Neophilia, innovation and social learning: a study of intergeneric differences in callitrichid monkeys

In a comparative study of neophilia, innovation and social attentiveness we exposed individuals in seven callitrichid species, from three genera, to novel extractive foraging tasks. The results revealed consistently shorter response latencies, higher levels of successful and unsuccessful manipulation, and greater attentiveness to the task and to conspecifics inLeontopithecus (lion tamarins) than in both Saguinus (tamarins) and Callithrix (marmosets). This is consistent with the hypothesis that species dependent upon manipulative and explorative foraging tend to be less neophobic and more innovative than other species. Furthermore, Callithrix appeared to be less neophobic than Saguinus; ifCallithrix is regarded as the greater specialist, this result is inconsistent with the hypothesis that neophobia is associated with foraging specialization. We consider the relevance of our findings to taxonomic relationships, and to technical and Machiavellian intelligence hypotheses and discuss the implications for captive breeding and reintroduction strategies.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Morphometrics of the callitrichid forelimb: A case study in size and shape

Mosimann and colleagues formulated a technique that distinguishes between size and shape, based on the concept of geometric similarity and the distinction between log size-and-shape and log shape variables. We extend these formulations in an examination of the forelimb of three callitrichid species (adultSaguinus oedipus, Saguinus fuscicollis, andCallithrix jacchus). We employ principal components analysis to explore the relationship between variance explained by size-and-shape versus shape alone. Independence of shape vectors is examined via correlation analysis. Then we use log shape data to construct intersample (species means) and total sample (between all paris of individuals) matrices of average taxonomic distances. These distance matrices are subjected to cluster analysis and principal coordinate ordinations. Results of principal components analysis suggest that after isometric size is removed, there remains sufficient shape information to discriminate among the three taxa. Careful examination and quantification of the relationships between shape and size suggest that size information (e.g., geometric mean) is fundamental for understanding shape differences within and among callitrichid species; in other words, most aspects of forelimb shape are significantly correlated with size. Contrary to conventional wisdom, we also demonstrate that such correlations are not spurious. Ordinations and clustering of log shape distance matrices (based on means and individuals) support the notion that, despite differences in size, the two tamarins are more similar in shape than either is toC. jacchus (despite size similarity betweenS. fuscicollis andC. jacchus). Although shape variation in the forelimb of calliirichids may have a functional component, the phylogenetic signal remains strong and serves to group individuals accordingly.     

The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys

Common (Callithrix jacchus) and pygmy (Cebuella pygmaea) marmosets and cotton‐top tamarins (Saguinus oedipus) share broadly similar diets of fruits, insects, and tree exudates. Marmosets, however, differ from tamarins in actively gouging trees with their anterior dentition to elicit tree exudates flow. Tree gouging in common marmosets involves the generation of relatively wide jaw gapes, but not necessarily relatively large bite forces. We compared fiber architecture of the masseter and temporalis muscles in C. jacchus (N = 18), C. pygmaea (N = 5), and S. oedipus (N = 13). We tested the hypothesis that tree‐gouging marmosets would exhibit relatively longer fibers and other architectural variables that facilitate muscle stretch. As an architectural trade‐off between maximizing muscle excursion/contraction velocity and muscle force, we also tested the hypothesis that marmosets would exhibit relatively less pinnate fibers, smaller physiologic cross‐sectional areas (PCSA), and lower priority indices (I) for force. As predicted, marmosets display relatively longer‐fibered muscles, a higher ratio of fiber length to muscle mass, and a relatively greater potential excursion of the distal tendon attachments, all of which favor muscle stretch. Marmosets further display relatively smaller PCSAs and other features that reflect a reduced capacity for force generation. The longer fibers and attendant higher contraction velocities likely facilitate the production of relatively wide jaw gapes and the capacity to generate more power from their jaw muscles during gouging. The observed functional trade‐off between muscle excursion/contraction velocity and muscle force suggests that primate jaw‐muscle architecture reflects evolutionary changes related to jaw movements as one of a number of functional demands imposed on the masticatory apparatus. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi's monkeys (Callimico goeldii)

Neophobia, defined as showing caution toward novel features of the environment, is widespread in birds and mammals; it can be affected by ecology, early experience, and social context. In this study, we aimed to (i) investigate the response to novel food in adult common marmosets and Goeldi's monkeys and (ii) assess the role of social influences. We used an experimental paradigm employed previously with capuchin monkeys and children, in which a subject (observer) was presented with a novel food under three conditions: (i) Presence: group members did not have food; (ii) Different color: group members received familiar food whose color differed from that of the observer's novel food; (iii) Same color: group members received familiar food of the same color as the observer's novel food. Although most common marmosets tasted and/or ate the novel food, none of the Goeldi's monkeys ate it and only two sampled it. Differences in home range size and early social experience might explain the divergent behavior of the two species. Observers of both species similarly attended to group members and their visual attention increased with the number of group members eating, especially when the observer's and group members' foods were perceptually similar. However, we observed social influences on explorative behavior in Goeldi's monkeys but not on explorative or eating behavior in common marmosets. This result might be explained by the different pattern of response to novel food observed in the two species. Moreover, social influences on Goeldi's monkeys' behavior were nonspecific, i.e. they were not based on an appreciation that the food is safe because eaten by group members.     

Age class differences in the feeding behavior of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups

Age class differences in feeding behavior of primates are affected by many factors, including feeding competition, foraging skills, habitat type, food abundance and distribution, body mass, and food types. Two captive groups of Japanese macaques (Macaca fuscata), one housed in a forested enclosure and the other in a nonvegetated enclosure, were studied to examine the effect of environmental enrichment on age class differences in feeding behavior. Although there was no significant age class difference in time spent feeding on provisioned foods in either enclosure, the feeding rate (intake of unit food/minute) of adults consuming provisioned monkey chow was significantly higher than that of immatures in both enclosures, and was faster for both age groups in the nonvegetated than in the forested enclosure. Overall, feeding time was greatly extended for individuals of both age classes in the forested enclosure compared with their counterparts in the nonvegetated enclosure. Immatures in the forested enclosure utilized a significantly greater number of plant species and food items, exploiting many food items available among the terminal branches, and spent significantly more time feeding than adults. Perhaps constrained by larger body size, adults fed more often on the ground or middle height of the trees, likely reducing competition over plant food resources between adults and immatures. The natural vegetation played an important role in extending feeding time and segregating substrate use during feeding by adults and immatures. This study revealed the benefits concerning environmental enrichment of a naturally forested enclosure, which provides captive primates the opportunity to exhibit age class and species-typical feeding behaviors of importance for their dietary maintenance and general health.     

Sex and age differences in juvenile social priorities in female philopatric,nondespotic blue monkeys

Juveniles should choose social partners on the basis of both current and future utility. Where one sex is philopatric, one expects members of that sex to develop greater and sex‐typical social integration with group‐mates over the juvenile period. Where a partner's position in a dominance hierarchy is not associated with services it can provide, one would not expect juveniles to choose partners based on rank, nor sex differences in rank‐based preferences. We tested these ideas on 39 wild juvenile (3.2–7.4 years) blue monkeys (Cercopithecus mitis stuhlmanni), cercopithecines with strict female philopatry and muted hierarchies. We made focal animal observations over 6 months, and computed observed:expected amounts of proximity time, approaches and grooming given to various social partners. Overall, our results agree with the hypothesis that juvenile blue monkeys target social partners strategically. Spatial proximity, approaches and active grooming showed similar patterns regarding juvenile social preferences. Females were far more sociable than males, groomed more partners, reciprocated grooming more frequently, and preferred—while males avoided—infants as partners. Older juveniles (5–7 years) spent more time than younger juveniles (3–4 years) near others, and older females were especially attracted to infants. Close kin, especially mothers and less consistently adult sisters, were attractive to both male and female juveniles, regardless of age. Both sexes also preferred same‐sex juveniles as social partners while avoiding opposite‐sex peers. Juveniles of both sexes and ages generally neither preferred nor avoided nonmaternal adult females, but all juveniles avoided adult males. Partner's rank had no consistent effect on juveniles' preference, as expected for a species in which dominance plays a weak role. Juveniles' social preferences likely reflect both future and current benefits, including having tolerant adult kin to protect them against predators and conspecifics, same‐sex play partners, and, for females, infants on which to practice mothering skills. Am. J. Primatol. 72:193–205, 2010. © 2009 Wiley‐Liss, Inc.     

Age, sex, and dominance-related mushroom body plasticity in the paperwasp Mischocyttarus mastigophorus

Social Hymenoptera are important models for analyzing functional brain plasticity. These insects provide the opportunity to learn how individuals' social roles are related to flexible investment in different brain regions. We assessed how age, sex, and individual behavior influence brain development in a primitively eusocial paper wasp, Mischocyttarus mastigophorus. Previous research in other species has demonstrated experience-dependent changes in central and primary sensory centers in the brain. The mushroom body (MB) calyx is a central processing region involved in sensory integration, learning and memory and may be particularly relevant to social behavior. We extend earlier cross-sectional studies of female brain/behavior associations by measuring sex- and age-related differences in MB calyx volume, and by quantifying optic lobe and antennal lobe development. Age did predict MB development: calyx neuropils increased in volume with age. We show that MB development differs between the sexes. Males, who frequently depart to seek mating opportunities, have larger MB calyx collars (which receive optic input) than females. In contrast, females have augmented predominantly antenna-innervated MB calyx lips, which may be useful for nestmate recognition and interactions on the nest. Sex differences in MB development increased with age. After accounting for age and sex effects, social aggression was positively correlated with MB calyx volume for both sexes. We found little evidence for relationships among sex, age, or behavior and the volumes of peripheral sensory processing structures. We discuss the implications of gender- and age-related effects on brain volume in relation to male and female life history and reproductive success.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Age and gender differences in body composition, energy expenditure, and glucoregulation of adult rhesus monkeys

The purpose of this study was to examine the relationship of age to body composition, glucoregulation, activity, and energy expenditure in male and female rhesus monkeys. The animals were studied in three groups, young adults (YA, 7-9 years), middle-aged adults (MA, 13-17 years), and older adults (OA, > 23 years) adults. OA had a lower (P < 0.05) lean body mass than the YA and MA. OA also had the lowest values (P < 0.06) for energy expenditure (kJ/minute). Age-related differences (P < 0.05) were observed in time spent resting and moving. The OA spent the most time resting and the least time in vertical movement. There was a trend towards an age-related decrease in acute insulin response to glucose, while other glucoregulatory parameters were not changed with age. These results are similar to findings in humans, providing further evidence that the rhesus monkey is an appropriate model of human aging.     

Litter size and infant survivorship in wild groups of cotton‐top tamarins (Saguinus oedipus) in Colombia

Cotton‐top tamains (Saguinus oedipus) are a critically endangered primate found only in Colombia. Efforts to conserve this species are centered on developing effective management plans that integrate biological information regarding population dynamics and factors that influence their survival. This study documented infants born to wild cotton‐top tamarin females from 1994–2008 at two distinct field sites in northern Colombia. Our studies have shown that wild cotton‐top tamarins typically give birth to one litter each year and infant survival to 6 months of age was greater in the wild than has been reported in captive colonies. However, similar to reports from captive colonies, litter size of wild cotton‐top tamarins ranges from 1–3 infants, with twin litters most common. Here we report the first occurrence of triplet litters in nearly 20 years of observing wild cotton‐top tamarin groups. Over the first 3 months of life, wild‐born infants exhibited highest mortality during the first week of life, similar to reports from captive colonies. Infant survival in the wild also increases with successive litters as it does in captivity. However, inter‐birth interval, group size, and the number of adult males in the group did not appear to influence infant survival in the wild. The value of such long‐term data from field studies aids in the information that can be used to model future population trends and develop effective conservation plans for this critically endangered primate. Am. J. Primatol. 71:707–711, 2009. © 2009 Wiley‐Liss, Inc.     

Primate Innovation: Sex,Age and Social Rank Differences

Analysis of an exhaustive survey of primate behavior collated from the published literature revealed significant variation in rates of innovation among individuals of different sex, age and social rank. We searched approximately 1,000 articles in four primatology journals, together with other relevant databases, for examples of innovation. The reported incidence of innovation is higher in males and adults, and lower in females and nonadults, than would be expected by chance given the estimated relative proportions of these groups. Amongst chimpanzees, the only species for which there are sufficient data to consider alone, there is a similar sex difference in the propensity to innovate, but no effect of age. Chimpanzees of low social rank are reported as innovators more frequently than high-ranking chimpanzees are. Male chimpanzees innovate more often than females in sexual, courtship, mating and display contexts; that is, in contexts likely to increase access to mates. The largest number of recorded observations are in the foraging context, wherein contrary to expectations, there is no evidence for female chimpanzees exhibiting more innovation than males. The study is the first extensive investigation of behavioral innovation in primates and provides evidence that much individual variation in the propensity to innovate can be explained in terms of sex, age, and social rank.     

Infant survival and number of helpers in captive groups of common marmosets (Callithrix jacchus)

In a colony of captive marmoset monkeys (Callithrix jacchus), the survival rate of infants up to the age of 90 days after birth was analyzed with special reference to the number of members in the group. The number of group members (newborns excluded) varied between two (parents only) and 18 (parents plus non-reproductive helpers); the number of adult group members varied between two and 15. Five hundred ninety-two live-born, parent-reared infants of 263 litters from 56 breeding females were included in the analysis. The greatest reproductive success was observed in groups of ten to 11 members or four to five adults, including the parents. However, the survival rate was fairly constant over group size at approximately 80% of an expected maximum value and no significant correlation was observed between the total number of group members and infant survival rate, or between the number of adult members and infant survival. While helpers may be necessary to increase the survival rate of infants in wild groups, help of non-reproductive animals is not required in captivity, where energetic demands are comparatively low and ecological constraints absent. Under laboratory conditions the parents' skill in infant handling and the mother's physical condition, i.e., the ability to provide enough milk for the infants, is likely to be the most important factor for infant survival. © 1993 Wiley-Liss, Inc.     

Age and sex composition of family groups in shopping and recreational settings

The age and sex compositions of 3838 family groups exiting shopping malls and the zoo were recorded and analyzed for patterns in parental accompaniment of children. The findings included higher relative frequencies of both-parent groups at the zoo, greater likelihood of both parents accompanying young children, and greater likelihood of the mother than the father accompanying the single child, especially daughters at the shopping centers. The presence of more than one child increases the likelihood of both parents being present. Father involvement is seen as high in escorting children to public settings.     

Reactions of adult and immature squirrel monkeys to intergroup exposure

Initial encounters between unfamiliar animals raise the practical problem of controlling aggression and provide the opportunity to examine changes in social structure that may occur as groups merge. Social interactions and spatial grouping patterns were examined in newly formed squirrel monkey groups, in which a subgroup of familiar adults was introduced to a subgroup of familiar immature squirrel monkeys. Yearlings (10–11 months) and subadults (20–50 months) generally remained spatially distinct from adults, and intergroup interactions often consisted of adult-initiated antagonism. Adults exhibited sexual segregation in their spatial grouping patterns and interactions, whereas yearlings and subadults generally showed sexual integration. These data suggest that there is considerable adult resistance to integration of unfamiliar immatures into established adult social groups. Zoo Biol 17:519–524, 1998. © 1998 Wiley-Liss, Inc.     

Hormonal monitoring of age at sexual maturation in female Goeldi's monkeys (Callimico goeldii) in their family groups

The aim of this study was to determine whether or not sexual maturation is attained in the family group in captive‐born Goeldi's monkey (Callimico goeldii) and if so, at what age and body weight. To monitor ovarian activity in 14 female Goeldi's monkeys, urinary content of pregnanediol‐3α‐glucuronide (PdG) was determined using radioimmunoassay. Urinary samples were collected between the ages of 6 and 70 weeks. Subjects became sexually mature while still housed in their family groups, at a median age of 57 weeks (48–< 70 weeks). Median body weight at the age of sexual maturity was 473 g (N = 10; 420–543 g). This corresponded to 90% of the median non‐pregnant body weight of breeding females in our colony (526 g, N = 8). Therefore, Goeldi's monkey is similar to Leontopithecus but different from Cebuella, Callithrix, and Saguinus, in terms of daughters ovulating in the family group and at a relatively young age. Am. J. Primatol. 48:77–83, 1999. © 1999 Wiley‐Liss, Inc.     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.     

Effects of experience and object complexity on exploration in garden warblers (Sylvia borin)

Animals are increasingly exposed to novel environmental conditions because of human activities. An organism's ability to cope with these challenges is critical to its survival. The decision of whether or not an animal should investigate environmental changes involves a trade-off between the risk and the potential benefit of a novel resource. Novelty often elicits approach (exploratory) as well as avoidance behaviour in animals, and the extent of each of these behaviours may influence learning about the environment. We formulated and tested several hypotheses to determine how external factors (complexity of a novel stimulus) and internal factors (experience with objects) might influence exploration latencies to touch a novel object based on either cost or benefit considerations. Garden warblers were confronted with a simple and a complex novel object in their familiar cages, and latencies until first touch were measured. Additionally, corticosterone levels before and after the experiment were measured to assess whether differences in baseline levels might explain variations in latency to approach and whether presentation of novel objects is stressful. The complex object was touched significantly later than the simple object. Experienced birds investigated both types of objects later than inexperienced birds. Although birds showed marked approach–avoidance behaviour with the complex object, none of the objects elicited a corticosterone stress response. The results indicate that garden warblers consider both costs and benefits when exploring novel objects, and that the relative influence of costs and benefits varies with external and internal factors.     

Individual vocal differences of the coo call in Japanese monkeys

We investigated individual vocal characteristics of the coo call in Japanese monkeys. The goal of the study was to determine which parameters are individual discriminators (for individuals of different ages and sexes) and to test whether those differences were similar for individuals of same age and sex. A discriminant analysis realized on eight individuals pointed out that three parameters (call duration, start and end frequencies of the fundamental component) differentiated individuals efficiently and was validated by a second discriminant analysis realized on three same-age females.     

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis)

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.