Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla)

Life-history traits and ecological conditions have an important influence on primate social systems. Most of what we know about the life-history patterns and social structure of gorillas comes from studies of eastern gorillas (Gorilla beringei sp.), which live under dramatically different ecological conditions compared to western gorillas (Gorilla gorilla sp.). In this paper we present new data on western gorilla social structure and life histories from four study sites, and make comparisons with eastern gorilla populations. Data were obtained from two study sites with gorilla groups undergoing the habituation process (Lossi, Democratic Republic of Congo and Bai Hokou, Central African Republic) and two "bai" studies (Maya Nord and Mbeli Bai, Republic of Congo). The size and structure of these groups were similar to those seen in eastern gorillas. However, differences in the occurrence of various group transitions (group formations, changes between one-male and multimale composition, and group disintegrations) exist, and western gorillas notably exhibit much higher rates of male emigration and correspondingly fewer multimale groups compared to mountain gorillas. Certain phenomena have been observed only rarely, including predation by leopards. The preliminary data show no significant differences in birth rates between western gorillas and mountain gorillas. The ecological variability across gorilla habitats likely explains the flexibility in the social system of gorillas, but we need more information on the social relationships and ecology of western gorillas to elucidate the causes for the similarities and differences between western and eastern gorillas on the levels of individuals, social groups, and population dynamics.     

Western gorilla diet: a synthesis from six sites

The objective of this paper is to collate information on western gorilla diet from six study sites throughout much of their current range, including preliminary information from two sites (Afi and Lossi), where studies of diet have begun only recently. Food lists were available from each site, derived from indirect signs of gorilla feeding (such as feces), with some observational data. Important staple, seasonal, and fallback foods have been identified, and a number of striking similarities across sites have been revealed based on a much larger data set than was previously available. It was confirmed that the western gorilla diet is always eclectic, including up to 230 items and 180 species. The greatest diversity is found among the fruit species eaten, fruit being included in western gorilla diets from all sites and throughout most or all of the year. Eight plant families provide important foods at five, or all six, sites, suggesting that it may be possible in the future to predict which habitats are the most suitable for gorillas. Gorillas exploit both rare and common forest species. Similarities and differences among sites can be explained superficially on the basis of geography and the past history of the forest. Gorilla density across sites appears to be most affected by the density of monocotyledonous bulk food plants, but its relationship to the density of important tree food species has yet to be tested.     

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.     

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.     

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.     

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.     

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.     

Physical maturation,life‐history classes and age estimates of free‐ranging western gorillas—insights from Mbeli Bai,Republic of Congo

Physical maturation and life‐history parameters are seen as evolutionary adaptations to different ecological and social conditions. Comparison of life‐history patterns of closely related species living in diverse environments helps to evaluate the validity of these assumptions but empirical data are lacking. The two gorilla species exhibit substantial differences in their environment, which allows investigation into the role of increased frugivory in shaping western gorilla life histories. We present behavioral and morphological data on western gorilla physical maturation and life‐history parameters from a 12.5‐year study at Mbeli Bai, a forest clearing in the Nouabalé‐Ndoki National Park in northern Congo. We assign photographs of known individuals to different life‐history classes and propose new age boundaries for life‐history classes in western gorillas, which can be used and tested at other western gorilla research sites. Our results show that western gorillas are weaned at a later age compared with mountain gorillas and indicate slower physical maturation of immatures. These findings support the risk‐aversion hypothesis for more frugivorous species. However, our methods need to be applied and tested with other gorilla populations. The slow life histories of western gorillas could have major consequences for social structure, mortality patterns and population growth rates that will affect recovery from population crashes of this critically endangered species. We emphasize that long‐term studies can provide crucial demographic and life‐history data that improve our understanding of life‐history evolution and adaptation and help to refine conservation strategies. Am. J. Primatol. 71:106–119, 2009. © 2008 Wiley‐Liss, Inc.     

Sexual behavior and hormonal estrus cycles in captive aged lowland gorillas (Gorilla gorilla)

To evaluate whether observed cycles in proceptive behavior in aging lowland gorilla females (age 40+) at Brookfield Zoo were driven by ovarian activity, we compared monthly behavioral data to estradiol and progestogen cycles based on fecal hormone assessments. Progestogen peaks showed regularity and close coincidence with monthly sexual behaviors. Estradiol was more variable. Progestogen peaks varied between 22+/-5 days for the control female (29 years old), to 24+/-2.5 and 29+/-8 for the two aged subjects. In the first aged female, which was housed with other females and a silverback, the high degree of cyclicity in sexual behavior, regularity of progestogen cycles, and close concordance between hormonal cycling and sexual behavior strongly compared to patterns found (in this and other studies) in gorilla females <35 years old. Cyclical progestogen peaks were longer and more variable in the second aged female-perhaps because she lacked the social mediation of other females or a male. For husbandry reasons she is not housed with the gorilla group, behavioral data were not collected from her. The value of our longitudinal study is in obtaining reproductive profiles of primate females that are approaching maximum lifespan. This pilot study is part of a larger research project on reproductive senescence that will include other captive females >35 years old, a population that is rapidly increasing in North American zoos as gorillas continue to age.     

Genetic identification of elusive animals: re-evaluating tracking and nesting data for wild western gorillas

Western gorillas Gorilla gorilla have been exceedingly difficult to habituate to the presence of human observers. Nevertheless, researchers have amassed a wealth of information on population densities and group structure for this ape species by locating and counting the sleeping nests of wild individuals. Such nest-count studies have suggested that western gorilla groups often have multiple silverbacks and these multimale groups occasionally divide into smaller subgroups. However, observational data from forest clearing sites and from a few recently habituated western gorilla groups show no evidence of multimale family groups or of subgrouping. This discrepancy underscores a long-standing question in ape research: How accurately do nesting sites reflect true group compositions? We evaluated these indirect measures of group composition by using DNA from faeces and hair to genetically identify individual gorillas at nesting sites. Samples were collected from unhabituated wild western gorillas ranging near Mondika Research Center in the Central African Republic and Republic of Congo. DNA extracted from these samples was genotyped at up to 10 microsatellite loci and one X–Y homologous locus for sex identification. Individuals were then identified at nesting sites by their unique multilocus genotypes, thus providing a 'molecular census' of individual gorillas. Results confirm that western gorillas often build more than one nest at a nesting site and, thus, nest counts can be highly inaccurate indicators of group size and composition. Indeed, we found that nest counts can overestimate group size by as much as 40%, indicating that true gorilla population numbers are probably lower than those reported from census surveys. This study demonstrates how genetic analysis can be a valuable tool for studying and conserving elusive, endangered animals.     

A preliminary behavioral comparison of two captive all-male gorilla groups

Gorillas live in polygamous harem groups, generally composed of one male, several adult females, and their offspring. With an equal numbers of male and female gorillas born in captivity, however, housing gorillas in social breeding units inevitably means that some males will not have access to female social partners. Thus, the future of the captive gorilla population depends on the collective ability of zoos to house equal numbers of males and females. This study examined the behavioral profiles of two all-male groups of captive lowland gorillas (Gorilla gorilla gorilla) to provide information on this type of housing situation. One group consisted of three subadult individuals, while the other consisted of two subadults and a silverback. Data were collected during two 6-month intervals, for a total of 284 hr. The behavioral profiles of the animals were stable over the course of the study but proximity patterns changed. Differences in feeding, solitary play, and object-directed behavior were found between groups, while no significant differences were observed in affiliative or agonistic social behavior. At both institutions, group cohesion appeared to be high, particularly between subadults; these individuals spent approximately 10% of their time engaging in social behavior and 25-50% of their time in close proximity (within 5 m). However, the Zoo Atlanta males spent significantly more time within 1 m and 5 m of each other than the Santa Barbara males, which may reflect a higher level of cohesiveness among members of the Zoo Atlanta group. The behavioral profiles of the animals in this study were similar to those found in bachelor groups of wild mountain gorillas. One notable exception was the absence of homosexual behavior between the silverback and subadults in Santa Barbara and the low frequency of this behavior between subadults in both groups. Although more longitudinal data are needed, these data suggest that all-male groups can be a feasible housing strategy for males at certain periods of their life span. Zoo Biol 20:27-40, 2001. Copyright 2001 Wiley-Liss, Inc.     

Ecological Constraints on the Foraging Effort of Western Gorillas (Gorilla gorilla gorilla) at Bai Hoköu, Central African Republic

Recent studies demonstrate that western lowland gorillas incorporate much more fruit into their diet than Virunga mountain gorillas do. Very little is known, however, about how the frugivorous behavior of western gorillas influences their daily ranging behavior, which may ultimately affect social factors such as group size and structure. I examined the influence of diet and the spatiotemporal availability of plant foods on the foraging effort of nonhabituated western lowland gorilla groups during 17 months at Bai Hoköu in the Dzanga-Ndoki National Park, Central African Republic. I determined diet from indirect methods and gorilla plant food availability and spatial distribution from phenology and line transects. Daily path length gives an estimate of foraging effort and was the distance paced, following fresh gorilla trails, from morning to evening nest sites. The availability and distribution of fruit and its consumption by gorillas varied seasonally. When concentrating on fruits, gorillas traveled significantly farther (mean = 3.1 km/day) than when their diet consisted mostly of nonfruit vegetation, such as leaves and woody pith, stems, and bark (mean = 2.1 km/day). The amount of herbaceous vegetation in the diet did not vary seasonally and did not influence daily path length. The best environmental predictor of foraging effort was fruit density, or a measure combining both density and spatial pattern: coefficient of dispersion. In addition, when fruit patches were small, path length tended to increase but not significantly. Compared with results of other studies, gorillas at Bai Hoköu travel farther (mean = 2.6 km/day) than gorillas in Gabon (mean = 1.7 km/day) and five times farther than mountain gorillas in the Virungas (mean = 0.5 km/day). Increased foraging effort of gorillas in this region, especially during the fruiting season, may have profound effects on group size and structure.     

Non‐invasive fecal hormone analysis and behavioral observations for monitoring stress responses in captive western lowland gorillas (Gorilla gorilla gorilla)

Non‐invasive techniques for monitoring the stress response in captive western lowland gorillas (Gorilla gorilla gorilla) were investigated. Fecal samples for cortisol measurement and concurrent behavioral data were collected from six individuals in a socially housed gorilla group (one adult male, three adult females and their three offspring) over a 7‐month period. Despite inter‐individual variation in the dynamics of fecal cortisol concentrations over time, several major secretory peaks coincided across individuals. High cortisol concentrations in feces were correlated with induced stressors or behavioral observations indicating high social tension, with a 1–2 day lag period. Entry progression order of the gorillas into a den complex and a supplant‐based dominance index were suitable indicators of overall dominance hierarchies, and fluctuations over time reflected periods of instability. Diurnal variation in fecal cortisol was not apparent when comparing afternoon and morning samples, however the sample collection interval was relatively short (3–5 hr). These results demonstrate the feasibility of monitoring stress responses based on the dynamics of both fecal cortisol excretion and behavior. This non‐invasive approach may be used for gauging responses to changes in husbandry, environment and group structure of captive gorillas. Zoo Biol 0:1–15, 2005. © 2005 Wiley‐Liss, Inc.     

Wild Western Lowland Gorillas Signal Selectively Using Odor

Mammals communicate socially through visual, auditory and chemical signals. The chemical sense is the oldest sense and is shared by all organisms including bacteria. Despite mounting evidence for social chemo-signaling in humans, the extent to which it modulates behavior is debated and can benefit from comparative models of closely related hominoids. The use of odor cues in wild ape social communication has been only rarely explored. Apart from one study on wild chimpanzee sniffing, our understanding is limited to anecdotes. We present the first study of wild gorilla chemo-communication and the first analysis of olfactory signaling in relation to arousal levels and odor strength in wild apes. If gorilla scent is used as a signaling mechanism instead of only a sign of arousal or stress, odor emission should be context specific and capable of variation as a function of the relationships between the emitter and perceiver(s). Measured through a human pungency scale, we determined the factors that predicted extreme levels of silverback odor for one wild western lowland gorilla (Gorilla gorilla gorilla) group silverback. Extreme silverback odor was predicted by the presence and intensity of inter-unit interactions, silverback anger, distress and long-calling auditory rates, and the absence of close proximity between the silverback and mother of the youngest infant. Odor strength also varied according to the focal silverback''s strategic responses during high intensity inter-unit interactions. Silverbacks appear to use odor as a modifiable form of communication; where odor acts as a highly flexible, context dependent signaling mechanism to group members and extra-group units. The importance of olfaction to ape social communication may be especially pertinent in Central African forests where limited visibility may necessitate increased reliance on other senses.     

Gorilla Behavior Index revisited: Age,housing and behavior

While personality and temperament assessments are becoming more common in animal science as a means for predicting behavior patterns, they are virtually unstudied in exotic animals outside of chimpanzees. We assessed behavioral profiles of 119 male gorillas using the Gorilla Behavior Index (GBI) and paired this assessment with behavior data on 25 male gorillas from our ongoing analysis of multi-male gorilla groups in North America. This comparison was made to determine if the GBI could be predictive of behavior patterns, with the hope that this could eventually be utilized to aid in the management of multi-male gorilla groups. With few exceptions, GBI factor scores were not related to age of subjects or their current housing condition. Individuals scoring high on the Extroverted factor were more likely to initiate and receive affiliative behaviors, but they were also more likely to initiate contact aggression. Those gorillas who scored high on the Dominant factor were more likely to initiate displacements and less likely to receive them. Gorillas rated as more Fearful were less likely to initiate displacements and those rated as less Understanding were more likely to initiate non-contact aggression. Two facts are evident from these data: (1) further work needs to be done to verify that the GBI is indeed assessing traits and not current behavioral states and (2) any relationships with behavior frequency are relatively weak. In addition to further exploration of the GBI we recommend other assessments to compliment the GBI to establish stronger links between subjective assessments and objective behavior patterns. If established, these short-term assessments may be combined with other historical information on these animals, such as age, rearing history, the number of animals in the group, and the design of the exhibit, to aid in forming and maintaining multi-male gorilla groups in captivity.     

Insectivory by Gorilla gorilla gorilla in Southeast Cameroon

Our study extends quantitative analyses of insect-eating by gorillas (Gorilla gorilla gorilla) to Cameroon. During a 2-mo period (May–June 2001), we recorded and analyzed feeding traces on plants and insects and in gorilla feces. We found 180 feeding traces, 17% of which involved insectivory. Seventy-eight percent of the fecal samples (n = 36) contained insects. Ants were found in 61% of the samples, termites in 39%, while 56% of the samples contained remains of other insects. We added 14 new species to the known insect diet of western lowland gorillas. Overall, social insects are predominant. The choice of prey by the Ntonga gorillas gives new clues for the existence of cross-cultural differences among gorilla populations. A comparison of the overall frequency of insectivory with those at other sites in Central Africa indicate a possible effect of forest disturbance on the insectivorous behavior of gorillas. The study suggests the existence of temporal variation in ant- and termite-eating by gorillas.     

Ranging Patterns of a Western Gorilla Group During Habituation to Humans in the Dzanga-Ndoki National Park,Central African Republic

The ranging patterns of western gorillas have been described in relation to their more frugivorous diet as compared to mountain gorillas. However, the lack of data from habituated groups prevents a full understanding of their ranging behavior and its implications for western gorilla social behavior. Unhabituated gorillas often flee from approaching researchers, possibly resulting in longer daily ranges and home range expansions and/or shifts. I report on the influence of habituation on the ranging patterns of a western gorilla group. I analyzed progress in habituation through changes in gorilla reactions, displayed upon detecting the observers. I measured daily path length and home range while following the group's trails and monitored diet via fecal analyses and direct observations. During the study period, habituation progressed and the gorillas increasingly ignored the arrival of observers. As a result, daily path lengths were longer during the early stages of habituation, when the gorillas were avoiding observers. There was no range expansion or shift, though the measure is more difficult to investigate, being subject to error due to variation in sample size. We recorded seasonal changes in the consumption of fruit by gorillas, but no direct effect on ranging patterns is detectable with the data available, which is likely a consequence of the combined effect of habituation and seasonality on group movements. The findings are not only important for understanding the extent of human influence while conducting research on wild gorillas but also suggest the need for caution when interpreting results from non-habituated gorillas.     

Noninvasive follow-up of simian immunodeficiency virus infection in wild-living nonhabituated Western lowland gorillas in cameroon

Simian immunodeficiency viruses infecting western lowland gorillas (SIVgor) are closely related to HIV-1 and are most likely the ancestors of HIV-1 groups O and P. At present, limited data are available on genetic diversity, transmission, viral evolution, and pathogenicity of SIVgor in its natural host. Between 2004 and 2011, 961 putative gorilla fecal samples were collected at the Campo Ma'an National Park, Cameroon. Among them, 16% cross-reacted with HIV-1 antibodies, corresponding to at least 34 infected gorillas. Combining host genotyping and field data, we identified four social groups composed of 7 to 15 individuals each, with SIV rates ranging from 13% to 29%. Eleven SIVgor-infected gorillas were sampled multiple times; two most likely seroconverted during the study period, showing that SIVgor continues to spread. Phylogenetic analysis of partial env and pol sequences revealed cocirculation of closely related and divergent strains among gorillas from the same social group, indicating SIVgor transmissions within and between groups. Parental links could be inferred for some gorillas infected with closely related strains, suggesting vertical transmission, but horizontal transmission by sexual or aggressive behavior was also suspected. Intrahost molecular evolution in one gorilla over a 5-year period showed viral adaptations characteristic of escape mutants, i.e., V1V2 loop elongation and an increased number of glycosylation sites. Here we show for the first time the feasibility of noninvasive monitoring of nonhabituated gorillas to study SIVgor infection over time at both the individual and population levels. This approach can also be applied more generally to study other pathogens in wildlife.     

Western lowland gorilla diet and resource availability: new evidence,cross-site comparisons,and reflections on indirect sampling methods

We describe the resource availability and diet of western lowland gorillas (Gorilla gorilla gorilla) from a new study site in the Central African Republic and Republic of Congo based on 3 years of study. The results, based on 715 fecal samples and 617 days of feeding trails, were similar to those reported from three other sites, in spite of differences in herb and fruit availability. Staple foods (consumed year-round) included high-quality herbs (Haumania), swamp herbs (when present), and a minimal diversity of fruit. A variety of fruits (average of 3.5 species per day and 10 per month) were selectively consumed; gorillas ignored some common fruits and incorporated rare fruits to a degree higher than predicted based on availability. During periods of fruit abundance, fruit constituted most of the diet. When succulent fruits were unavailable, gorillas used low-quality herbs (i.e., low-protein), bark, and more fibrous fruits as fallback foods. Fibrous fruit species, such as Duboscia macrocarpa and Klainedoxa gabonensis, were particularly important to gorillas at Mondika and other sites as fallbacks. The densities of these two species are similar across sites for which data are available, in spite of major differences in forest structure, suggesting they may be key species in determining gorilla density. No sex difference in diet was detected. Such little variation in western lowland gorilla diet across sites and between sexes was unexpected and may partly reflect limitations of indirect sampling.