to several mounds being completely cut out.
It was concluded that current mound utilization by villagers is not sustainable. To ensure sustainable termite utilization in the future, studies should be conducted to enhance factors that promote mound restoration by termites. Furthermore, it will be necessary to improve mound conservation methods used by the villagers after changes in the soil mass of mounds in paddy fields and forests has been measured accurately. The socio-economic factors that affect mound utilization should also be studied.
PMCID: PMC3174111  PMID: 21849087
Fertilizer; Laos; Mound volume; Paddy field; Termite; Termite mound
21.  Isolation and characterization of two new herpes-like viruses from capuchin monkeys. 
Infection and Immunity  1976;14(3):759-766.
Two herpes-like viruses were isolated from capuchin monkey (Cebus apella) brain and (Cebus albifrons) spleen cell cultures, respectively. Both isolates induced similar cytopathic effects consisting of rounded and ballooned cells in the original monkey cell cultures and in a wide range of permissive cell types. Neutralizing antibody to each virus was present in serum from the capuchin monkey from which it was isolated, but the two viruses did not cross-react by neutralization. Fluorescein isothiocyanate conjugates of hyperimmune rabbit serum to one of the isolates showed an antigenic cross relationship between the two isolates. By electron microscopy, herpes-like virus particles were observed in the nucleus and cytoplasm of infected human diploid fibroblast cell cultures. Virus-infected cell cultures stained with acridine orange revealed small deoxyribonucleic acid-containing intranuclear inclusion bodies. Both viruses were inhibited by 5-fluorodeoxyuridine and inactivated by chloroform or exposure to 56 degrees C for 30 min. Antisera prepared against 16 prototype herpesviruses and cytomegaloviruses did not neutralize approximately 100 50% tissue culture infective doses of either capuchin isolate. Neutralizing antibody to the capuchin isolates was detected in sera from 8 of 17 capuchin monkeys but not in sera from 16 humans, 15 chimpanzees, and 10 spider, 6 rhesus, and 5 squirrel monkeys.
PMCID: PMC420951  PMID: 823119
22.  Color Discrimination in the Tufted Capuchin Monkey, Sapajus spp 
PLoS ONE  2013;8(4):e62255.
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.
PMCID: PMC3631197  PMID: 23620819
23.  Capuchin monkeys (Cebus apella) use positive, but not negative auditory cues to infer food location 
Animal cognition  2011;15(1):45-55.
Nonhuman primates appear to capitalize more effectively on visual cues than corresponding auditory versions. For example, studies of inferential reasoning have shown that monkeys and apes readily respond to seeing that food is present (“positive” cuing) or absent (“negative” cuing). Performance is markedly less effective with auditory cues, with many subjects failing to use this input. Extending recent work, we tested eight captive tufted capuchins (Cebus apella) in locating food using positive and negative cues in visual and auditory domains. The monkeys chose between two opaque cups to receive food contained in one of them. Cup contents were either shown or shaken, providing location cues from both cups, positive cues only from the baited cup, or negative cues from the empty cup. As in previous work, subjects readily used both positive and negative visual cues to secure reward. However, auditory outcomes were both similar to and different from those of earlier studies. Specifically, all subjects came to exploit positive auditory cues, but none responded to negative versions. The animals were also clearly different in visual versus auditory performance. Results indicate that a significant proportion of capuchins may be able to use positive auditory cues, with experience and learning likely playing a critical role. These findings raise the possibility that experience may be significant in visually based performance in this task as well, and highlight that coming to grips with evident differences between visual versus auditory processing may be important for understanding primate cognition more generally.
PMCID: PMC3249518  PMID: 21681475
24.  Cyto-, myelo- and chemoarchitecture of the prefrontal cortex of the Cebus monkey 
BMC Neuroscience  2011;12:6.
According to several lines of evidence, the great expansion observed in the primate prefrontal cortex (PfC) was accompanied by the emergence of new cortical areas during phylogenetic development. As a consequence, the structural heterogeneity noted in this region of the primate frontal lobe has been associated with diverse behavioral and cognitive functions described in human and non-human primates. A substantial part of this evidence was obtained using Old World monkeys as experimental model; while the PfC of New World monkeys has been poorly studied.
In this study, the architecture of the PfC in five capuchin monkeys (Cebus apella) was analyzed based on four different architectonic tools, Nissl and myelin staining, histochemistry using the lectin Wisteria floribunda agglutinin and immunohistochemistry using SMI-32 antibody.
Twenty-two architectonic areas in the Cebus PfC were distinguished: areas 8v, 8d, 9d, 12l, 45, 46v, 46d, 46vr and 46dr in the lateral PfC; areas 11l, 11m, 12o, 13l, 13m, 13i, 14r and 14c in the orbitofrontal cortex, with areas 14r and 14c occupying the ventromedial corner; areas 32r, 32c, 25 and 9m in the medial PfC, and area 10 in the frontal pole. This number is significantly higher than the four cytoarchitectonic areas previously recognized in the same species. However, the number and distribution of these areas in Cebus were to a large extent similar to those described in Old World monkeys PfC in more recent studies.
The present parcellation of the Cebus PfC considerably modifies the scheme initially proposed for this species but is in line with previous studies on Old World monkeys. Thus, it was observed that the remarkable anatomical similarity between the brains of genera Macaca and Cebus may extend to architectonic aspects. Since monkeys of both genera evolved independently over a long period of time facing different environmental pressures, the similarities in the architectonic maps of PfC in both genera are issues of interest. However, additional data about the connectivity and function of the Cebus PfC are necessary to evaluate the possibility of potential homologies or parallelisms.
PMCID: PMC3030535  PMID: 21232115
25.  Exploring the Relationship Between Cerebellar Asymmetry and Handedness in Chimpanzees (Pan troglodytes) and Capuchins (Cebus apella) 
Neuropsychologia  2007;45(10):2333-2339.
A comparative study of chimpanzee (Pan troglodytes) and capuchin monkey (Cebus apella) cerebellar asymmetry and its relationship to handedness was conducted. Magnetic resonance images of the brain and behavioral data on a coordinated bimanual task were obtained from 16 chimpanzees and 11 capuchins. Chimpanzees displayed a greater rightward bias of the posterior cerebellum and capuchins displayed a greater leftward bias of the anterior cerebellum. Cerebellar asymmetries were significantly associated with handedness in capuchins but not chimpanzees, and this effect was most pronounced in right-handed capuchins.
PMCID: PMC1951511  PMID: 17382360
Handedness; asymmetry; cerebellum; chimpanzees; capuchins

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