Effects of hand‐rearing on the reproductive success of western lowland gorillas in North America

This study sought to assess the potential effects of hand‐rearing by evaluating the relationships among rearing type and reproductive success in the American Zoo and Aquarium Association's Species Survival Plan^® for western lowland gorillas. Our study included data on 697 gorillas: 257 wild‐born (WB) and 440 born at zoos or related facilities in North America. We found no significant differences in the number of reproductive zoo‐born (ZB) and WB females, but more WB males sired infants than their ZB counterparts. This was influenced by a skew in the number of reproductive years for WB males in the studbook. ZB males showed no difference in infants produced per reproductive year, as compared to WB males, while ZB females produced more infants per reproductive year than did WB females. Mother‐reared (MR), ZB females produced more offspring and used more reproductive opportunity than hand‐reared (HR) females, whereas rearing had no effect on the reproductive success of ZB males. Moreover, MR and partially hand‐reared (PHR) females were more likely to become nurturing mothers themselves. Zoo Biol 21:389–401, 2002. © 2002 Wiley‐Liss, Inc.     

Urinary androgen and corticoid levels in captive, male Western lowland gorillas (Gorilla g. gorilla): age- and social group-related differences.

Urinary androgen and corticoid levels were measured for 52 captive male Western lowland gorillas to examine age-related variance and potential differences resulting from various social situations. Significant diurnal variation was present in both hormones. Age-related differences in androgens revealed that males experienced two stages of androgen increase and one stage of decrease: increases occurred from juvenile (less than 10 yr of age) to subadult (between 10-13 yr) and subadult to young adult (14-20 yr), whereas decreases occurred from young adult to adult (> 20 yr). Age-related differences in corticoid levels varied depending on the time of day, but morning corticoids were greatest in juvenile males, followed by young adult males. The type of social grouping was associated with differences in corticoid levels, as animals housed socially (in either a heterosexual or all-male group) had similar corticoid levels, whereas solitary males showed greater corticoid levels than their socially-housed counterparts. The increased levels of corticoids in solitary-housed males suggest this management strategy might not be optimal, although more data are needed. Additionally, the significantly greater levels of androgens and corticoids in young adult male gorillas may present management challenges, and thus zoos may need to consider increasing the flexibility of their current management practices with respect to males.     

Regurgitation and reingestion in captive gorillas: Description and intervention

Direct observation of regurgitation and reingestion (r/r) of captive gorillas was used to describe and catalog this behavior and thus lay the groundwork for possible intervention in the r/r cycle. Analysis of questionnaires regarding 117 gorillas at 17 zoos suggests that social deficits during early development contribute to the occurrence of r/r later in life. Wild-caught and captive-born, hand-reared gorillas show higher incidence of r/r than that of mother-reared infants. R/r increases the daily ingestion time. Feeding browse decreases r/r and increases time spent feeding from about 11% of the day to 27% of the day.     

Regurgitation/reingestion and coprophagy in captive gorillas

The behavior of wild animals can be significantly affected by captivity. Among the least documented adaptations are (1) the regurgitation and reingestion of food and (2) coprophagy. This paper reviews the occurrence of the two phenomena in captive lowland gorilla populations. In addition, data and speculations based on wild populations are discussed. Data from a preliminary study at the Stone Zoo are reported, and several causal relationships are explored.     

Effects of combination birth control on estrous behavior in captive western lowland gorillas, Gorilla gorilla gorilla

Combination birth control pills (CBC) are one of the most common birth control methods used for western lowland gorillas (Gorilla gorilla gorilla) housed in zoos. Since zoos are interested in maintaining as many natural behaviors as possible, it is important to know how contraception may affect social and sexual interactions among group members. Although some data are available regarding the influence of the pill on sexual behavior in human females, no data are available on its effects on gorilla estrous behavior. We examined temporal trends of estrous, aggressive, affiliative, and activity budget data in four females on CBC at the Lincoln Park Zoo in Chicago, IL. Behavioral data were collected using point sampling, all-occurrence records, and one-zero sampling. Estrous behavior occurred in less than 1% of observations. Using all-occurrence and one-zero sampling, estrous behavior occurred more frequently in week one of the cycle than any other week. The focal females exhibited affiliative, aggressive, and activity budget data evenly across their cycles. There were also no temporal trends in proximity to the silverback. Females varied by the types of estrous behavior they exhibited. We give a hormonal explanation for the prevalence of estrous behaviors in week one, and recommendations for effective behavioral sampling of gorilla estrous behavior.     

An experimental study of nettle feeding in captive gorillas

Mountain gorillas (Gorilla beringei beringei) in Karisoke, Rwanda, feed on the stinging nettle Laportea alatipes by means of elaborate processing skills. Byrne [e.g. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 358:529–536, 2003] has claimed that individuals acquire these skills by means of the so‐called program‐level imitation, in which the overall sequence of problem‐solving steps (not the precise actions) is reproduced. In this study we present western lowland gorillas (Gorilla gorilla gorilla) with highly similar nettles. Twelve gorillas in three different groups (including also one nettle‐naïve gorilla) used the same program‐level technique as wild mountain gorillas (with differences mainly on the action level). Chimpanzees, orangutans, and bonobos did not show these program‐level patterns, nor did the gorillas when presented with a plant similar in structural design but lacking stinging defenses. We conclude that although certain aspects (i.e. single actions) of this complex skill may be owing to social learning, at the program level gorilla nettle feeding derives mostly from genetic predispositions and individual learning of plant affordances. Am. J. Primatol. 70:584–593, 2008. © 2008 Wiley‐Liss, Inc.     

Feeding ecology of western lowland gorillas in the Nouabalé-Ndoki National Park,Congo

The feeding ecology of western lowland gorillas (Gorilla gorilla gorilla) living in the Nouabalé-Ndoki National Park, northern Congo, was surveyed for one full year. This is the first record to make clear the seasonal changes in the feeding habits of gorillas in a whole year, living in the primary lowland forest almost completely undisturbed. Fecal contents, feeding traces, and direct observation were analyzed with reference to a fruit availability survey. Although the gorillas fed largely on fruits in the forest, their basic diet was fibrous parts of plants, including shoots, young leaves, and bark. Terrestrial herbaceous vegetation, such as monocotyledons of the Marantaceae and aquatic herbs having much protein content and minerals, were frequently eaten even in the fruiting season. As these highly nutritious fibrous foods were superabundant all year, the major foods of the Ndoki gorillas seemed to be those plants. However, they selected fruits as their alternative food resources in the fruiting season. Gorillas foraged on many fruit species, while showing strong preferences for some particular species. The swamp forest, including marshy grasslands, was an important and regular habitat for the Ndoki gorillas.     

Impact of ecological and social factors on ranging in western gorillas

We examined the influence of ecological (diet, swamp use, and rainfall) and social (intergroup interaction rate) factors on ranging behavior in one group of western gorillas (Gorilla gorilla gorilla) during a 16-month study. Relative to mountain gorillas, western gorillas live in habitats with reduced herb densities, more readily available fruit (from seasonal and rare fruit trees), and, at some sites, localized large open clearings (swamps and "bais"). Ranging behavior reflects these ecological differences. The daily path length (DPL) of western gorillas was longer (mean=2,014 m) than that of mountain gorillas, and was largely related to fruit acquisition. Swamp use occurred frequently (27% of days) and incurred a 50% increase in DPL, and 77% of the variation in monthly frequency of swamp use was explained by ripe fruit availability within the swamp, and not by the absence of resources outside the swamp. The annual home-range size was 15.4 km2. The western gorilla group foraged in larger areas each month, and reused them more frequently and consistently through time compared to mountain gorillas. In contrast to mountain gorillas, intergroup encounters occurred at least four times more frequently, were usually calm rather than aggressive, and had no consistent effect on DPL or monthly range size for one group of western gorillas. High genetic relatedness among at least some neighboring males [Bradley et al., Current Biology, in press] may help to explain these results, and raises intriguing questions about western gorilla social relationships.     

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro‐ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the host's external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga‐Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context.     

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.     

Behavioral responses of an infant gorilla to maternal separation in a captive social group of lowland gorillas (Gorilla gorilla gorilla)

The present report describes behavioral reactions of a 33-month-old female infant gorilla to maternal separation in a captive social group whose composition is similar to that of wild groups. The infant gorilla responded differently to two types of maternal separation. When she remained alone for a few hours, she cried repeatedly and moved restlessly, indicating protest. Upon reunion and also for a few days thereafter, an intensification of the mother-infant relationship occurred. On the other hand, when she was separated from her mother but remained with the other group members for nine days, she did not display any behaviors that could be characterized as protest, but rather showed clear behavioral depression. During the 9-day separation period, she hardly played with other group members but she developed affiliative relationships with the leading male. After the reunion from the 9-day separation, she spent as much time near her mother as before separation and played with other infants at a level similar to that before separation, while she sometimes displayed behavioral patterns demanding the maintenance of physical contact with her mother. The present findings are compared with other reports in great apes and human children.     

Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory

The most important environmental factor explaining interspecies variation in ecology and sociality of the great apes is likely to be variation in resource availability. Relatively little is known about the activity patterns of western lowland gorillas (Gorilla gorilla gorilla), which inhabit a dramatically different environment from the well‐studied mountain gorillas (G. beringei beringei). This study aims to provide a detailed quantification of western lowland gorillas' activity budgets using direct observations on one habituated group in Bai Hokou, Central African Republic. We examined how activity patterns of both sexes are shaped by seasonal frugivory. Activity was recorded with 5‐min instantaneous sampling between December 2004 and December 2005. During the high‐frugivory period the gorillas spent less time feeding and more time traveling than during the low‐frugivory period. The silverback spent less time feeding but more time resting than both females and immatures, which likely results from a combination of social and physiological factors. When compared with mountain gorillas, western lowland gorillas spend more time feeding (67 vs. 55%) and traveling (12 vs. 6.5%), but less time resting (21 vs. 34%) and engaging in social/other activities (0.5 vs. 3.6%). This disparity in activity budgets of western lowland gorillas and mountain gorillas may be explained by the more frugivorous diet and the greater dispersion of food resources experienced by western lowland gorillas. Like other apes, western lowland gorillas change their activity patterns in response to changes in the diet. Am. J. Primatol. 71:91–100, 2009. © 2008 Wiley‐Liss, Inc.     

Functional analysis of social staring behavior in an all-male group of mountain gorillas

A total 202 social staring episodes (prolonged gazing by one individual toward another within a short distance) were observed in various social contexts among six unrelated, adult, and subadult male mountain gorillas. Staring was not accompanied by distinct facial expressions by actors or recipients, irrespective of their age or dominance rank. Younger, subordinate animals tended to stare at elder, dominant animals more frequently than vice versa. Staring may have multiple functions depending on the social context. In the initiation of non-agonistic interactions, staring rarely occurred, but was very successful for younger males in eliciting play or homosexual interactions from older animals. Staring was also directed by younger males to older males for greeting or appeasement. It may possibly play a role in reducing the increased social tension that occurs during or after conflict and in averting the potential conflict among older males. Younger males occasionally supplanted older males by staring at feeding spots. This slow supplantation is similar to the phenomenon of food sharing achieved through begging behavior in chimpanzees and bonobos. A prolonged gaze including staring by subordinates towards dominants may characterize the frequent and prolonged face-to-face interactions in the African great apes, and contrasts with a frequent gaze aversion by subordinates towards dominants in macaques or baboons. A difference between gorillas and other apes is that, chimpanzees and bonobos make positive contact with each other through eye contact, while gorillas simply stare at another without physical contact in greeting or appeasement process. Staring may serve an effective strategy for younger male gorillas to intervene safely in olders' conflict and sometimes to suppress or inhibit olders' performance, but their non-agonistic contacts or supporting attacks may not contribute to the establishment or support of social bonds between them. It is possible that staring may be common among the African great apes and man, and that it has evolved as a tactics to mask the dominant/subordinate relationships between individuals with multiple functions.     

Spatial memory and foraging competition in captive western lowland gorillas (Gorilla gorilla gorilla)

Spatial memory and foraging competition were investigated in three mother/offspring pairs of western lowland gorillas,Gorilla gorilla gorilla, using a naturalistic foraging task at the Toronto Zoo. Sixteen permanent food sites were placed throughout the animals’ enclosures. All of the sites were baited and a pair of animals was free to visit the sites and collect the food. Five of the subjects collected the food with accuracy better than chance. Most of the subjects visited the sites using a pattern, and for half the subjects this was one of adjacency. The high accuracy of five of the subjects and the lack of a consistent adjacency pattern suggest that the animals did in fact use spatial memory. Furthermore, the gorillas tended to avoid visiting food sites that had been previously depleted by their partner. They also appeared to split their search of the enclosures, each visiting only a proportion of the food sites. This indicated that the animals were competing and altering their foraging behaviour based on the behaviour of their partner. Therefore, accuracy was recalculated to take this into account. When the sites depleted by either animal in a pair during a given trial were worked into the accuracy calculations for individual animals, three of the animals still maintained accuracy above chance. This suggests that the animals were not only able to remember which sites they had depleted, but those sites depleted by their foraging partner as well.     

Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human

In this study we investigated the communicative abilities of 10 orangutans (Pongo pygmaeus) and seven western lowland gorillas (Gorilla gorilla gorilla), and particularly focused on their sensitivity to the attentional state of a human experimenter when choosing from a repertoire of both auditory and visual communication strategies. In experiment 1 a banana was placed in front of the subject's cage and a human experimenter was either present or absent. The subject's behavior was recorded for 60 sec. Both gorillas and orangutans gestured (t(16)=-3.58, P<.005) and vocalized (t(16)=-2.47, P<.05) more when the experimenter was present. In experiment 2 a human experimenter held a banana in front of the subject's cage and was oriented either toward or away from the subject. Again the subject's behavior was recorded for 60 sec. In this experiment both gorillas and orangutans gestured significantly more frequently (t(16)=3.40, P<.005) when the experimenter was oriented toward them. In addition, gorillas and orangutans used other forms of visual communication signals, such as lip pout (t(16)=3.66, P<.005), barter/trade (t(16)=2.31, P<.05), and body present (t(16)=2.31, P<.05) significantly more when an experimenter was facing them. The overall results indicate that both gorillas and orangutans are sensitive to the attentional state of a human experimenter and use appropriate communicative signals to gain that individual's attention. These results are also similar to previous findings on communicative behaviors in chimpanzees.     

The development of infant play in a captive group of lowland gorillas (Gorilla gorilla gorilla)

Three infant gorillas born at the Yerkes Regional Primate Research Center of Emory University were studied during their first year and one-half of life for various aspects of behavior, including solitary and social play, using both focal animal and one-zero sampling. The appearance of play in these infants followed a developmental trend, beginning with mother-infant play, and followed by solitary play, and then social play among peers. Mothers were initially very vigilant, repeatedly interrupting infant peer play bouts, this relaxing toward the end of the first year. Evidence for a possible sex difference in active social play is presented.     

Ecology of gorillas and its relation to female transfer in mountain gorillas

Understanding the principles that underly primate social evolution depends on integrated analysis of data on behavioral ecology, demography, life history tactics, and social organization. In this paper, data on the behavioral ecology of gorillas are reviewed and comparisons made among the three subspecies. Gorillas are selective feeders; and, their patterns of food choice are consistent with models of feeding by large generalist herbivores. They rely heavily on terrestrial herbaceous vegetation, which provides an abundant supply of densely distributed food. Availability of this food varies little in space and time; and, gorilla foraging activity can maintain its productivity. The level of frugivory and the extent of seasonal variation in diet and habitat use vary among and within populations. Low variability in food distribution patterns makes cooperative defense of foraging areas not worthwhile; but, it also means that ecological costs associated with gregariousness are low. However, demographic and life history data on mountain gorillas show that these costs may be sufficient to reduce female reproductive success as group size increases. Advantages to being with high quality males apparently can outweigh these costs. The implications of these data for the evolution of the mountain gorilla social system, and the possible roles of male protection, predation, and female/female competition in this regard, are discussed.     

The costs of infant carrying in captive cotton-top tamarins

Marmosets and tamarins have a communal rearing system in which all group members help to care for the twin infants characteristic of this family of primates. Helpers are likely to incur time and energy costs by contributing to infant care. Predictions that cotton-top tamarin (Saguinus oedipus) helpers would change their behavior when carrying infants because of reduced mobility and/or a need for increased vigilance were tested in a captive colony. Tamarins carrying an infant spent significantly less time feeding, foraging, moving, or engaging in social activities such as grooming than they did when not carrying. Frequencies of scratching, autogrooming, and scent marking were significantly reduced in carriers, suggesting that their mobility was reduced. However, carriers were significantly less likely to be vigilant (measured by direction of gaze) than when not carrying. Further observations showed that carriers spent more time in concealed areas than they did when not carrying and were probably therefore adopting a cryptic strategy to reduce predation risks to themselves and to infants. These results demonstrate that tamarin helpers pay costs by carrying infants. Some possible compensating benefits are indicated.