A case study of primiparous maternal and infant gorilla (Gorilla gorilla gorilla) behavior

A primiparous mother and her infant were subjects of a longitudinal behavioral study at Lincoln Park Zoo in Chicago, Illinois. From November 1998 to November 1999, we collected a total of 100 hr of focal nonhuman animal instantaneous point sampling and all occurrence data on the mother and her infant. After 8 months, we introduced the 4-member focal group to an 8-member gorilla group, thus providing an opportunity to study the effect of the introduction on mother-infant behavior. Overall, time the pair spent physically apart was notably high with contact and proximate scores steadily decreasing over time. The infant was largely responsible for maintaining social proximity, rarely leaving the mother and frequently approaching her. In contrast, the mother left the infant frequently and approached the infant minimally. Maternal affiliative and nonaffiliative behaviors fluctuated throughout the study. Over time, both decreased. Despite a precarious maternal relationship, infant developmental trends were typical for captive gorillas. The results of this study suggest that allowing flexibility in judging maternal conduct can be of benefit to successful gorilla husbandry.     

A Case Study of Primiparous Maternal and Infant Gorilla (Gorilla gorilla gorilla) Behavior

A primiparous mother and her infant were subjects of a longitudinal behavioral study at Lincoln Park Zoo in Chicago, Illinois. From November 1998 to November 1999, we collected a total of 100 hr of focal nonhuman animal instantaneous point sampling and all occurrence data on the mother and her infant. After 8 months, we introduced the 4-member focal group to an 8-member gorilla group, thus providing an opportunity to study the effect of the introduction on mother-infant behavior. Overall, time the pair spent physically apart was notably high with contact and proximate scores steadily decreasing over time. The infant was largely responsible for maintaining social proximity, rarely leaving the mother and frequently approaching her. In contrast, the mother left the infant frequently and approached the infant minimally. Maternal affiliative and nonaffiliative behaviors fluctuated throughout the study. Over time, both decreased. Despite a precarious maternal relationship, infant developmental trends were typical for captive gorillas. The results of this study suggest that allowing flexibility in judging maternal conduct can be of benefit to successful gorilla husbandry.     

Neonatal nipple preference and maternal cradling laterality in wild Taihangshan macaques (Macaca mulatta tcheliensis)

Lateralized behavior is considered an observable phenotype of cerebral functional asymmetry and has been documented in many mammalian species. In the present study, we examined evidence of lateralization in neonatal nipple contact, maternal cradling, and the relationship between these two behaviors during the first 12 weeks of life in wild Taihangshan macaques (Macaca mulatta tcheliensis). The results showed that across our sample of nine mother–infant dyads: (1) Seven of nine neonates exhibited a significant left-side nipple preference during the first 12 weeks of life, whereas eight of nine mothers displayed a significant right-side cradling preference; (2) at the population level, there was a significant preference for left nipple contact by neonatal Taihangshan macaques and a significant right-hand maternal cradling preference; (3) at the population level, there was a nonsignificant negative correlation between neonatal nipple preference and maternal cradling bias; and (4) the strength of individual neonatal nipple preference and maternal cradling laterality were not correlated. We conclude that asymmetry in nipple contact of Taihangshan macaques occurs early in behavioral development. Given that infant Taihangshan macaques are able to nurse and cling unassisted to their mothers within a few days after birth, it appears that the infant rather than its mother is responsible for determining a nipple-side preference. Our results indicating a left-side nipple bias in 78% of wild neonatal Taihangshan macaques are most consistent with the heartbeat hypothesis.     

Brief communication: Captive gorillas are right‐handed for bimanual feeding

Predominance of right‐handedness has historically been considered as a hallmark of human evolution. Whether nonhuman primates exhibit population‐level manual bias remains a controversial topic. Here, we investigated the hypothesis that bimanual coordinated activities may be a key‐behavior in our ancestors for the emergence and evolution of human population‐level right‐handedness. To this end, we collected data on hand preferences in 35 captive gorillas (Gorilla gorilla) during simple unimanual reaching and for bimanual coordinated feeding. Unimanual reaching consisted of grasping food on the ground, while bimanual feeding consisted of using one hand for holding a food and processing the food item by the opposite hand. No population‐level manual bias was found for unimanual actions but, in contrast, gorillas exhibited a significant population‐level right‐handedness for the bimanual actions. Moreover, the degree of right‐handedness for bimanual feeding exceeds any other known reports of hand use in primates, suggesting that lateralization for bimanual feeding is robust in captive gorillas. The collective evidence is discussed in the context of potential continuity of handedness between human and nonhuman primates. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

The Occurrence and Ape-to-Ape Transmission of the Entodiniomorphid Ciliate Troglodytella abrassarti in Captive Gorillas

ABSTRACT. Entodiniomorphid ciliates are often present in the colons of wild apes. In captive apes the infection tends to gradually disappear, with the exception of Troglodytella abrassarti . We used fecal examinations to screen the gorillas ( Gorilla gorilla gorilla ) in European (Czech Republic, UK) and Australian Zoos to explore the ape-to-ape transmission pattern of T. abrassarti . Gorillas from two out of three European Zoos were positive for T. abrassarti , while gorillas from the Australian Zoo were negative. We documented a horizontal transmission of T. abrassarti to a non-infected adult gorilla introduced into a Troglodytella -positive group in the Prague Zoo and traced the origin of the ciliate infection to the Paignton Zoo (UK) using serial fecal examinations. During this study, two infant gorillas born in the Prague Zoo (CZ) first became positive for T. abrassarti at the age of 9 mo. Ciliate morphology and the sequencing of the small subunit rRNA gene and the internal transcribed spacer rDNA spacer region revealed that T. abrassarti affects both captive gorillas and chimpanzees. We conclude that zoo transport plays a major role in the distribution of T. abrassarti among captive gorillas.     

Brief communication: Hand preference for bimanual and unimanual feeding in captive gorillas: extension in a second colony of apes

Right-hand dominance is widely considered to be a uniquely human trait. Whether nonhuman primates exhibit similar population-level hand preferences remains a topic of considerable debate. Despite extensive research focusing on laterality in nonhuman primates, our interpretation of these studies is limited due to methodological issues including the lack of a common measure of hand preference and the use of tasks that may not be reliable indicators of handedness. The use of consistent methods between studies is necessary to enable comparisons within and between species and allow for more general conclusions to be drawn from these results. The present study replicates methods used in recent research reporting population-level right-handedness in captive gorillas (Meguerditchian et al.,2010). Observational data were collected on hand preference for unimanual and bimanual feeding in 14 captive western lowland gorillas (Gorilla gorilla gorilla). Individual-level preferences were found, primarily for bimanual feeding; however, the data reveal no group-level directional bias (contra Meguerditchian et al.). Like the study by Meguerditchian et al. (2010), though, bimanual feeding revealed significantly stronger hand preferences than unimanual reaching, and age, sex, group membership, or rearing history had no effect on hand preference. Finally, variations in diet and corresponding grip type between studies suggest that hand preferences may vary across bimanual tasks depending on grip morphology. This study aims to contribute to our existing knowledge of primate laterality by increasing the number of individuals investigated using methods that allow for comparisons with similar research.     

Ear asymmetry and left-side cradling

Women and girls tend to cradle infants and dolls on the left side of the body. Left-sided cradling is found in chimpanzees and gorillas, is cross-cultural and present in historical works of art, and is transmitted down the human maternal line. One explanation for the left-cradling tendency is that it facilitates the flow of affective information from the infant via the left ear and eye to the center for emotional decoding, that is, the right hemisphere of the mother. We show that the developmental stability of the ear, as measured by ear asymmetry, is negatively correlated with the left-sided cradling tendency. Left-cradling English women holding infants and Jamaican girls holding dolls had a strong tendency to show lower ear asymmetry than right cradlers, whereas no such relationship was found in boys nor for various measures of asymmetry of the hand, with the possible exception of the wrist in Jamaican girls. Degree of handedness, as measured by the Annett peg-moving test, did not predict cradling preference in the Jamaican children, and the relationship between ear asymmetry and cradling preference was independent of hand preference. Our results suggest that developmental instability of the ear (including the pinna, external auditory meatus, and middle ear) may interfere with the flow of affective information to the right hemisphere. Ear asymmetry also showed evidence of strong maternal but not paternal transmission. It is suggested that between-individual variation of in utero stress may explain patterns of maternal transmission of lateral cradling tendencies.     

Transport of dead infant mountain gorillas by mothers and unrelated females

This report describes prolonged carriage of the corpses of two mountain gorilla infants by both related and unrelated adult females. Two hypotheses regarding this transport are considered: 1) that maternal behavior toward unrelated infants may be a by‐product of the hormonal condition of pregnancy, and 2) that the animals may be “learning to mother,” as nulliparous females could benefit from the experience of handling an infant that is no longer alive. Some factors pertinent to the event of infant deaths in captivity are considered. Zoo Biol 23:375–378, 2004. © 2004 Wiley‐Liss, Inc.     

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.     

Patterns of lateralized hand use in an arboreal primate, Simias concolor

Studies of hand use in nonhuman primates suggest that several species exhibit hand preferences for a variety of tasks. The majority of studies, however, focus on the lateralized hand use of captive nonhuman primate populations. Although captive settings offer a more controlled environment for assessing hand preferences, studies of wild populations provide important insights into how handedness is affected by natural environmental conditions and thus potential insights into the evolution of handedness. To investigate handedness in a population of wild nonhuman primates, we studied patterns of lateralized hand use during feeding in four simakobu monkeys (Simias concolor), an arboreal species inhabiting the Mentawai Islands, Indonesia. Our data show that individual variation in hand preferences for feeding existed among our study animals. In addition, each simakobu expressed a significant hand preference for supporting itself on a branch during feeding, an uncoordinated bimanual task. This bias was most prevalent when the branch used for support was a main branch rather than a terminal branch. When both hands were employed in a coordinated bimanual feeding activity (bimanual manipulation), only two subjects showed a significant bias for feeding. Our data suggest that these individuals are more likely to express significant hand preferences when feeding from stable, rather than precarious, positions within the canopy.     

Scan and focal sampling: reliability in the laterality for maternal cradling and infant nipple preferences in olive baboons, Papio anubis

We compared measures of laterality obtained by two observational sampling procedures (a 15-min focal-dyad sampling with continuous recording, and a scan and instantaneous sampling), using 10 mother-infant dyads of captive olive baboons. The two measures of lateral biases for maternal cradling, infant nipple preference, infant head position and maternal carrying, but not those for infant retrieval, were positively and significantly correlated. Our results clearly show that the two sampling procedures produce equally sensitive measures of lateral bias for both the maternal and the infant behaviours. They also provide evidence of asymmetries in mean bout length and therefore suggest that recording bouts is not necessarily the best measure of lateral bias. Taken together, these results show empirically that the scan and instantaneous sampling procedure does not lead to a lack of independence of data points, as previously assumed.     

The behavior of a zoo-housed infant orangutan after the death of its mother

The behavior of an infant female orangutan at Dublin Zoo before and after the death of her mother was recorded using scan sampling and compared. Social interactions and associations of the infant with the other individuals in the group were also compared before and after the death of her mother. Increases in climbing and object manipulation were observed, and a decrease in resting occurred. The infant orangutan significantly increased the amount of time she spent in close contact with another related adult female in the group after her mother's death. This case study describes an example of a zoo‐housed infant orangutan being successfully fostered by a related female without human intervention. It also provides a quantification of the behavior of an infant orangutan before and after being orphaned. Zoo Biol 30:205–211, 2011. © 2010 Wiley‐Liss, Inc.     

Introducing fecal stable isotope analysis in primate weaning studies

This research investigates the potential of a new, noninvasive method for determining age of weaning among primates using stable carbon and nitrogen isotope ratios in feces. Analysis of stable isotope ratios in body tissues is a well‐established method in archeology and ecology for reconstructing diet. This is the first study to investigate weaning in primates using fecal stable isotope ratios. Diets of a single François’ langur (Trachypithecus francoisi) mother–infant pair at the Toledo Zoo are reconstructed using this technique to track changes in infant suckling behavior over the weaning period. Stable isotope ratios in feces are sampled instead of more traditional samples such as bone or hair to enable daily, noninvasive snapshots of weaning status. Isotopic assessments of weaning status are compared to visual assessments to identify any discordance between the two. Three measurements documented the transition from breast milk to solid foods: stable carbon isotope ratios (δ¹³C), stable nitrogen isotope ratios (δ¹⁵N), and nitrogen content of feces (%N). It appears that solid foods were introduced at approximately 2 months of infant age, but that nursing continued into the 12th month, when sample collection ceased. Stable isotope data exposed a much longer weaning period than what was expected based on previously published data for captive langurs, and clarified visual estimates of weaning status. This reflects the method's sensitivity to suckling at night and ability to distinguish actual nursing from comfort nursing. After testing this method with zoo animals, it can readily be applied among wild populations. An isotopic approach to weaning provides a new, accurate, and biologically meaningful assessment of interbirth intervals, and facilitates a better understanding of mother–infant interactions. Both of these outcomes are critical for developing successful conservation strategies for captive and wild primates. Am. J. Primatol. 74:926‐939, 2012. © 2012 Wiley Periodicals, Inc.     

Non‐invasive fecal hormone analysis and behavioral observations for monitoring stress responses in captive western lowland gorillas (Gorilla gorilla gorilla)

Non‐invasive techniques for monitoring the stress response in captive western lowland gorillas (Gorilla gorilla gorilla) were investigated. Fecal samples for cortisol measurement and concurrent behavioral data were collected from six individuals in a socially housed gorilla group (one adult male, three adult females and their three offspring) over a 7‐month period. Despite inter‐individual variation in the dynamics of fecal cortisol concentrations over time, several major secretory peaks coincided across individuals. High cortisol concentrations in feces were correlated with induced stressors or behavioral observations indicating high social tension, with a 1–2 day lag period. Entry progression order of the gorillas into a den complex and a supplant‐based dominance index were suitable indicators of overall dominance hierarchies, and fluctuations over time reflected periods of instability. Diurnal variation in fecal cortisol was not apparent when comparing afternoon and morning samples, however the sample collection interval was relatively short (3–5 hr). These results demonstrate the feasibility of monitoring stress responses based on the dynamics of both fecal cortisol excretion and behavior. This non‐invasive approach may be used for gauging responses to changes in husbandry, environment and group structure of captive gorillas. Zoo Biol 0:1–15, 2005. © 2005 Wiley‐Liss, Inc.     

Baseline cortisol levels and social behavior differ as a function of handedness in marmosets (Callithrix jacchus)

Population hand preferences are rare in nonhuman primates, but individual hand preferences are consistent over a lifetime and considered to reflect an individual's preference to use a particular hemisphere when engaged in a specific task. Previous findings in marmosets have indicated that left‐handed individuals tend to be more fearful than their right‐handed counterparts. Based on these findings, we tested the hypotheses that left‐handed marmosets are (a) more reactive to a social stressor and (b) are slower than right‐handed marmosets in acquiring a reversal learning task. We examined the hand preference of 27 male and female marmosets (ages of 4–7 years old) previously tested in a social separation task and a reversal learning task. Hand preference was determined via a simple reaching task. In the social separation task, monkeys were separated from their partner and the colony for a single 7‐hr session. Urinary cortisol levels and behavior were assessed at baseline, during the separation and 24 hr postseparation. Hand preferences were equally distributed between left (n = 10), right‐handed (n = 10), and ambidextrous (n = 7) individuals. The separation phase was associated with an increase in cortisol levels and behavioral changes that were similar across handedness groups. However, cortisol levels at baseline were positively correlated with right‐handedness, and this relationship was stronger in females than in males. In addition, the occurrence of social behaviors (pre‐ and postseparation) was positively correlated with right‐handedness in both sexes. Baseline cortisol levels did not correlate significantly with social behavior. Acquisition of the reversals was poorer in females than males but did not differ as a function of handedness. We conclude that (a) both stress reactivity and cognitive flexibility are similar across handedness groups and (b) left‐handers exhibit less social behavior and have lower basal cortisol levels than ambidextrous and right‐handed subjects. The underlying causes for these differences remain to be established.     

Termite fishing laterality in the fongoli savanna chimpanzees (Pan troglodytes verus): Further evidence of a left hand preference

Whether nonhuman primates show population‐level handedness is a topic of much scientific debate. A previous study of handedness for termite fishing reported population‐level left handedness in the chimpanzees from Gombe National Park, Tanzania. In the current study, we examined whether similar hand preferences were evident in a savanna‐dwelling chimpanzee population with regards to termite fishing. Hand preference data were collected for 27 chimpanzees from February 2007 through July 2008 and November 2011 through January 2012 in southeastern Senegal. Overall, the Fongoli chimpanzees demonstrate a trend toward population‐level handedness, though the results did not reach conventional levels of statistical significance likely due to the limited sample size. Fongoli chimpanzees showed the same pattern of left hand preference as reported at Gombe and the two populations did not differ significantly. When the data were combined across all studies, wild chimpanzees showed a population‐level left hand preference for termite fishing. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Individual variation in the growth of captive infant gorillas

Serial anthropometric data were obtained during the first year of life of six nursery-reared infant gorillas in the Columbus (Ohio) Zoo. Two of the infants are likely to be monozygotic twins as determined by DNA analysis. Growth curves were fitted to serial measures of cephalo-thoracic-abdominal length, arm length, leg length, head circumference, upper arm circumference, and weight from each gorilla, to describe individual patterns of variation in skeletal growth and body composition. Growth in skeletal measures tended to be curvilinear to varying degrees over the first year of life. Body composition varied more than skeletal measures throughout the first year as a consequence of individual health status. Individual growth and body composition variations appear to reflect both genetic and environmental influences in this small sample of captive infant gorillas.     

Seasonal shifts in giant panda feeding behavior: relationships to bamboo plant part consumption

The giant panda (Ailuropoda melanoleuca) is classified as a carnivore, yet subsists on a diet comprised almost exclusively of bamboo. Wild and captive giant pandas use highly selective foraging behaviors for processing and consuming bamboo. These behaviors are for the first time quantified in captive giant pandas over a 5‐year period of time showing highly specific seasonal trends. Giant panda feeding behavior was recorded using live video observations of two giant pandas housed at the Memphis Zoo from November 2003 to June 2008. Leaf was the primary plant part consumed from June to December, whereas culm was consumed primarily from February to May, with both bears displaying similar seasonal shifts in plant part consumption. From May to June, leaf consumption increased significantly (P‐values<0.001); from June to August, leaf consumption remained high and stable. From December to March, leaf consumption decreased significantly (P‐values<0.001). Specific behaviors for bamboo leaf and culm consumption were also observed. Both bears formed wads of leaves before ingestion while feeding on leaf, but the male employed this feeding behavior more often than the female (54 and 33%, respectively). Both bears used similar culm‐stripping behavior (26 and 25%), used to remove the outer layer and isolate the pith for consumption. This study indicates that unique seasonal foraging behaviors observed in wild pandas are also apparent in captive animals in relation to plant part selectivity and feeding behaviors. Zoo Biol 29:470–483, 2010. © 2009 Wiley‐Liss, Inc.     

Baby-transfer and other interactions between its mother and grandmother in a captive social group of lowland gorillas

This report describes the responses of an experienced gorilla mother to inappropriate maternal behavior displayed by her young adult daughter toward a newborn baby and repeated acts of baby-transfer between these two females in a captive social group of lowland gorillas (Gorilla g. gorilla). The quality of infant care by the young adult daughter clearly improved during the first 4 days after birth, and this improvement was at least partly based on her mothers encouragement. Thus, the mothers activities can be considered scaffolding for her daughter with regard to maternal infant care.     

Social dynamics modify behavioural development in captive white-cheeked (<Emphasis Type="Italic">Nomascus leucogenys</Emphasis>) and silvery (<Emphasis Type="Italic">Hylobates moloch</Emphasis>) gibbons

Behavioural development was quantified in one family group of silvery gibbons (Hylobates moloch) and one of white-cheeked gibbons (Nomascus leucogenys) over 11 months during 2005 and 2008 at the Perth Zoo. Levels of locomotion, solo play and play solicitation peaked by 5 years of age but continued solo and social play in older immatures suggested that social development continued until at least 7 years of age. Mature offspring responded to play solicitations from younger siblings. The transition to sub-adulthood was marked by the presence of spatial peripheralisation from the parents, and coincided with aggression from the father to a sub-adult male. After the birth of a new infant, the male sub-adult stayed closer to his mother (and the infant) but not to his father; his juvenile brother was closer to both parents. Within-family observations of behaviour that is difficult to observe in the wild but can be observed in captivity contributes to our understanding of family dynamics in gibbons. Observations of these captive groups suggest that sub-adult peripheralisation may be influenced by family social dynamics as well as by local ecology, and that older offspring are responsive to the development of younger siblings.