Deception and hiding in captive lowland gorillas (Gorilla gorilla gorilla)

Deception and hiding are described for a group of captive lowland gorillas comprising two adult males, one female, and her infant. The males repeatedly interacted with the infant, and their interest was repeatedly thwarted by the mother. As in other social situations in which one animal controls access to an object desired by another, deceit was used to thwart the other's control. Either one or both males at times concealed their actions toward the infant, inhibited their attention to the infant, created a neutral image to get the infant, or interacted with the infant to tease the mother.     

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla)

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.     

Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla)

The geographical distribution of genetic variation within western lowland gorillas (Gorilla gorilla gorilla) was examined to clarify the population genetic structure and recent evolutionary history of this group. DNA was amplified from shed hair collected from sites across the range of the three traditionally recognized gorilla subspecies: western lowland (G. g. gorilla), eastern lowland (G. g. graueri) and mountain (G. g. beringei) gorillas. Nucleotide sequence variation was examined in the first hypervariable domain of the mitochondrial control region and was much higher in western lowland gorillas than in either of the other two subspecies. In addition to recapitulating the major evolutionary split between eastern and western lowland gorillas, phylogenetic analysis indicates a phylogeographical division within western lowland gorillas, one haplogroup comprising gorilla populations from eastern Nigeria through to southeast Cameroon and a second comprising all other western lowland gorillas. Within this second haplogroup, haplotypes appear to be partitioned geographically into three subgroups: (i) Equatorial Guinea, (ii) Central African Republic, and (iii) Gabon and adjacent Congo. There is also evidence of limited haplotype admixture in northeastern Gabon and southeast Cameroon. The phylogeographical patterns are broadly consistent with those predicted by current Pleistocene refuge hypotheses for the region and suggest that historical events have played an important role in shaping the population structure of this subspecies.     

Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla)

Postconflict (PC) behaviors, including reconciliation and consolation, have been observed in many primate and several nonprimate species. Using the PC-matched control (MC) method, PC behavior was examined in two groups (n=13) of captive western lowland gorillas, a species for which no conflict resolution data have been published. Analyses of 223 conflicts showed significantly more affiliation between former opponents after a conflict when compared to control periods, indicating reconciliation. Results also showed significantly more affiliation between the victim and a third-party after a conflict, indicating consolation. Both solicited and unsolicited consolation were observed. The majority of the affiliative interactions observed for both reconciliation and consolation were social proximity, which suggests that unlike most nonhuman primates, proximity, rather than physical contact, may be the main mechanism for resolving conflicts in western lowland gorillas. PC behavior was not uniform throughout the groups, but rather varied according to dyad type.     

Tree structure and sex differences in arboreality among western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic

The aim of six months of research in 1995 on the gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic, was to study the effects of tree structure, relative numbers of arboreal feeding sites, and sex differences in body size on arboreal foraging. The analysis presented here also documents inter-annual variation in fruit availability and climbing by silverback gorillas by comparing the 1995 results to those from earlier research, 1990–1992. This analysis suggests that female gorillas maintain similar levels of arboreality in fruit-rich and fruit-poor seasons and years, but silverbacks may be more terrestrial when fruit is scarce or difficult to access. Trees of different shapes present different numbers of feeding sites to bigger males and smaller females. Male climbing is affected by the availability of fruit, and small trees with narrow crowns that lend easy access to fruit from the core. This study suggests that the energetics of vertical climbing and biomechanical constraints imposed by small branch feeding sites in the periphery of trees may constrain the arboreal behavior of male gorillas. Fine-tuned comparisons of food availability, tree structure, and variation in social context of behavior across habitats, will assist efforts to understand differences in ecology among populations and species of African apes.     

Food transfers in immature wild western lowland gorillas (Gorilla gorilla gorilla)

The transfer of food items between individuals has been described in primates as serving an informative purpose in addition to supplementing the diet of immature individuals. This behaviour has yet to be described in western lowland gorillas (Gorilla gorilla gorilla), and results are presented here of observations of food transfers in immature gorillas at Mbeli Bai, Republic of Congo. The frequency of food transfers decreased with increasing immature age, while the frequency of independent feeding and processing of food increased. Transfers between mothers and infants were the most frequent, with infants attempting to take items from the mother. These attempts were not always successful and the item was relinquished on less than 50% of attempts. Mothers also took items from their offspring. The results point to the functional significance of food transfers in western lowland gorillas being informational. In a bai environment, where one species forms the majority of a visiting gorilla’s diet despite other species being available, the initiation of food transfers by immatures is proposed to serve the purpose of familiarising them with which species, and which parts of those species, may be eaten.     

Male genetic structure and paternity in western lowland gorillas (Gorilla gorilla gorilla)

The male dispersal patterns of western lowland gorillas (WLGs, Gorilla gorilla gorilla) are not well understood. To determine whether most silverbacks stay close to their relatives, we analyzed autosomal and Y‐chromosomal microsatellites (STRs) in wild WLGs at Moukalaba, Gabon. We obtained STR genotypes for 38 individuals, including eight silverbacks and 12 adult females in an approximately 40 km² area. Among them, 20 individuals were members of one identified group (Group Gentil; GG), including one silverback and six adult females. The silverback sired all 13 of the offspring in GG and no Y‐STR polymorphism within GG was found, as expected in a one‐male group structure. Over all silverbacks sampled, Y‐STR diversity was high considering the limited sampling area, and silverbacks with similar Y‐STR haplotypes were not always located in nearby areas. Although the misclassification rate of kinship estimates in this study was not negligible, there were no kin dyads among all silverbacks sampled. These results suggest that silverbacks born in the same group do not stay close to each other after maturation. The Y‐STR diversity in this study was similar to that of a previous study conducted in an area that was approximately 150 times larger than our study area. Similarity of WLG Y‐STR diversity between studies at different sampling scales suggests that male gene flow may not be geographically limited. These results suggest that WLG males normally disperse from their natal areas after maturation, at least, in Moukalaba. Am J Phys Anthropol 151:583–588, 2013. © 2013 Wiley Periodicals, Inc.     

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.     

Exchange of objects between humans and captive western lowland gorillas

An experiment was carried out to assess the ability of captive western lowland gorillas (Gorilla g. gorilla) to exchange objects with a human partner. Before the exchange itself, individuals had to learn to give an item to the experimenter. Four individuals out of nine performed active giving. After that familiarization with giving behaviour, two kinds of exchanges, of increasing complexity, were tested with gorillas. Simple exchange (give C to obtain D) was the first procedure and six gorillas out of nine succeeded. Double exchange (give B to receive C, then give back C to obtain D) was performed only by three individuals and triple exchange (give A to receive B, give back B to receive C, then give back C to obtain D) was performed only by two individuals. Different types of errors were scored, as well as social constraints on learning. Results showed that (1) naive gorillas are able to get a reward (D) in an experimental exchange situation; and (2) the complex rules of multiple successive exchanges were not easily understood by gorillas.     

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.     

A training program for noninvasive semen collection in captive western lowland gorillas (Gorilla gorilla gorilla)

Staff at Omaha's Henry Doorly Zoo devised a training program for noninvasive semen collection from three male gorillas. Trained behaviors, shaped using food rewards and verbal praise, enabled the trainer to perform a cursory physical examination and collect >270 semen samples during the study period. Ejaculate volume, sperm motility, and progressive forward motion were recorded. Two of the gorillas regularly produced semen samples that were cryopreserved. Frozen semen from one gorilla was successfully used in an assisted reproductive procedure. The training program may be used as a guideline for other institutions to create similar programs. Zoo Biol 17:143–151, 1998. © 1998 Wiley-Liss, Inc.     

Endoparasites of western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic

A coprologic study of free-ranging western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Dzangha-Ndoki National Park, Central African Republic (2 degrees 51'34'N, 16 degrees 28'03'E) was conducted from October 1999 to November 2000. All 75 fecal samples examined were positive for endoparasites, and each contained at least two species. Parasites present included two genera of amoebae, entodiniomorph ciliates, including Prototapirella gorillae, Troglodytella spp., and Gorillophilus thoracatus, a Balantidium-like organism, strongyle/trichostrongyle eggs (including a presumptive Mammomonogamus sp. and several other genera), Strongyloides sp., Probstmayria sp., a spirurid, a trichuroid, and several unidentified trematodes. Flagellates and cestodes were not found. Despite the presence of a variety of parasite genera, in general, levels of parasitism were low. These data provide baseline parasitologic data for this population as part of a comprehensive health-monitoring program. With the advent of ecotourism in this study area, continued monitoring is indicated for insuring the health of both gorillas and humans in the Bai Hokou study area.     

Sexual behavior in female western lowland gorillas (Gorilla gorilla gorilla): evidence for sexual competition

Previous research in gorillas suggests that females engage in post‐conception mating as a form of sexual competition designed to improve their own reproductive success. This study focused on sexual behaviors in a newly formed group of western lowland gorillas (Gorilla gorilla gorilla) housed at Zoo Atlanta. All females engaged in mating outside their conceptive periods, although there was individual variation in the frequency of the behavior. An analysis of the presence/absence of sexual behavior found females, regardless of reproductive condition, were more likely to engage in sexual behavior on days when other females were sexually active. On these “co‐occurrence” days, females were significantly more likely to solicit the silverback, but copulations did not differ from expectation. The results find further evidence for sexual competition among female gorillas and suggest that this may occur throughout their reproductive cycle rather than only during pregnancy. Am. J. Primatol. 71:587–593, 2009. © 2009 Wiley‐Liss, Inc.     

Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla)

Within-group female relationships, and relationships between females and adult males have not been described for wild western lowland gorillas. New data are presented here from Mbeli Bai in the Nouabale-Ndoki National Park, Republic of Congo. Nine groups were observed over a continuous 2-year period, and affiliative and agonistic interactions, as well as time spent by females and adult males in proximity to each other were recorded. Affiliative behavior was extremely rare in the bai, and measures of proximity between individuals were inconclusive because of the small sample sizes. Rates of agonistic interaction among females were highly variable between groups. The majority of agonistic interactions were undecided, and the supplant rate was low. Evidence for an agonistic dominance hierarchy is weak. The data do not support hypotheses that increased frugivory in western lowland gorillas raises levels of within-group contest competition; however, the need for intersite comparisons is stressed. In contrast, rates of agonistic behavior between females and silverback males were higher and more consistent between groups. Agonistic relationships between males and females conformed with patterns seen in mountain gorillas, where male protection from intraspecific aggression is important. The benefit females gain by forming long-term cooperative alliances appears to be small, and is likely outweighed by reproductive advantages associated with male protection.     

Comparison of arthritis characteristics in lowland Gorilla gorilla and mountain Gorilla beringei

Gorilla gorilla and the less-studied G. beringei occupy very different, geographically separate habitats. We studied the occurrence of various forms of arthritis to examine possible nature/nurture causality. The macerated skeletons of 38 G. beringei and 99 G. gorilla individuals were examined macroscopically for the presence of articular and osseous pathologies. Contrasting with only isolated osteoarthritis and infectious arthritis was the frequent occurrence of a form of erosive arthritis associated with joint fusion. Twenty-one percent of the G. beringei and 20% of G. gorilla specimens were afflicted, which are statistically indistinguishable frequencies. While both had prominent axial disease, they differed in patterns of peripheral arthritis. Whereas G. beringei showed a pauciarticular pattern, the pattern in G. gorilla was more often polyarticular. Susceptibility to spondyloarthropathy was apparently genetically imprinted before Gorilla separated into G. gorilla and G. beringei. However, the different patterns of peripheral joint involvement suggest a causality resulting from lifestyle (e.g., the presence/absence or extent of knuckle walking) or a habitat-related infectious agent.     

Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the six months after parturition

Studies of wild mountain gorillas have demonstrated strong preferences among new mothers for the silverback. Protection against infanticide has been theorized to be the primary cause for this attraction. We examined social partner preferences in captive western lowland mothers during the 6 mo after parturition and found that juveniles and females were the primary members of the new mothers' social network. Mothers spent significantly more time in close proximity with both of these subgroups than with the silverback. Proximity patterns changed over time: new mothers spent more time near females in the month after parturition than in the month prior to parturition, and spatial proximity increased again in months 2-6 postparturition. These findings differ from those reported for wild mountain gorillas, which may reflect the lack of infanticide risk in captivity. Given current hypotheses that infanticide may be a limited in western lowland gorillas, the social partner preferences observed here may be indicative of patterns in wild populations.     

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.     

Relationship between behavior, adrenal activity, and environment in zoo-housed western lowland gorillas (Gorilla gorilla gorilla)

Monitoring adrenal activity through noninvasive fecal hormone sampling is rapidly gaining popularity as a tool to assess zoo animal welfare. However, few studies have sought to investigate the interrelationships between behavior, adrenal activity, and environment, and ask whether both behavioral and adrenal monitoring strategies are required to assess welfare sufficiently. We present the findings of a 9-month study of a small group (one male, two females) of Western lowland gorillas, Gorilla gorilla gorilla. First, we examined the effect of environmental variables on gorilla behavior. Second, we examined the effect of environmental variables on the concentration of fecal glucocorticoid metabolites (FGC) and the relationship between behavior and FGC. Environmental variables had similar effects on all three gorillas. Negative vigilance of visitors (NVV; staring, posturing, and charging at visitors) significantly increased in all subjects as environmental noise levels increased, and food-related behavior significantly decreased in all subjects as crowd size increased. Exhibit modifications had a number of positive effects on behavior. Notably, when privacy screens were used, NVV significantly decreased in two subjects. We found no significant effects of environmental variables on FGC. However, we did find significant relationships between behavior and FGC in one female. Specifically, her NVV was significantly higher one day before, and on the same day as, raised FGC. Also, hair plucking significantly increased in the two days following raised FGC. Overall, this study demonstrates how concurrent noninvasive fecal and behavioral monitoring can be used for gorilla welfare assessment.