Third-Party Intervention in Wild Western Lowland Gorillas (Gorilla gorilla gorilla)

International Journal of Primatology -     

Effects of selected behavioral enrichment devices on behavior of Western Lowland Gorillas (Gorilla gorilla gorilla)

Environmental complexity plays an integral role in the activity and psychological well-being of primates. The experiment described in this article evaluates the effects of nonintrusive, inexpensive, and easily managed behavioral enrichment devices on the behavior of a group of captive Western lowland gorillas. Devices used included cardboard boxes containing food items, paper bags containing food items, burlap rags, and willow and maple browse. The enrichment devices increased foraging, social play, and solitary play behaviors. Sedentary behaviors decreased. Rags, bags, browse, and boxes did not statistically decrease the incidence of regurgitation/reingestation or coprophagy. Depending on the type of enrichment item used, the effects on agonism and manipulation of enrichment item were variable. To make informed management decisions about the psychological well-being of captive animals, it is important to objectively quantify and examine the influences on their behavior.     

Socioecological Factors Influencing Intergroup Encounters in Western Lowland Gorillas (Gorilla gorilla gorilla)

International Journal of Primatology - Socioecological variables influence the rate and nature of encounters between conspecific primate groups. Both social (i.e., type of encounter) and ecological...     

Behavioral Responses of Silverback Gorillas (Gorilla gorilla gorilla) to Videos

This study examined the impact of video presentations on the behavior of 4 silverback, western lowland gorillas (Gorilla gorilla gorilla). On each of 5 occasions, gorillas viewed 6 types of videos (blue screen, humans, an all-male or mixed-sex group engaged in low activity, and an all-male or mixed-sex group engaged in agonistic behavior). The study recorded behavioral responses and watching rates. All gorillas preferred dynamic over static videos; 3 watched videos depicting gorillas significantly more than those depicting humans. Among the gorilla videos, the gorillas clearly preferred watching the mixed-sex group engaged in agonistic behavior; yet, this did not lead to an increase in aggression or behavior indicating agitation. Further, habituation to videos depicting gorillas did not occur. This supports the effectiveness of this form of enrichment, particularly for a nonhuman animal needing to be separated temporarily due to illness, shipment quarantine, social restructuring, or exhibit modification.     

Habitat Use and Structural Preferences of Captive Western Lowland Gorillas (Gorilla gorilla gorilla(: Effects of Environmental and Social Variables

Exhibit naturalism has become the architectural standard for new zoo exhibits, yet our scientific understanding of how animals interact with naturalistic environments is very limited. Given the expense incurred in building new exhibits, it is essential that more information on animal-environment interactions be obtained and that it be incorporated at the outset into exhibit designs. We documented four years of habitat use and structural preferences of western lowland gorillas at Zoo Atlanta. We found that quality of space rather than quantity of space was important, as subjects spent 50% of their time in <15% of the exhibits. Subjects showed strong preferences for the areas near structures, particularly the holding building, and spent significantly less time away from structures than expected. Temperature interacted with structural preferences in that the subjects spent more time away from structures when temperatures were cold and more time near them when temperatures were hot. There was no difference in habitat use and structural preferences due to age, sex, and rearing history, but social factors appear to play a role. Our results are similar to those found a decade earlier in the same population and to other studies of space use in apes but are the first to include significant temperature effects. Additionally, they suggest that managers and designers need to take into account factors such as quality of space, attractiveness of the holding building, and the interaction of structural preferences with variables such as temperature and social factors when designing exhibits.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.     

The Intestinal Entodiniomorph Ciliates of Wild Lowland Gorillas (Gorilla gorilla gorilla) in Gabon,West Africa

Examination of 109 fecal samples from wild lowland gorillas revealed the presence of five species of entodiniomorph ciliates: Troglodytella ahrassarti, Troglodytella gorillae, and three unclassified species. These latter three species were also found in the feces of a captive gorilla in Gabon and are considered to be intestinal parasites or commensals.     

Birth of a Western Lowland gorilla (Gorilla gorilla gorilla) following in vitro fertilization and embryo transfer

A 21-year-old multiparous female exhibiting 31–41 day menstrual cycles was given hFSH (225 IU/day, Metrodin 75, from cycle day 3 through 9 (menses = day 1) and hCG (10,000 IU, Profasi, on day 10 to stimulate follicular development. At 35 h after hCG, under isoflurane (AErrane) anesthesia, follicles were aspirated by controlled suction under transvaginal ultrasound guidance. Metaphase II oocyctes (n = 11) were placed in modified human tubal fluid (mHTF, 100 μl) medium under oil at 37°C in humidified 5% CO₂. Frozen semen, collected by voluntary ejaculation, was thawed (70°C H₂O bath, 6 sec), diluted slowly, centrifuged, and resuspended in mHTF, and 160,000 motile spermatozoa/ml were added at 6 h after oocyte recovery. At 21 h postinsemination (p.i.) eight oocytes were at the two-cell stage, five were cryopreserved, and three were cultured to the six- to eight-cell stage in mHTF with granulosa cells before transcervical uterine transfer at 47 h p.i. using a Teflon catheter. Micronized progesterone (400 mg/d) was orally administered for 10 weeks posttransfer (p.t.). Ultrasound examination revealed a single fetus at 15 weeks p.t., and unassisted delivery of a live 1.37 kg female infant occurred at 29 weeks. Am. J. Primatol. 41:247–260, 1997. © 1997 Wiley-Liss, Inc.     

Taste Responses to Fructose and Tannic Acid Among Gorillas (Gorilla gorilla gorilla)

We investigated the taste responses to fructose and tannic acid compounds among 6 western gorillas (Gorilla gorilla gorilla) at the San Francisco Zoo. We presented the subjects with 12 reference concentrations of 3–300 mM fructose, paired with tap water in paired-choice experimental trials. We subsequently presented them with tap water paired with 8 dilute concentrations of tannic acid (0.25–6 mM) dissolved in 100 mM fructose solutions and 8 concentrations (0.25–6 mM) dissolved in 300 mM fructose solutions. The gorillas exhibited a broadly similar preference threshold for fructose (50 mM) to those of other nonhuman primate and human samples. The gorillas tolerated moderate levels of tanninc acid, especially when presented in a very sweet package. The depressing effect of tannic acid on the ingestion of fructose solutions appeared to increase progressively with tannin concentration and was lower as fructose concentration increased. The inhibition threshold for tannic acid solutions was reached at 4 mM tannic acid in 100 mM fructose solution, and at 6 mM tannic acid in 300 mM fructose solutions. These results suggest that gorillas use sweetness as a criterion for food selection and regard those with moderate levels of tannins as palatable. Our findings corroberate food preference studies and nutritional analyses of wild gorilla foods indicating that they prefer sugary foods and readily consume ones containing moderate levels of tannins. Taste responses may facilitate a flexible frugivorous/folivorous diet among gorillas.     

Gorilla Mothers Also Matter! New Insights on Social Transmission in Gorillas (Gorilla gorilla gorilla) in Captivity

The present paper describes two distinct behaviors relating to food processing and communication that were observed in a community of five separately housed groups of lowland gorillas (Gorilla gorilla gorilla) in captivity during two study periods one decade apart: (1) a food processing technique to separate wheat from chaff, the so-called puff-blowing technique; and (2) a male display used to attract the attention of visitors, the so-called throw-kiss-display. We investigated (a) whether the behaviors were transmitted within the respective groups; and if yes, (b) their possible mode of transmission. Our results showed that only the food processing technique spread from three to twenty-one individuals during the ten-year period, whereas the communicative display died out completely. The main transmission mode of the puff-blowing technique was the mother-offspring dyad: offspring of puff-blowing mothers showed the behavior, while the offspring of non- puff-blowing mothers did not. These results strongly support the role mothers play in the acquisition of novel skills and vertical social transmission. Furthermore, they suggest that behaviors, which provide a direct benefit to individuals, have a high chance of social transmission while the loss of benefits can result in the extinction of behaviors.     

Nutritional Aspects of Western Lowland Gorilla (Gorilla gorilla gorilla) Diet During Seasons of Fruit Scarcity at Bai Hokou,Central African Republic

Traditionally, gorillas were classified as folivores, yet 15 years of data on western lowland gorillas (Gorilla gorilla gorilla) show their diet to contain large quantities of foliage and fruit, and to vary both seasonally and annually. The consumption of fruit by gorillas at Bai Hokou, Central African Republic, is correlated with rainfall and ripe fruit availability (Remis, 1997a). We investigated the nutritional and chemical content of gorilla foods consumed at Bai Hokou during two seasons of fruit scarcity as measured by phenological observations and compared our findings with the nutrient content of gorilla foods at other African sites. We conclude that during lean times, Bai Hokou gorillas consumed fruits with higher levels of fiber and secondary compounds than those of other populations of western lowland or mountain gorillas. Conversely, leaves consumed by Bai Hokou gorillas were relatively low in fiber and tannins. Bai Hokou gorillas appeared to meet their nutritional needs by eating a combination of fruit and foliage. They ate fruits comparatively high in secondary compounds and fiber when necessary. While gorillas are selective feeders, wherever and whenever preferred foods are scarce, their large body size and digestive anatomy enable them to consume and process a broader repertoire of foods than smaller bodied-apes.     

Behavioral responses of silverback gorillas (Gorilla gorilla gorilla) to videos

This study examined the impact of video presentations on the behavior of 4 silverback, western lowland gorillas (Gorilla gorilla gorilla). On each of 5 occasions, gorillas viewed 6 types of videos (blue screen, humans, an all-male or mixed-sex group engaged in low activity, and an all-male or mixed-sex group engaged in agonistic behavior). The study recorded behavioral responses and watching rates. All gorillas preferred dynamic over static videos; 3 watched videos depicting gorillas significantly more than those depicting humans. Among the gorilla videos, the gorillas clearly preferred watching the mixed-sex group engaged in agonistic behavior; yet, this did not lead to an increase in aggression or behavior indicating agitation. Further, habituation to videos depicting gorillas did not occur. This supports the effectiveness of this form of enrichment, particularly for a nonhuman animal needing to be separated temporarily due to illness, shipment quarantine, social restructuring, or exhibit modification.     

Assessing Initial Reintroduction Success in Long-Lived Primates by Quantifying Survival, Reproduction, and Dispersal Parameters: Western Lowland Gorillas (Gorilla gorilla gorilla) in Congo and Gabon

Postrelease monitoring is an important aspect of reintroduction projects, one outcome of which is to allow an assessment of the initial success of the reintroduction, often measured by quantifying survival and reproduction rates. In long-lived species, accurate estimations of demographic parameters are difficult to obtain, and therefore assessment of reintroduction success in such species is challenging. To assess the initial success of a reintroduction program for the long-lived, slow-reproducing, and critically endangered western lowland gorilla Gorilla gorilla gorilla, we analyzed postrelease monitoring data from 2 reintroduced populations, in the Batéké Plateau region of the Republics of Congo and Gabon, to quantify several demographic parameters, and compared our results with published data on wild gorilla populations. Annual survival rate of the 51 released gorillas was 97.4%, 9 females gave birth to 11 infants at an annual birth rate of 0.196 births per adult female, and first-year survival of the infants was 81.8%. Annual birth rate within the reintroduced populations is not significantly different from that given for wild western gorilla populations, and other demographic parameters fall within the range of published data for wild gorilla populations. Our analysis illustrates that the reintroduction program has been successful in terms of the initial measures of postrelease survival and reproduction, and our quantitative data should facilitate the development of a population model that can predict the probability of population persistence and therefore provide an indication of longer-term reintroduction success.     

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.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

Behavioral and hormonal responses to the availability of forage material in Western lowland gorillas (Gorilla gorilla gorilla)

We investigated how forage material affects indicators of welfare in three male Western lowland gorillas (Gorilla gorilla gorilla) at the Detroit Zoo. In addition to their maintenance diet and enrichment foods, the gorillas generally received forage material four times a week. From this baseline, we systematically manipulated how much forage material the group received on a weekly basis, with either daily or bi (twice)‐weekly presentation of browse (mulberry, Morus sp.) or alfalfa hay. We collected behavioral data (60 hr per gorilla) and measured fecal glucocorticoid metabolites (FGM). Mixed models indicated that the presence of forage material significantly increased time feeding (F_2,351 = 9.58, p < 0.001), and decreased rates of noncontact aggression (F_2,351 = 3.69, p = 0.03), and regurgitation and reingestion (F_2,353 = 4.70, p = 0.01). Regurgitation and reingestion were never observed during the condition when forage material was provided daily. When forage material was provided, time spent feeding was similar across gorillas, compared to a disproportionately greater amount of time spent feeding by the dominant individual when forage material was absent. Providing forage material in addition to the regular diet likely created more opportunities for equitable feeding for the subordinate gorillas. FGM concentrations did not vary based on the presence or type of forage material available and, instead, likely reflected group social dynamics. In general, alfalfa and mulberry had similar impacts on behavior, indicating that alfalfa can be an adequate behavioral substitute during times when browse is less readily available for gorillas housed in seasonally variable climates.     

The Influence of Transect Use by Local People and Reuse of Transects for Repeated Surveys on Nesting in Western Lowland Gorillas (Gorilla gorilla gorilla) and Central Chimpanzees (Pan troglodytes troglodytes) in Southeast Cameroon

Monitoring populations of endangered species over time is necessary to guide and evaluate conservation efforts. This is particularly important for nonprotected areas that ensure connectivity between protected populations but are prone to uncontrolled hunting pressure. We investigated whether use of transects by local people and transect reuse for repeated surveys influence great ape nesting and bias results. We conducted simultaneous marked nest count surveys over 12 mo on established and newly opened transects in a nonprotected area subject to traditional heavy use by local people and recorded forest composition and signs of human activity. Chimpanzee and gorilla density estimates and encounter rates per kilometer were lower on established transects than on new ones. A generalized linear model indicated that hunting activity, distance to a regularly used forest trail, and transect type (old or new) predicted chimpanzee nest abundance, and distance to the trail and transect type predicted gorilla nest abundance, with no effect of habitat type (percentage suitable habitat) for either species. We, therefore, suggest that the difference in great ape nesting is a result of high levels of hunting by local people on established transects and forest trails. Our results support the use of repeated line transect surveys for monitoring great ape populations in many circumstances, although we advocate taking precautions in nonprotected areas, to avoid the bias imposed by use of established transects for hunting.     

Assessing Stress in Zoo-Housed Western Lowland Gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>) Using Allostatic Load

Stress contributes to the development of chronic degenerative diseases in primates. Allostatic load is an estimate of stress-induced physiological dysregulation based on an index of multiple biomarkers. It has been applied to humans to measure effects of stress and predict health outcomes. Assessing allostatic load in nonhuman primates may aid in understanding factors promoting compromised health and longevity in captive populations, as well as risk assessment among wild populations following human activities. We applied an allostatic load index to gorillas housed at the Columbus Zoo and Aquarium (N = 27, 1956–2014) using data from medical records and biomarkers from banked serum. We estimated allostatic load using seven biomarkers (albumin, cortisol, corticotropin-releasing hormone, dehydroepiandrosterone sulfate, glucose, interleukin-6, and tumor necrosis factor alpha) and then examined this index for associations with age, sex, number of stressful events, parturition, physiological health measures, and age at death. Stressful events were defined as agonistic interactions with wounding, translocations, and anesthetizations. Allostatic load positively associated with age and total number of lifetime stressful events. Allostatic load was significantly higher in females than in males. Allostatic load was not associated with number of pregnancies and was not different between nulliparous and parous females. Allostatic load associated positively with serum creatinine and triglyceride levels, showed a nonsignificant negative association with cholesterol, and did not associate significantly with age at death. These results demonstrate the potential utility of allostatic load for exploring long-term stress and health risks, as well as for evaluating environmental stressors for gorillas and other nonhuman primates in captivity and in the wild.