Lateral bias in feeding and brachiation inHylobates

Lateralized hand use in gibbons was assessed for both food reaching and leading limb in brachiation. Sex and age effects were found in hand preference for food reaching. Adult females were all very strongly right hand preferent, whereas adult males had no across group consistent preference. Within the female group there was a strong correlation between age and strength of right handedness. When compared in terms of absolute strength of hand preference, females were found to be more strongly lateralized than males. Leading limb preference in brachiation was scored into vocal and non-vocal categories. Three subjects had a shift in preferred leading limb from the non-vocal brachiation condition to the vocal brachiation condition. This shift may be influenced by the arousal effects of species typical vocalization. The results of this study underline the importance of consideration of such factors as sex and age when interpreting behavioral lateralization data. The exploration of laterality in many different response measures is important to the achievement of a complete understanding of behavioral lateralization in primates.     

The potential effects of sex,posture and living condition on lateralized behaviors in ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>)

This research explores the effects of posture, sex, and living condition on hand and side preferences of semi-free-ranging, adult ring-tailed lemurs (Lemur catta) housed at the Duke University Primate Center in Durham, NC. Data were collected on 11 adult individuals (five females and six males) during normal daily activities over a ten-week period from May–July 2001. Variables analyzed in this study include unimanual behaviors (i.e., reach, hold, and limb used to start locomotion) and other potentially lateralized behaviors that do not involve handuse (i.e., whole-body turning and tail position). The data were analyzed to investigate potential individual and population level side biases for each behavior; potential sex biases in side preference for each behavior; and for ‘reach’, potential effects of posture (sitting, tripedal stance, or bipedal stance) on individual hand preferences. Additionally, to investigate potential effects of living condition on lateral biases, the data from this study were compared to data collected on the same individual Lemurs living under more restrictive living conditions during the previous year. Largely, as predicted based on available literature, we found that there was a significant sex difference across all hand-use categories and for whole-body turning, and that posture was a significant factor in the expression of hand preference for reaching. Contrary to previous research, the effect of living condition on lateral preferences was minimal, and no side preferences were found at the population level for any of the behaviors analyzed.     

Paternal Care in <Emphasis Type="Italic">Propithecus verreauxi coquereli</Emphasis>

Alloparental behavior is documented for several anthropoid primates, but few researchers have investigated the extent or variability of such behavior in prosimians. We report results from a study of male-infant interactions in 2 groups of Coquerel’s sifaka (Propithecus verreauxi coquereli) at the Duke University Primate Center (DUPC). Both groups contained 1 adult pair, 2 juveniles, and a newborn. The adult males exhibited paternal behavior toward their offspring in the form of grooming and holding the infant, though males differed in the amount of time they spent engaged in these activities. Group differences in the proximity maintained between the infants’ parents suggest that the relationship between adult males and females may help account for the variation. The presence of juveniles appeared to diminish paternal behavior in the group exhibiting a higher overall rate of male-infant interaction.     

Effects of housing differences upon activity budgets in captive sifakas (Propithecus verreauxi)

Activity budgets of captive sifakas (Propithecus verreauxi coquereli and Propithecus verreauxi verreauxi) were assessed from 500 hours of observational data obtained at the Duke University Primate Center (Durham, NC). Data were examined for behavioral differences according to gender, availability of intergroup contact, subspecies, indoor/outdoor housing, and enclosure size. Results showed few differences between the activity budgets of males and females. Several differences found in conjunction with availability of intergroup contact appeared to relate more to subspecific, than to contact, differences. Sifakas housed outdoors were more active, spending less time resting and more time in locomotion, feeding, and playing than sifakas housed indoors. The findings of this study implicate outdoor housing as a primary factor in stimulating activity in these rare prosimian primates.     

Mate-Guarding as a Male Reproductive Tactic in <Emphasis Type="Italic">Propithecus verreauxi</Emphasis>

Sexual selection theory predicts that in group-living mammals, male reproductive tactics can lead to high reproductive skew in favor of dominant individuals. In sifakas (Propithecus verreauxi), a group-living primate with extremely seasonal reproduction, male reproductive success is highly skewed because dominant males sire almost all offspring despite a tendency toward an even adult group sex ratio. To understand the underlying behavioral mechanism resulting in this rank-related reproductive skew in male sifakas, we studied mate-guarding as a potential reproductive tactic. Behavioral observations of dominant males and adult females in combination with hormonal determination of timing of female receptivity in 9 groups at Kirindy Forest revealed that dominant males spent more time in proximity to females when they were receptive and were responsible for the maintenance of this proximity. Results also indicated that monopolization of receptive females was facilitated by both estrous asynchrony within groups and by the ability of dominant males to obtain olfactory cues as to the timing of female receptivity. Although dominant males engaging in mate-guarding are expected to experience various costs, there was no evidence for decreased foraging behavior and only a trend toward increased aggression between dominant and subordinate non-natal males within groups. Our results are in accordance with the hypothesis that dominant males use mate-guarding to monopolize receptive females and that it is one proximate mechanism that contributes to the high reproductive skew observed within the population of male sifakas at Kirindy.     

Avian nest predation by a semi-captive collared lemur (Lemur fulvus collaris)

A lemur (Lemur fulvus collaris) in a semi-captive group of six animals at the Duke University Primate Center (DUPC) was observed eating an egg from the nest of a mourning dove (Zenaida macroura). The manner in which the animal had been foraging prior to this incident, and the fact that wild birds at the DUPC frequently direct antipredator behaviors, such as mobbing toward thisL. f. collaris group, suggest that nest predation is part of normal foraging behavior in these animals.     

Patterns of affiliation among immature rhesus monkeys (Macaca mulatta)

The affiliative interaction patterns of the immature members of a group of rhesus monkeys at the Yerkes Regional Primate Research Center reflected a strong bias toward matrilineal kin, although this effect was modified by age and sex variables. Association with kin decreased with age, particularly for males. Juvenile males showed less of a kin bias in their behavior than did juvenile females, especially for grooming. Juvenile males also exhibited a preference for interaction with other males. The diminished association with kin and the same-sex bias may be reinforced in adolescence as adult males begin to aggressively target adolescent males involved in agonistic encounters with females or immatures. Adolescent males did not decrease their levels of social interaction relative to those of adolescent females; however, these males preferentially associated with other males (predominantly their own age-sex class) and specifically avoided females and younger animals, both kin and nonkin. Avoidance may diminish conflicts with females or immatures which could result from association, thereby decreasing the potential for selective aggressive interference by adult males. Juvenile and adolescent females maintained strong ties with their kin and preferentially associated with other females and immatures. The breadth of interaction of females with other females may facilitate the establishment of dominance relationships as females mature. Familiarity and predictability may also decrease the necessity of more severe agonistic interaction.     

Population-Level Right Handedness for a Coordinated Bimanual Task in Chimpanzees: Replication and Extension in a Second Colony of Apes

The purpose of this study was to evaluate the reliability of previously published findings on hand preferences in chimpanzees by evaluating hand use in a second colony of captive chimpanzees. We assessed hand preferences for a coordinated bimanual task in 116 chimpanzees (Pan troglodytes) at the University of Texas M. D. Anderson Cancer Center and compared them to previously published findings in captive chimpanzees at the Yerkes National Primate Research Center. The new sample showed significant population-level right handedness, which is consistent with previously published findings in the Yerkes chimpanzees. Combined data on the 2 chimpanzee colonies, revealed a significant effect of rearing history on hand preference, with wild-caught chimpanzees showing less right-handedness than captive-born mother-reared chimpanzees. We discuss the results in terms of the role of early environment on the development of laterality.     

Social organization of free-ranging ruffed lemurs,Varecia variegata variegata: mother-adult daughter relationship

The relationship between a mother and an adult daughter is examined in a group of free-ranging ruffed lemurs (Varecia variegata) at the Duke University Primate Center (DUPC). Although the two females were affiliative during the birth season, interactions during the mating season were predominantly agonistic. The maturing daughter was dominant to the mother, as has been observed in many caged social groups at the DUPC. Although both mother and daughter produced offspring in the same group, the daughter subsequently aggressively evicted the mother from the enclosure. It was not possible to maintain more than one long-term resident breeding female in the same social group. This pattern contrasts with observations of affiliation among breeding females in the wild. © 1992 Wiley-Liss, Inc.     

Isolation of females prior to parturition reduces neonatal mortality in Galago

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effects of isolation of pregnant females on neonatal mortality rates. Isolation significantly decreased neonatal mortality rates in all three species over neonatal mortality rates in infants born to unisolated females. The frequency of cannibalism of infants did not differ between isolated and unisolated females. Secondary sex ratio differed significantly from 1:1 for all three species, but higher mortality in males in the first 10 days of life resulted in sex ratios that did not differ from 1:1 in G. garnettii and G. crassicaudatus.     

Hand preferences in captive orangutans (Pongo pygmaeus)

The strength of the evidence for population-level handedness in the great apes is a topic of considerable debate, yet there have been few studies of handedness in orangutans. We conducted a study of manual lateralization in a captive group of eight orangutans (Pongo pygmaeus) ranking the degrees of manual preference according to a defined framework. We analyzed five behavioral patterns: eat (one- and two-handed), make/modify tool, oral tool-use, and manual tool-use. Although some individuals showed significant manual preferences for one or more tasks, at the group-level both one-handed and two-handed eating, oral tool-use, and make/modify tool were ranked at level 1 (unlateralized). Manual tool-use was ranked at level 2, with four subjects demonstrating significant hand preferences, but no group-level bias to the right or left. Four subjects also showed hand specialization to the right or left across several tasks. These results are consistent with most previous studies of manual preference in orangutans. The emergence of manual lateralization in orangutans may relate to more complex manipulative tasks. We hypothesize that more challenging manual tasks elicit stronger hand preferences.     

Handedness in wild chimpanzees

The debate over nonhuman primate precursors to human handedness is unsettled mainly due to lack of data, particularly on apes. Handedness in wild chimpanzees at the Taï National Park Côte d'Ivoire, has been monitored in four tasks. For the simple unimanual ones, reaching and grooming, adults use both hands equally (ambidextrous), while for the more complex unimanual wadge-dipping and the complex bimanual nut-cracking, adults are highly lateralized. These results support the hypothesis that lateralization increases with the complexity of the task. The lateralization is constant for years for each task but may vary in an individual with respect to different tasks. For nutcracking females are more lateralized than males. The ontogeny of handedness for nut-cracking shows many variations in the tendency to use one hand and in the side preferred, until at about 10 years of age, the individual achieves her adult handedness. No population bias toward one side exists in Taï chimpanzees. No heritability of handedness between mother and offspring was observed. Human and chimpanzees handedness are compared.     

Patterns of wounding in stumptail macaques (macaca arctoides)

A three-year study of the patterns of wounding in a group of stumptail macaques (Macaca arctoides) was conducted at the Yerkes Regional Primate Research Center Field Station. Wounds were classified as punctures, lacerations or abrasions. Data were analyzed to determine if patterns of wounding vary by age/sex class, body part or wound type. Results indicate that adult males receive significantly more total wounds than expected, based on their total time spent in the group. Adult males also receive more serious wounds than other age/sex classes. Low-ranking animals are wounded more often than high-ranking individuals. Moreover, the location of wounds within each age/sex class is non-random. Adult males receive a disproportionate number of wounds on the forequarters, but adult and immature females are wounded disproportionately on the hindquarters. Finally, age/sex classes differ in the number of wounds on individual body parts. Adult males receive more wounds on the head, arms and hands than other age/sex classes, but adult and immature females receive more wounds on the feet than other age/sex classes. These results demonstrate that wounding patterns are clearly non-random and depend on a variety of factors such as age, sex and dominance rank.     

Preferred hand use in the japanese macaque troop,arashiyama-R,during visually guided reaching for food pellets

A troop of Japanese macaques, which consisted of about 45 monkeys and was raised at the Primate Research Institute, Kyoto University, was observed during the period from April to June 1988, to evaluate the preferred choice of hand when reaching for food pellets. Nineteen monkeys showed a consistent left-hand preference, 5 monkeys showed a consistent right-hand preference, and the remaining 20 monkeys did not reveal a preference for either hand. Monkeys of more than 8 years of age tended to exhibit a greater left-hand preference with a lower incidence of absence of preference. A tendency to use either left or right hand increased with increasing age: the correlation ratio between age in years and the index to use either hand, designated as the laterality index, was significant (t-test,p<0.001,N=42). Children of mothers with a left-hand preference tended to show a left-hand preference.     

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

Corpus callosum morphology in capuchin monkeys is influenced by sex and handedness

Sex differences have been reported in both overall corpus callosum area and its regional subdivisions in humans. Some have suggested this reflects a unique adaptation in humans, as similar sex differences in corpus callosum morphology have not been reported in any other species of primate examined to date. Furthermore, an association between various measurements of corpus callosum morphology and handedness has been found in humans and chimpanzees. In the current study, we report measurements of corpus callosum cross-sectional area from midsagittal MR images collected in vivo from 14 adult capuchin monkeys, 9 of which were also characterized for hand preference on a coordinated bimanual task. Adult females were found to have a significantly larger corpus callosum: brain volume ratio, rostral body, posterior midbody, isthmus, and splenium than adult males. Left-handed individuals had a larger relative overall corpus callosum area than did right-handed individuals. Additionally, a significant sex and handedness interaction was found for anterior midbody, with right-handed males having a significantly smaller area than right-handed females. These results suggest that sex and handedness influences on corpus callosum morphology are not restricted to Homo sapiens.     

Lactation and interbirth interval in the Senegal galago (Galago senegalensis moholi)

Five years of reproductive data on Galago senegalensis moholi at the Duke University Primate Center were examined to determine the effect of lactation on interbirth interval and its component phases, postpartum anovulatory interval and interval from onset of estrous cycles to conception. Females whose infants died within 3 weeks of birth had significantly shorter interbirth intervals and postpartum anovulatory intervals than did females who raised their infants until weaning.     

Duke University Primate Center

The Duke University Primate Center houses the world's largest collection of prosimian primates. The Center is a research resource for undergraduate and graduate students, as well as faculty from Duke University and other U.S. and international universities. Researchers have access to the animals for noninvasive studies, to a large collection of preserved tissues and cadavers, and to an extensive collection of Eocene and Oligocene fossils. The Center is also involved in conservation programs in Madagascar which provide opportunities for field research in primatology and conservation.     

Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes)

The developmental origin of abnormal behaviors is generally associated with early rearing environments that lack sufficient physical and sensory stimulation. However, other factors should also be considered. A large sample of captive chimpanzees (128 males and 140 females) was surveyed for the presence or absence of 18 abnormal behaviors. Origin variables included the subject's source (zoo, pet, performer, or laboratory), rearing (mother‐ or hand‐reared), and sex. Animals were assessed while held at the Primate Foundation of Arizona, University of Texas M. D. Anderson Cancer Center, or White Sands Research Center. There was a confound among origin variables; more hand‐reared animals than expected were from laboratories. Logistic regression tested the relationship of rearing and source, with sex as a secondary predictor variable, to each of the abnormal behaviors. There was no clear association between any abnormal behavior and source. However, for coprophagy, relative to animals from the laboratory, zoo animals tended to show a higher prevalence, while performers tended to show a lower prevalence (when rearing and sex were controlled). Rocking and self‐sucking were significantly more likely in hand‐reared animals. Coprophagy and depilation of self were significantly more likely in mother‐reared animals. When rearing and source were statistically controlled, the only significant sex difference was a higher prevalence of coprophagy in females and a higher prevalence of rocking in males. In a second, smaller sample of 25 males and 33 females from Southwest Foundation for Biomedical Research, no significant sex association was found for coprophagy, urophagy, rocking, or self‐depilation. In this second sample, coprophagy was also significantly more likely in mother‐reared than hand‐reared subjects. The association of some abnormal behaviors with mother‐rearing suggests that some form of social learning may be involved in the origin of some of these behavior patterns. This indicates that some abnormal behaviors may not be always be indicative of reduced psychological well‐being in captive chimpanzees. Am. J. Primatol. 48:15–29, 1999. © 1999 Wiley‐Liss, Inc.