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.     

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.     

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.     

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.     

Density of herbaceous plants and distribution of western gorillas in different habitat types in south‐east Cameroon

The study of forest herb availability improves knowledge of ecology and conservation of gorillas that depend on such herbs. Density patterns of herbs and location of western gorilla nest sites were studied in different habitat types at a site in south‐east Cameroon to assess their relationship. Herb stems of the families Marantaceae and Zingiberaceae were identified and counted in 10,713 1‐m² plots distributed within six habitat types. Stem density correlated with light availability and ranged from 2.38 stems m^?² in near primary forest to 4.66 stems m^?² in light gaps. Gorillas showed marked preferences for habitats with high herb densities such as light gaps, swamps and young secondary forest. However, no clear relationship exists between terrestrial herbaceous vegetation and gorilla densities across Central Africa. It is suggested that differences in ecological factors and land use history within and between sites may explain differences in herb density and diversity which partly account for variations in the historical and present population distribution and density of western gorillas. Formerly logged and swamp forests, which are characterized by an abundance of herbs, may prove to be of great value in the conservation of western gorillas given appropriate forest management practices, adequate protection from poaching and limited human encroachment.     

The effect of feeding enrichment methods on the behavior of captive Western lowland gorillas

Three feeding enrichment treatments were tested in an outdoor yard used by six Western lowland gorillas (Gorilla gorilla gorilla). In "Yard-toss," forage was thrown by hand over one third of the yard. In "Set-up," forage and browse were hand-scattered throughout the yard. "Set-up Enriched" was similar with the addition of either a hay- and forage-filled feeder or forage-filled boomer ball(s) suspended from a climbing structure. Each treatment was presented on 5 d. Behavior was recorded for 30 min before (baseline) and 30 min after the start of each treatment. All treatments led to more foraging and less inactivity compared with baseline (P80.05), but Yard-toss was the least effective, likely because resources were clumped and monopolized by dominant animals. In Set-up Enriched, dominant animals had the greatest increase in foraging (P=0.03), partly because they generally monopolized the suspended items, but this allowed others to forage at ground level. This separation of the animals likely explains why Set-Up Enriched led to more foraging than all other treatments (P80.05). Findings show that for these hierarchical animals, enrichment resources are most effective when distributed widely, including vertically, and that enrichment strategies must take social structure into account.     

Changes in nearest‐neighbor associations in a captive group of western lowland gorillas after the introduction of five hand‐reared infants

The successful management of a captive gorilla population often necessitates the hand‐rearing of infants and their subsequent re‐integration into social groups of conspecifics. In the present study we quantified the changes in nearest‐neighbor associations in a group consisting of a silverback male, three adult females, and two sub‐adult females after the introduction of five hand‐reared infants. Additionally, we examined the associations among kin and non‐kin group members to determine whether genetic relatedness was a factor influencing the integration of the infants into the group and the subsequent patterns of association among infants and adults. Results showed that after the introduction, the silverback male spent >60% of his time in close proximity to an infant and 10% of his time within a “cluster” of infants. There was a significant change in a female's nearest‐neighbor associations; however, the change did not include an infant. The most significant finding among infants was a strong bias by each to associate with another infant. When the infants associated with an adult, three of the five associated most with the silverback male (P < 0.001), whereas the other two infants distributed their time among all the adults. The most significant change in behavior patterns was exhibited by one of the sub‐adult females who displayed parental behaviors 18% of the time compared to <1% for all other females. Adults and one sub‐adult female associated significantly more often with related infants compared to unrelated infants (P < 0.025), and the infants showed a bias to associate with another related infant (P < 0.0001). Results of an infant's association with an adult showed that three of the five infants preferred to associate with a related adult (P < 0.0001). An individual's age, sex, and behavioral profile may have also influenced association patterns among group members. These findings lend strong support to the importance of peer groups and the presence of a silverback male for facilitating the integration of hand‐reared infants into established adult groups. Zoo Biol 18:261–278, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

High‐fiber diet promotes weight loss and affects maternal behavior in vervet monkeys

The dramatic increase in obesity in western societies has shifted the emphasis in nutrition research from the problems of undernutrition to the adverse consequences of being overweight. As with humans, Old World monkeys are at increased risk for type II diabetes and other chronic diseases when they gain excessive weight. To prevent overweight and obesity, promote animal health, and provide a more natural level of fiber in the diet, the standard commercial monkey chow diet at a vervet monkey breeding colony was changed to a higher fiber formulation in 2004. The new diet was also higher in protein and lower in carbohydrate and energy density than the standard diet. Because maternal behavior is known to be sensitive to differences in resource availability, data on weight and mother–infant interactions for 147 mothers with 279 infants born from 2000 through 2006 were assessed for effects of the diet change. The results showed that, even though food was provided ad libitum, the mean body weight of breeding females was 10% lower after the transition to the high‐fiber diet. Behaviorally, mothers on the high‐fiber diet were significantly more rejecting to their infants, and their infants had to play a greater role in maintaining ventral contact in the first few months of their lives. The effects of the diet change on maternal rejection were significantly related to the mother's body weight, with lower‐weight mothers scoring higher in maternal rejection. These results demonstrate that maternal behavior is responsive to changes in maternal condition, and that beneficial changes in the diet may have unintended consequences on behavior. Am. J. Primatol. 72:234–241, 2010. © 2009 Wiley‐Liss, Inc.     

Inter-group encounters and female transfer in mountain gorillas: Influence of group composition on male behavior

This paper examines the behaviors used by male gorillas (G. gorilla beringei) to influence female choice during inter-group encounters. Encounters are related to the acquisition of females rather than to the defense of a group's range. Data on 58 independent encounters confirms that encounters are generally aggressive, but that contact aggression is less frequent than previously reported. A high number of potential migrants in one of the groups involved, rather than the newness of either group, predicts the likelihood of contact aggression between males. Encounters with a newly formed unit last longer than encounters involving established groups. Male herding serves to prevent female transfer. Females without dependent offspring are more likely than others to be herded. Proceptive females are the target of herding more often than non-proceptive cycling females. Groups where herding has been observed are more likely to be newly formed, and they include significantly more males. This last result confirms that there are advantages to male cooperation in gorillas. It also raises the question of why such cooperation does not occur more often. © 1993 Wiley-Liss, Inc.     

Ape behavior in two alternating environments: comparing exhibit and short‐term holding areas

In many facilities, primates are voluntarily transferred between different enclosures on a daily basis to facilitate animal husbandry and exhibit maintenance. This procedure is particularly relevant in the management of great apes living in zoos, where the requirements of functional management must be balanced with the desire to maintain enriching and naturalistic exhibit enclosures that benefit ape residents and attract the visiting public. In these settings, examinations of ape behavior and welfare typically focus exclusively on activity in the primary exhibit area. However, physical, social and sensory experiences unique to each area may shape different patterns of behavior. In the current study, zoo‐living chimpanzees and gorillas were moved each day from exhibit areas to off‐exhibit holding areas for a short duration as a part of regular management procedures. Behavioral data indicated species‐specific reactions to the holding area, including increased aggression and self‐directed behavior by chimpanzees and increased activity and prosocial behavior among gorilla subjects. Both species showed more feeding‐foraging behavior while in the exhibit enclosure. Results suggest that holding areas may not meet all behavior needs of captive great apes and demonstrate the importance of including all components of the captive enclosure in comprehensive analyses of great ape behavior and welfare. Am. J. Primatol. 72:951–959, 2010. © 2010 Wiley‐Liss, Inc.     

Going to extremes for sodium acquisition: use of community land and high‐altitude areas by mountain gorillas Gorilla beringei in Rwanda

Space use in mammals may be influenced not only by their primary foods, but also by localized sources of physiologically critical resources such as sodium‐rich plants. We examined how sodium acquisition influences habitat use in mountain gorillas (Gorilla beringei) in Rwanda which have increased the amount of time they forage on community land outside of Volcanoes National Park (VNP), where eucalyptus (Eucalyptus spp.) tree bark is their most frequently eaten food. We measured sodium content in samples from 34 main dietary items and quantified sodium intake by 22 gorillas in three social groups over one year. On a dry weight basis, eucalyptus bark contains 3100 mg Na/kg. In contrast, the four herbs most frequently exploited for food inside the park are relatively sodium‐poor (<70 mg/kg each). Further, sodium intake rates were highest when the gorillas were on community land. Of the two groups that fed outside of the park, one obtained 73% and the other one 45% of their sodium in that habitat despite only feeding for minimal amounts of time there. However, one group that did not feed on community land acquired 78% of its sodium in the subalpine and alpine zones through the consumption of pith of giant lobelias and groundsels. Obtaining sodium thus likely creates an incentive for the gorillas to leave the park and make forays into high‐altitude habitat. Both strategies are not without risks: exiting their natural habitat and feeding on crops may increase human‐wildlife conflict and visiting high‐altitude areas may increase the risk of hypothermia.     

Effect of alanine supply on hepatic protein synthesis in animals maintained on a protein free diet

In contrast to what it is observed during starvation, animals maintained on a protein-free isocaloric diet showed an increase in the rate of hepatic peptide chain elongation as determined by measuring the ribosomal transit time in vivo. The loss of body nitrogen per se is insufficient to generate the signal(s) which arrests hepatic peptide chain elongation. This observation suggests that it is an increase in gluconeogenic demand, and not the negative nitrogen balance, which is implicated in determining reciprocal changes in the rate of protein synthesis.The rate of protein synthesis, as expressed per mg of DNA, does not change in protein deprived animals, while the RNA to DNA ratio decreased. These data also agree with a higher ribosomal efficiency at the elongation step. The animals maintained on a protein-free diet have a decreased hepatic content of protein and an increased concentration of valine, indicating an increased proteolysis.The enhanced rate of polypeptide elongation observed in animals kept on a protein-free diet was accompanied by decreases in the state of aggregation of polyribosomes and in the ability of liver extracts to form eIF-2 catalyzed ternary complexes. These observations suggest that the activity of the hepatic initiation factor in vivo may not be rate limiting.The administration of alanine in vivo to animals maintained on a protein-free diet showed a preferential effect in reaggregating polyribosomes. This action was neither accompanied by detectable effects on the rate of eIF-2 catalyzed ternary complexes formation nor by significant changes in the rate of elongation. It is concluded that factors other than eIF-2 activity or the rate of polypeptide elongation must be controlling the hepatic polyribosomal state of aggregation.