Intra-specific variation in social organization of gorillas: implications for their social evolution

We analysed intra-specific variation in the social organization of gorillas and ecological and social factors influencing them, based on recent data on diet, day journey length, home range size, group size and proportion of multi-male groups in three subspecies [western lowland gorillas (WLG); eastern lowland gorillas (ELG); mountain gorillas (MG)]. Median group size was similar across subspecies and across habitats, but the extraordinarily large group including >30 gorillas was only found in habitat with dense terrestrial herbaceous vegetation. Within-group competition may determine the upper limit of group size in frugivorous WLGs and ELGs in lowland habitats with scarce undergrowth. A frugivorous diet may be a causal factor of subgrouping in multi-male groups of WLGs and ELGs, while a folivorous diet may prevent subgrouping in multi-male groups of MGs. Social factors, rather than ecological factors, may play an important role in the formation of multi-male groups and their cohesiveness in MGs. High gregariousness of female gorillas and their prolonged association with a protector male are explained by their vulnerability to both infanticide (MGs) and predators (ELGs). Comparison of long-term changes in group composition and individual movements between ELGs in Kahuzi and MGs in the Virungas suggest that the occurrence of infanticide may promote kin-male association within a group. Threat of infanticide may stimulate MG females to transfer into multi-male groups to seek reliable protection and maturing MG males to stay in their natal groups after maturity. By contrast, the absence of infanticide may facilitate ELG females to associate with infants and other females at transfer and ELG males to establish large groups in a short period by taking females from their natal groups, by luring females from neighbouring groups, or by takeover of a widow group after the death of its leading male. These conditions may prevent ELG and WLG maturing males from remaining to reproduce in their natal groups and possibly result in a rare occurrence of multi-male groups in their habitats. Similar reproductive features of MG and ELG females suggest both female strategies have been adaptive in their evolutionary history.     

How fruit abundance affects the chimpanzee party size: a comparison between four study sites

We examined the relationship between fruit abundance and chimpanzee (Pan troglodytes) party size by comparing data from four study sites: the Kalinzu Forest Reserve, Uganda, the Djinji Camp and Guga Camp in the Ndoki Forest, Congo, and Kahuzi-Biega National Park, Democratic Republic of Congo. Although the difference in the fruit abundance between the sites was responsible for the difference in the party size between the sites, the seasonal changes in fruit abundance did not explain the changes in the party size in each study site. Across the four study sites, there were significant correlations of the mean and minimum of monthly party size with the mean of monthly fruiting-tree density, and a significant correlation of the maximum of monthly party sizes with the minimum of monthly fruiting-tree density. We proposed a hypothesis that (1) the monthly fruit abundance affects the monthly party size in the sites where the fruit availability is as low as to limit the party size during a major part of a year, while (2) the party size does not increase with the increase in the monthly fruit abundance, but is affected by other social factors, in the sites where the minimum of monthly fruit abundance is high enough for chimpanzees to form parties of an adequate size. Electronic Publication     

Species and sex identification of western lowland gorillas (Gorilla gorilla gorilla), eastern lowland gorillas (Gorilla beringei graueri) and humans

Methods for the identification of the sex and species of individuals from samples non-invasively taken from humans and gorillas were established. Amplification of a segment of amelogenin (AMG), which is an X–Y homologous gene, using two pairs of primers from human AMG, revealed both X- and Y-specific bands. The possibility of sex identification was examined by typing the AMG gene using hair and fecal samples from captive western lowland gorillas (Gorilla gorilla gorilla) in Japan and hair samples from wild eastern lowland gorillas (Gorilla beringei graueri) in the Kahuzi-Biega National Park, Democratic Republic of Congo, which were sexed by direct observation. Species-specific bands of AMG in gorillas and humans were identified by restriction fragment length polymorphisms analysis. These tests could be used for sexing unidentified individuals of wild western and eastern lowland gorillas, and screening contamination of human DNA from non-invasively acquired samples.     

Predation on mammals by chimpanzees in the montane forest of Kahuzi, Zaire

The rate of predation on mammals by chimpanzees was determined from carcasses and from fecal specimens found on fresh trails during a 16-month period in the montane forest of Kahuzi-Biega National Park, Zaire. A unit-group of semi-habituated chimpanzees, composed of 22 – 23 individuals including 8 adult or adolescent males, appeared to kill about 18 – 30 mammalian prey (16 – 28Cercopithecus monkeys) per year, if the multiple kills by chimpanzees were not considered. A juvenile l'Hoest's monkey was recorded for the first time as the prey of chimpanzees in this study. Predation occurred in the late dry and the early rainy seasons, when the diversity of ripe fruits was the highest during the year. The Kahuzi chimpanzees tended to kill mammals less frequently but to killCercopithecus monkeys more frequently than chimpanzees in other habitats. The absence of red colobus monkeys, which are the most frequent prey in Gombe, Mahale, and Tai, might be responsible for the low predation rate. However, the estimated rate of predation onCercopithecus monkeys is the highest record among various chimpanzee habitats. At least 11 – 18% of theCercopithecus population seemed to be lost annually as a result of being killed by chimpanzees. Chimpanzees may be the most important predators on these monkeys in the absence of leopards at Kahuzi. The examination of fecal samples and carcasses suggested that adult (probably male) or adolescent chimpanzees tended to eat juvenile or subadult monkeys most frequently, as is also seen for chimpanzees in Gombe, Mahale, and Tai.     

Extreme conservation leads to recovery of the Virunga mountain gorillas

As wildlife populations are declining, conservationists are under increasing pressure to measure the effectiveness of different management strategies. Conventional conservation measures such as law enforcement and community development projects are typically designed to minimize negative human influences upon a species and its ecosystem. In contrast, we define "extreme" conservation as efforts targeted to deliberately increase positive human influences, including veterinary care and close monitoring of individual animals. Here we compare the impact of both conservation approaches upon the population growth rate of the critically endangered Virunga mountain gorillas (Gorilla beringei beringei), which increased by 50% since their nadir in 1981, from approximately 250 to nearly 400 gorillas. Using demographic data from 1967-2008, we show an annual decline of 0.7%±0.059% for unhabituated gorillas that received intensive levels of conventional conservation approaches, versus an increase 4.1%±0.088% for habituated gorillas that also received extreme conservation measures. Each group of habituated gorillas is now continuously guarded by a separate team of field staff during daylight hours and receives veterinary treatment for snares, respiratory disease, and other life-threatening conditions. These results suggest that conventional conservation efforts prevented a severe decline of the overall population, but additional extreme measures were needed to achieve positive growth. Demographic stochasticity and socioecological factors had minimal impact on variability in the growth rates. Veterinary interventions could account for up to 40% of the difference in growth rates between habituated versus unhabituated gorillas, with the remaining difference likely arising from greater protection against poachers. Thus, by increasing protection and facilitating veterinary treatment, the daily monitoring of each habituated group contributed to most of the difference in growth rates. Our results argue for wider consideration of extreme measures and offer a startling view of the enormous resources that may be needed to conserve some endangered species.     

Factors Affecting Nesting Site Choice in Chimpanzees at Tshibati,Kahuzi-Biega National Park: Influence of Sympatric Gorillas

We recorded 310 fresh chimpanzee night nests at 72 nest sites to determine their choice of tree and site for nesting vis-à-vis the effects of sympatric gorillas. Chimpanzees did not use trees for nesting according to their abundance, but instead tended to nest in fruit trees that they used as food sources. Nesting patterns of chimpanzees may vary with nesting group size, the type of vegetation, and fruit species eaten or not eaten by gorillas. When chimpanzees lodged as a small group in the secondary forest, they nested more frequently in trees bearing ripe fruits eaten only by themselves than in those with fruit eaten also by gorillas. When they lodged as a large group in the primary forest, they nested more frequently in trees bearing ripe fruits eaten by both apes. Nest group size is positively correlated with the availability of preferred ripe fruits in secondary forest. These findings not only reflect the larger foraging groups at the larger fruiting trees but also suggest that chimpanzees may have tended to occupy fruiting trees effectively by nesting in them and by forming large nest groups when the fruits attracted gorillas. Competition over fruits between gorillas and chimpanzees, due to their low productivity in the montane forest of Kahuzi, may have promoted the chimpanzee tactics.     

Impact of Male Infanticide on the Social Structure of Mountain Gorillas

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.     

Infanticide and social flexibility in the genus <Emphasis Type="Italic">Gorilla</Emphasis>

Based on the cases of infanticide by male mountain gorillas reported from the Virunga volcanic region, the socioecological and life history features of gorillas satisfy the conditions for which infanticide may be expected. However, there are considerable variations in the occurrence of infanticide between habitats. We analyze the recent reports of infanticides that were directly observed or are suspected based on field evidence in two populations of eastern and western lowland gorillas (Kahuzi and Mbeli Bai, respectively) along with previous reports on mountain gorillas, and consider which social features are linked with and which factors influence the occurrence of infanticide in the gorilla populations. All victims were suckling infants and most of them were killed by males who seemed unrelated to them. Dependent infants are most vulnerable to infanticide when the protector male (its putative father in most cases) is absent, and so male protection ability seems to be important in determining female transfer decisions. Two cases observed in Kahuzi suggest that the infanticidal male may discriminate between infants to accept and those to kill according to his previous interactions with their mothers. Mating for a prolonged period prior to parturition is necessary for immigrant females to avoid infanticide by the new male of the group that they join. Infanticide was usually associated with female transfer, and the patterns of female association at transfer may shape variations in social structure between populations. Female mountain gorillas prefer large groups with multiple males and tend to transfer alone in order to seek more protection against infanticide in Virunga. By contrast, female eastern and western lowland gorillas tend to transfer with other females to small groups or solitary males, and maturing silverbacks take females to establish new groups through group fission in Kahuzi and Mbeli Bai. These differences may result in more multi-male and larger groups in the Virungas than in Kahuzi and Mbeli Bai. Rapid changes in density of gorilla social units and their relations following drastic environmental changes caused by recent human disturbances may also increase the probability of infanticide.     

Diet and seasonal changes in sympatric gorillas and chimpanzees at Kahuzi–Biega National Park

Based on 8 years of observations of a group of western lowland gorillas (Gorilla beringei graueri) and a unit-group of chimpanzees (Pan troglodytes schweinfurthii) living sympatrically in the montane forest at Kahuzi–Biega National Park, we compared their diet and analyzed dietary overlap between them in relation to fruit phenology. Data on fruit consumption were collected mainly from fecal samples, and phenology of preferred ape fruits was estimated by monitoring. Totals of 231 plant foods (116 species) and 137 plant foods (104 species) were recorded for gorillas and chimpanzees, respectively. Among these, 38% of gorilla foods and 64% of chimpanzee foods were eaten by both apes. Fruits accounted for the largest overlap between them (77% for gorillas and 59% for chimpanzees). Gorillas consumed more species of vegetative foods (especially bark) exclusively whereas chimpanzees consumed more species of fruits and animal foods exclusively. Although the number of fruit species available in the montane forest of Kahuzi is much lower than that in lowland forest, the number of fruit species per chimpanzee fecal sample (average 2.7 species) was similar to that for chimpanzees in the lowland habitats. By contrast, the number of fruit species per gorilla fecal sample (average 0.8 species) was much lower than that for gorillas in the lowland habitats. Fruit consumption by both apes tended to increase during the dry season when ripe fruits were more abundant in their habitat. However, the number of fruit species consumed by chimpanzees did not change according to ripe fruit abundance. The species differences in fruit consumption may be attributed to the wide ranging of gorillas and repeated usage of a small range by chimpanzees and/or to avoidance of inter-specific contact by chimpanzees. The different staple foods (leaves and bark for gorillas and fig fruits for chimpanzees) characterize the dietary divergence between them in the montane forest of Kahuzi, where fruit is usually scarce. Gorillas rarely fed on insects, but chimpanzees occasionally fed on bees with honey, which possibly compensate for fruit scarcity. A comparison of dietary overlap between gorillas and chimpanzees across habitats suggests that sympatry may not influence dietary overlap in fruit consumed but may stimulate behavioral divergence to reduce feeding competition between them.     

Fallback foods and dietary partitioning among Pan and gorilla

Recent findings on the strong preference of gorillas for fruits and the large dietary overlap between sympatric gorillas and chimpanzees has led to a debate over the folivorous/frugivorous dichotomy and resource partitioning. To add insight to these arguments, we analyze the diets of sympatric gorillas and chimpanzees inhabiting the montane forest of Kahuzi-Biega National Park (DRC) using a new definition of fallback foods (Marshall and Wrangham: Int J Primatol 28 [2007] 1219–1235). We determined the preferred fruits of Kahuzi chimpanzees and gorillas from direct feeding observations and fecal analyses conducted over an 8-year period. Although there was extensive overlap in the preferred fruits of these two species, gorillas tended to consume fewer fruits with prolonged availability while chimpanzees consumed fruits with large seasonal fluctuations. Fig fruit was defined as a preferred food of chimpanzees, although it may also play a role as the staple fallback food. Animal foods, such as honey bees and ants, appear to constitute filler fallback foods of chimpanzees. Tool use allows chimpanzees to obtain such high-quality fallback foods during periods of fruit scarcity. Among filler fallback foods, terrestrial herbs may enable chimpanzees to live in small home ranges in the montane forest, whereas the availability of animal foods may permit them to expand their home range in arid areas. Staple fallback foods including barks enable gorillas to form cohesive groups with similar home range across habitats irrespective of fruit abundance. These differences in fallback strategies seem to have shaped different social features between sympatric gorillas and chimpanzees. Am J Phys Anthropol 140:739–750, 2009. © 2009 Wiley-Liss, Inc.