The effect of visitors on the behavior of zoo-housed western lowland gorillas (Gorilla gorilla gorilla)

Primates, especially apes, are popular with the public, often attracting large crowds. These crowds could cause behavioral change in captive primates, whether positive, neutral, or negative. We examined the impact of visitors on the behavior of six western lowland gorillas (Gorilla gorilla gorilla), observing the troop over 6 weeks during high season (4.5 hr/day, 35 days, May–July 2016). We used focal scan sampling to determine activity budget and enclosure usage, and focal continuous sampling to identify bouts of anxiety-related behavior (visitor-directed vigilance, self-scratching, and aggression). Both daily zoo-entry numbers (V_GATE) and instantaneous crowds at the exhibit (V_DENSITY) were measured. Overall, V_GATE had little effect across behaviors. However, consistent with the more acute time frame of measurement, V_DENSITY was a better predictor of behavior; at high crowd volumes, we observed significant group-level changes in activity budget (increased inactivity, increased locomotion, and decreased environment-related behaviors), increase in some anxiety-related behaviors, and decreased enclosure usage. Although contributing similar effects, it could not be determined if crowd numbers, composition, or noise most affected the troop, nor any chronic effects of exposure to large crowds. Nevertheless, our findings suggest that measures to minimize the impacts of large crowds at the exhibit would be beneficial. Furthermore, we highlight potential discrepancies between common methods for measuring visitor numbers: V_GATE is less sensitive to detecting visitor effects on behavioral indices than V_DENSITY. Future studies should appropriately match the biological time frame of welfare indicators and visitor measures used to ensure the reliability of findings.     

Social interactions between captive adult male and infant lowland gorillas: Implications regarding kin selection and zoo management

Interactions between unrelated and related silverback‐infant dyads are compared in an attempt to assess the influence that kinship may have on male parental behavior. Observational data were collected on each member of two silverback‐infant dyads, in two separate enclosures at the Lincoln Park Zoo in Chicago, IL. The silverback was the father of the infant in one dyad, and unrelated to the infant in the other. Each infant was responsible for initiating most of the encounters with its respective group silverback. However, based on the frequency and duration of interactions, there is a significantly higher degree of affiliation and tolerance within the silverback‐offspring dyad. Furthermore, the unrelated infant was the recipient of more than 40% of the agonistic behaviors exhibited by the silverback, whereas no such encounters were recorded within the related dyad. Although alternative explanations must be considered, these findings are consistent with kin selection theory, are similar to observations documented for wild mountain gorillas, and provide uncommon comparative data on adult male interactions with related and unrelated infants. In addition, this study offers behavioral information relevant to the management of captive gorillas, which often requires the introduction of immatures into non‐natal groups. Zoo Biol 18:53–62, 1999. © 1999 Wiley‐Liss, Inc.     

Behavioral response of captive western lowland gorillas (Gorilla gorilla gorilla) to the death of silverbacks in multi‐male groups

In both free‐ranging and captive western lowland gorillas, a silverback provides protection and leadership, mediating conflict within a group. In the wild, when a dominant silverback dies the group will disperse or transfer to a solitary male, unless a subsequent male is present to inherit the group. In captivity, studies have focused on groups containing one male and therefore it is unclear how gorillas respond to the death or removal of a silverback in multi‐male groups. This study examined the behavior of a bachelor group (Cleveland Metroparks Zoo) and a multi‐male, mixed‐sex group (Pittsburgh Zoo and PPG Aquarium) following the death of two older silverbacks in 2005. Both of the younger but dominant males maintained their same level of dominance after the death. We predicted that agonism would increase after the death as groups struggled for social stablility. We did observe an increase in both agonism and displacements among the bachelor group, but only observed an increase in displacements among the mixed‐sex group. Although we predicted that there would be no change in solitary behavior, both groups decreased feeding and the mixed‐sex group increased self‐directed behavior post‐death. In the bachelor group, self‐directed behavior decreased and undesirable behavior increased. We also observed a difference in spatial distance after the death with members of the mixed‐sex group becoming more dispersed and members of the bachelor group more converged. This study demonstrates that there is a period of transition for multi‐male groups after the death or removal of the oldest silverback. Future research could integrate physiological measures with behavioral analyses before and after the death or removal of a prominent member of the group. Zoo Biol 29:16–29, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

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.     

Long‐term proximity relationships in a captive social group of western lowland gorillas (Gorilla gorilla gorilla)

To visualize long‐term social relationships among 12 gorillas in a captive breeding group at the San Diego Wild Animal Park, San Diego, CA, the multidimensional scaling (MDS) procedure was applied to proximity (within 5 m) values collected in five different periods over 2.5 years. The resulting two‐dimensional representations clearly show that in samples taken during this 2.5‐year period, the silverback male was surrounded by five adult females, while three infant or young juvenile females, gathered in a body, remained between the silverback male and adult females. Some adult females maintained proximity to the silverback male more frequently than other adult females throughout the five periods. Unlike mountain gorillas in the wild, females with dependent offspring did not tend to stay near the silverback male more frequently than other females, and related females did not tend to spend more time near each other than non‐related females. Three older juvenile or young adult males were plotted the furthest from the silverback male, with gradual changes with increasing age. The usefulness of the MDS procedure, which can be used to visualize easily and clearly the social relationships among individuals, is discussed from the viewpoint of the management of breeding groups of captive gorillas. Zoo Biol 20:197–209, 2001. © 2001 Wiley‐Liss, Inc.     

Seasonal change in the composition of the diet of eastern lowland gorillas

Details are presented of the composition of the diet of eastern lowland gorillas, derived mainly from a study of their fresh trails and fecal analysis, during the course of an entire year in the tropical lowland forests of the Itebero region, Zaire. Gorillas ate 194 plant foods from 121 species and 45 families. They consumed 48 species of fruits; and 89% of fecal samples contained fruit seeds, but fruits were a relatively small part (25%) of the total number of food items. The composition of their diet changed seasonally. When consumption of fruit decreased in the long rainy and the long dry seasons, the gorillas ate, in addition to Zingiberaceae and Marantaceae, many kinds of leaf and bark, which may be an important buffer against the shortage of fruits. Gorillas also fed regularly on ants (Ponerinae), and the frequency of consumption showed small seasonal variations. From a comparison of diet composition, eastern lowland gorillas appeared to be intermediate between the other two subspecies. The choice of food showed differences in preference of fruits and insects between subspecies and may reflect high similarities within subspecies in lowland and montane forests.     

Group size and structure in western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo

This paper describes the size and structure of western lowland gorilla groups visiting Mbeli Bai, a swampy forest clearing in northern Congo. An observation platform at the edge of the clearing was used over a 3-yr period, with gorillas visible for 1,681 hr. Data are presented on 14 groups and seven solitary males. Mean group size (excluding solitary males) was 8.4 +/- SD 4.3, and did not differ significantly from most other gorilla studies. All groups at Mbeli contained only one fully mature male and did not show evidence of fission-fusion or regular subgrouping. All emigrating males that remained in the population became solitary, and "bachelor" groups were not observed. Methodological issues are raised, including the classification of multi-male groups, and the demographic profiles of other populations are discussed in the light of results from Mbeli.     

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.     

A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas

Urinary steroid hormone levels were measured in wild male mountain gorillas (Gorilla gorilla beringei) to determine how levels of testosterone and cortisol corresponded with age and social rank. Urine samples were collected noninvasively from 18 males, ranging in age from 3–26 years, in three groups of wild mountain gorillas at the Karisoke Research Center, Rwanda, Africa, and samples were analyzed using radioimmunoassay procedures. Males were classified as being immature (<7 years), maturing (10–13 years), or adult (+13 years of age). Immature males had significantly lower levels of testosterone and higher levels of cortisol than both maturing and adult males. No differences in testosterone or cortisol levels were found between maturing and adult males. Dominant males exhibited a trend toward significantly higher levels of testosterone than subordinate males, but no difference was found between cortisol levels of dominant and subordinate males. These results suggest that the increase in testosterone associated with puberty occurs prior to any outward sign of development of secondary sexual characteristics. Within-group male–male competition may affect testosterone levels, but the lack of difference in cortisol levels between dominant and subordinate males suggests that subordinate males are not socially stressed, at least as measured by cortisol. Am. J. Primatol. 43:51–64, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Bed and bed-site reuse by western lowland gorillas (<Emphasis Type="Italic">Gorilla g. gorilla</Emphasis>) in Moukalaba-Doudou National Park,Gabon

In this paper we describe bed (nest) and bed-site reuse by western lowland gorillas (Gorilla g. gorilla) in Moukalaba-Doudou National Park, south-eastern Gabon. During an eight-month study 44 bed sites and 506 beds were found. Among these, 38.6% of bed sites and 4.1% of beds were reused. We analyzed the monthly frequency of bed-site reuse in relation to rainfall, fruit abundance, and fruit consumption by the gorillas. The different frequency of bed-site reuse in the rainy and dry seasons was not significant. More bed-site reuse was observed during the fruiting season than during the non-fruiting season. Results from fecal analysis suggested that gorillas ate more fruit in the fruiting season than in the non-fruiting season. The frugivorous diet of western gorillas may possibly cause gorillas to stay in some areas and, consequently, reuse their bed sites. Reuse of bed sites by gorillas suggests their frequent return to an area where preferred fruit is readily available. A higher percentage of arboreal beds may also affect bed-site reuse, because of the shortage of bed material.     

Peaceful post-conflict interactions between aggressors and bystanders in captive lowland gorillas (Gorilla gorilla gorilla)

We observed a colony of lowland gorillas in order to assess the occurrence of Peaceful Post-Conflict Interactions between Aggressors and Bystanders (PPIAB). We compared the dynamics of PPIAB with those of Peaceful Post-Conflict Interactions between Victims and Bystanders (PPIVB), which are directed toward victims. We confirmed the occurrence of PPIAB (mean Triadic Contact Tendency: 41.7%+/-16.2% SEM) at frequencies comparable to PPIVB. Immature gorillas were responsible for most PPIAB. PPIAB occurred when the bystander was unrelated to either the aggressor or the victim, and when it was a relative of the aggressor. However, affinitive contact rates were higher in the former case. Unlike PPIVB, PPIAB significantly reduced the likelihood of further aggressions within the group, suggesting that they work at an immediate level. Our data also suggest that bystanders decide when a peaceful contact may be too risky; in fact, neither PPIAB nor PPIVB occurred after high-intensity aggressions.     

Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic

The objectives of this 27 month study were to document the positional behaviors used by lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic and to compare the effects of body size dimorphism on the use of arboreal substrates. During this study, despite their great size, all gorillas used trees regularly. Predictions concerning the relationship of body size to arboreal behavior were generally upheld. Small branch and suspensory activities were rare for silverbacks. Females used smaller and multiple substrates and suspensory postures more frequently than males. Although females foraged in the periphery of trees, males stayed close to the cores and rarely used terminal branches. In addition to body size, this study found that party size, social rank, and tree structure all influence an animal's substrate choice and subsequent positional activities. Lone males typically remained in the cores of trees where substrates are large. Group males may have been forced to use all parts of trees because others were present. Lone males used small crown trees which provided easy access to terminal branch foods. Males and females foraging together used larger trees (containing more feeding sites) than single sex groups. Female positional behavior may have been affected by the presence of males. When apart from males, females used the cores of trees and larger substrates more than when foraging with males. As habitat and social context both influence substrate use, they should be considered essential components of body-sized based interpretations of the behavior of fossil or extant species. © 1995 Wiley-Liss, Inc.     

Population structure and group composition of western lowland gorillas in North‐Western Republic of Congos

Population studies are an essential part of conservation actions. Under exceptional observation conditions we studied a western lowland gorilla population visiting the Maya salt‐clearing (north of the Parc national d'Odzala, P.N.O., Congo) over an 8 month period; 36 groups and 18 solitary individuals (a total of 420 individuals) have been identified visiting the clearing, which suggests a high gorilla density in the region. Ninety‐six percent of the gorillas entered the clearing in groups. One‐male groups had a mean size of 11.2. Ninety percent of solitary individuals were silver‐back males. Compared with other populations of both lowland gorillas and mountain gorillas, the Maya population had the highest immature rate and the highest number of infants per female. Ecological correlates that could explain the attractiveness of the Maya clearing are discussed. The present status and the renewal rate of the Maya population indicate the need for further studies and confirm the importance of developing eco‐tourism in this region as part of the sustainable park management activities developed by the ECOFAC programme (European Union). The results also provide arguments to support the proposal for extending the P.N.O. to include this region, which is rich in salt‐clearings and attracts many other key‐species of mammal such as forest elephants. Am. J. Primatol. 48:1–14, 1999. © 1999 Wiley‐Liss, Inc.