Inter-group relationships influence territorial defence in mountain gorillas.

Many species show territoriality, in which territory owners have exclusive or priority use of a region. In humans, tolerance of others within our space also depends greatly on our social relationships with them. This has been hypothesized as one potential driver of the evolution of long-term, inter-group relationships, through enabling shared access of resources and easing disputes over space. However, extremely little is known about the importance of social relationships between neighbouring groups in non-humans for how space is used and shared. Using 16 years of data on the simultaneous movement and interaction patterns of 17 mountain gorilla groups, we investigated how the occurrence of aggressive and affiliative behaviour during inter-group encounters was influenced by both their social and spatial context. We found evidence of territorial defence, with rates of aggression increasing towards the centre of home ranges. Groups which had previously split from each other showed higher levels of affiliation during encounters with each other and experienced lower levels of aggression when within the other's peripheral home range. However, encounters within core areas of the home range consistently elicited higher aggression, regardless of the groups' history. Our findings indicate that not only are the social relationships between groups retained after they split from one another but also that these relationships enable groups to access certain areas with a reduced risk of aggression. This suggests that reduced aggression when accessing areas within neighbours' home ranges may be an advantage for the maintenance of inter-group relationships and a potential driver in the evolution of long-term, post-dispersal relationships and complex multi-level societies.

Incisor tooth wear and age determination in mountain gorillas from Volcanoes National Park, Rwanda.

OBJECTIVES: Ecological factors, but also tooth-to-tooth contact over time, have a dramatic effect on tooth wear in primates. The aim of this study is to test whether incisor tooth wear changes predictably with age and can thus be used as an age estimation method in a wild population of mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. MATERIALS AND METHODS: In mountain gorillas of confidently known chronological age (N = 24), we measured the crown height of all permanent maxillary and mandibular incisors (I1 , I1 , I2 , I2 ) as a proxy for incisal macrowear. Linear and quadratic regressions for each incisor were used to test whether age can be predicted by crown height. Using these models, we then predicted age at death of two individual mountain gorillas of probable identifications, based on their incisor crown height. RESULTS: Age decreased significantly with incisor height for all teeth, but the upper first incisors (I1 ) provided the best results, with the lowest Akaike's Information Criterion corrected for small sample size (AICc) and lowest Standard Error of the Estimate (SEE). When the best age equations for each sex were applied to gorillas with probable identifications, the predicted ages differed 1.58 and 3.33 years from the probable ages of these individuals. CONCLUSIONS: Our findings corroborate that incisor crown height, a proxy for incisal wear, varies predictably with age. This relationship can be used to estimate age at death of unknown gorillas in the skeletal collection, and in some cases, to corroborate the identity of individual gorillas recovered from the forest postmortem at an advanced state of decomposition. Such identifications help fill gaps in the demographic database and support research that requires individual-level data.

Tooth wear and feeding ecology in mountain gorillas from Volcanoes National Park, Rwanda.

OBJECTIVES: Ecological factors have a dramatic effect on tooth wear in primates, although it remains unclear how individual age contributes to functional crown morphology. The aim of this study is to determine how age and individual diet are related to tooth wear in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. MATERIAL AND METHODS: We calculated the percent of dentine exposure (PDE) for all permanent molars (M1-M3) of known-age mountain gorillas (N = 23), to test whether PDE varied with age using regression analysis. For each molar position, we also performed stepwise multiple linear regression to test the effects of age and percentage of time spent feeding on different food categories on PDE, for individuals subject to long-term observational studies by the Dian Fossey Gorilla Fund International's Karisoke Research Center. RESULTS: PDE increased significantly with age for both sexes in all molars. Moreover, a significant effect of gritty plant root consumption on PDE was found among individuals. Our results support prior reports indicating reduced tooth wear in mountain gorillas compared to western gorillas, and compared to other known-aged samples of primate taxa from forest and savanna habitats. DISCUSSION: Our findings corroborate that mountain gorillas present very low molar wear, and support the hypothesis that age and the consumption of particular food types, namely roots, are significant determinants of tooth wear variation in mountain gorillas. Future research should characterize the mineral composition of the soil in the Virunga habitat, to test the hypothesis that the physical and abrasive properties of gritty foods such as roots influence intra- and interspecific patterns of tooth wear.

Mountain gorilla ranging patterns: influence of group size and group dynamics.

Since the 1980s, the Virunga mountain gorilla population has almost doubled, now reaching 480 individuals living in a 430-km(2) protected area. Analysis of the gorillas' ranging patterns can provide critical information on the extent and possible effects of competition for food and space. We analyzed 12 years of daily ranging data and inter-group encounter data collected on 11 gorilla groups monitored by the Karisoke Research Center in Rwanda. During that period, the study population increased in size by almost 50% and the number of groups tripled. Groups had small yearly home ranges compared to other known gorilla populations, with an average 90% kernel density estimate of 8.07 km2 and large between-group variations (3.17-23.59 km2). Most groups had consistent home range location over the course of the study but for some, we observed gradual range shifts of up to 4 km. Neighboring groups displayed high home range overlap, which increased dramatically after the formation of new groups. On average, each group used only 28.6% of its 90% kernel home range exclusively, and in some areas up to six different groups had overlapping home ranges with little or no exclusive areas. We found a significant intra-group positive relationship between the number of weaned individuals in a group and the home range size, but the fitted models only explained 17.5% and 13.7% of the variance in 50% and 90% kernel home range size estimates, respectively. This suggests that despite the increase in size, the study population is not yet experiencing marked effects of feeding competition. However, the increase in home range overlap resulting from the formation of new groups led to a sixfold increase in the frequency of inter-group encounters, which exposes the population to elevated risks of fight-related injuries and infanticide.

Comparative life history patterns of female gorillas.

OBJECTIVES: Several theories have been proposed to explain the impact of ecological conditions on differences in life history variables within and between species. Here we compare female life history parameters of one western lowland gorilla population (Gorilla gorilla gorilla) and two mountain gorilla populations (Gorilla beringei beringei). MATERIALS AND METHODS: We compared the age of natal dispersal, age of first birth, interbirth interval, and birth rates using long-term demographic datasets from Mbeli Bai (western gorillas), Bwindi Impenetrable National Park and the Virunga Massif (mountain gorillas). RESULTS: The Mbeli western gorillas had the latest age at first birth, longest interbirth interval, and slowest surviving birth rate compared to the Virunga mountain gorillas. Bwindi mountain gorillas were intermediate in their life history patterns. DISCUSSION: These patterns are consistent with differences in feeding ecology across sites. However, it is not possible to determine the evolutionary mechanisms responsible for these differences, whether a consequence of genetic adaptation to fluctuating food supplies ("ecological risk aversion hypothesis") or phenotypic plasticity in response to the abundance of food ("energy balance hypothesis"). Our results do not seem consistent with the extrinsic mortality risks at each site, but current conditions for mountain gorillas are unlikely to match their evolutionary history. Not all traits fell along the expected fast-slow continuum, which illustrates that they can vary independently from each other ("modularity model"). Thus, the life history traits of each gorilla population may reflect a complex interplay of multiple ecological influences that are operating through both genetic adaptations and phenotypic plasticity.

Social groups buffer maternal loss in mountain gorillas.

Mothers are crucial for mammals' survival before nutritional independence, but many social mammals reside with their mothers long after. In these species the social adversity caused by maternal loss later in life can dramatically reduce fitness. However, in some human populations these negative consequences can be overcome by care from other group members. We investigated the consequences of maternal loss in mountain gorillas and found no discernible fitness costs to maternal loss through survival, age at first birth, or survival of first offspring through infancy. Social network analysis revealed that relationships with other group members, particularly dominant males and those close in age, strengthened following maternal loss. In contrast to most social mammals, where maternal loss causes considerable social adversity, in mountain gorillas, as in certain human populations, this may be buffered by relationships within cohesive social groups, breaking the link between maternal loss, increased social adversity, and decreased fitness.

Most mammals depend entirely upon their mothers when they are born. In these species, losing a mother at a young age has dramatic consequences for survival. In cases where orphaned individuals do reach adulthood, they often suffer negative effects, like reduced reproductive success or lower social status. But this is not the case for humans. If a child loses their mother; relatives, friends and the wider community can take over. This does not tend to happen in nature. Even our closest relatives, chimpanzees, are much less likely to survive if their mothers die before they reach adolescence. Although orphan survival is not the norm for mammals, humans may not be entirely unique. Mountain gorillas also live in stable family groups, usually with a dominant male and one or more females who care for their offspring for between 8 and 15 years. It is possible that gorillas may also be able to provide community support to orphans, which could buffer the costs of losing a mother, just as it does in humans. To answer this question, Morrison et al. examined 53 years of data collected by the Dian Fossey Gorilla Fund to assess the effects of maternal loss in mountain gorillas. The analysis examined survival, reproduction and changes in social relationships. This revealed that, like humans, young gorillas that lose their mothers are not at a greater risk of dying. There is also no clear long-term effect on their ability to reproduce. In fact, gorillas who lost their mothers ended up with stronger social relationships, especially with the dominant male of the group and young gorillas around the same age. It seems that gorilla social groups, like human families, provide support to young group members that lose their mothers. These findings suggest that the human ability to care for others in times of need may not be unique. It is possible that the tendency to care for orphaned young has its origins in our evolutionary past. Understanding this in more depth could provide clues into the social mechanisms that help to overcome early life adversity, and have a positive impact on future health and survival.

Violent encounters between social units hinder the growth of a high-density mountain gorilla population.

Density-dependent processes such as competition for resources, migration, predation, and disease outbreaks limit the growth of natural populations. The analysis of 50 years of mountain gorilla data reveals that social behavior changes observed at high group density may also affect population growth in social species. A sudden increase in social group density observed in 2007 caused a threefold increase in the rate of violent encounters between social units (groups and solitary males). A fivefold increase in the rate of infanticide and seven cases of lethal fights among mature males were subsequently recorded, and the annual subpopulation growth rate declined by half between 2000 and 2017. The increase in infanticide alone explains 57% of this decline. These findings highlight the complex relationship between population density and growth in social species and hold important implications for the management of island populations.

Behavioral responses around conspecific corpses in adult eastern gorillas (Gorilla beringei spp.).

Humans were once considered unique in having a concept of death but a growing number of observations of animal responses to dying and dead conspecifics suggests otherwise. Complex arrays of behaviors have been described ranging from corpse removal and burial among social insects to quiet attendance and caregiving among elephants and primates. Less frequently described, however, are behavioral responses of individuals from different age/sex classes or social position toward the death of conspecifics. We describe behavioral responses of mountain gorillas (Gorilla beringei beringei) to the deaths of a dominant silverback and a dominant adult female from the same social group in Volcanoes National Park in Rwanda and the responses of Grauer's gorillas (Gorilla b. graueri) to the corpse of an extra-group silverback in Kahuzi-Biega National Park, Democratic Republic of Congo. In gorillas, interactions between groups or with a lone silverback often result in avoidance or aggression. We predicted that: (i) more individuals should interact with the corpses of same-group members than with the corpse of the extra-group silverback; (ii) adult females with infants should avoid the corpse of the extra-group silverback; and (iii) in the mountain gorilla cases, individuals that shared close social relationships with the dead individual should spend more time with the corpse than other individuals in the group. We used a combination of detailed qualitative reports, photos, and videos to describe all occurrences of affiliative/investigative and agonistic behaviors observed at the corpses. We observed similar responses toward the corpses of group and extra-group individuals. Animals in all three cases showed a variety of affiliative/investigative and agonistic behaviors directed to the corpses. Animals of all age/sex classes interacted with the corpses in affiliative/investigative ways but there was a notable absence of all adult females at the corpse of the extra-group silverback. In all three cases, we observed only silverbacks and blackbacks being agonistic around and/or toward the corpses. In the mountain gorilla cases, the individuals who spent the most time with the corpses were animals who shared close social relationships with the deceased. We emphasize the similarity in the behavioral responses around the corpses of group and extra-group individuals, and suggest that the behavioral responses were influenced in part by close social relationships between the deceased and certain group members and by a general curiosity about death. We further discuss the implications close interactions with corpses have for disease transmission within and between gorilla social groups.

Quadratic relationships between group size and foraging efficiency in a herbivorous primate.

The effect of feeding competition on foraging efficiency is an important link between ecological factors and the social organization of gregarious species. We examined the effects of group size on daily travel distances, activity budgets, and energy intake of mountain gorillas in Rwanda. We measured daily travel distances of five groups, activity budgets of 79 gorillas in nine groups, and energy intake data for 23 adult females in three groups over a 16-month period. Travel distances and the proportion of time spent traveling increased with size for most groups, which would be expected if their foraging efficiency is limited by intragroup feeding competition. However, travel distances and times decreased for the largest group, which also had higher energy intake rates than intermediate sized groups. The improved foraging efficiency of the largest group may be explained by advantages in intergroup contest competition. The largest group had much lower home range overlap than the other study groups which may be due to groups avoiding one another as a result of male mating competition. Collectively, our results indicate that intermediate sized groups had the lowest foraging efficiency and provide a new twist on the growing evidence of non-linear relationships between group size and foraging efficiency in primates.

Observations of severe and lethal coalitionary attacks in wild mountain gorillas.

In humans and chimpanzees, most intraspecific killing occurs during coalitionary intergroup conflict. In the closely related genus Gorilla, such behavior has not been described. We report three cases of multi-male, multi-female wild mountain gorilla (G. beringei) groups attacking extra-group males. The behavior was strikingly similar to reports in chimpanzees, but was never observed in gorillas until after a demographic transition left ~25% of the population living in large social groups with multiple (3+) males. Resource competition is generally considered a motivator of great apes' (including humans) violent intergroup conflict, but mountain gorillas are non-territorial herbivores with low feeding competition. While adult male gorillas have a defensible resource (i.e. females) and nursing/pregnant females are likely motivated to drive off potentially infanticidal intruders, the participation of others (e.g. juveniles, sub-adults, cycling females) is harder to explain. We speculate that the potential for severe group disruption when current alpha males are severely injured or killed may provide sufficient motivation when the costs to participants are low. These observations suggest that the gorilla population's recent increase in multi-male groups facilitated the emergence of such behavior, and indicates social structure is a key predictor of coalitionary aggression even in the absence of meaningful resource stress.