A recent study unveils some of the enigmas associated with the social behaviour of the western lowland gorilla (Gorilla gorilla gorilla) from the impenetrable African equatorial forests; it was the result of an international cooperation bringing together the efforts of scientists at Spanish and French research institutions assisted by the SPAC Foundation gGmbH (Germany). This multidisciplinary study was based on five years of monitoring three gorilla groups habituated to human observers, and 4 months of intensive non-invasive genetic sampling of the entire population of an area of about 44 km² in the Ngaga Forest (Republic of the Congo). The research has revealed a dynamic social structure with frequent exchanges of individuals between groups favoured by a high degree of tolerance and peaceful coexistence among their members.

Since the dawn of great ape studies, it was clear that the western lowland gorillas inhabiting the remote rainforests of the Congo River basin and the mountain gorillas (Gorilla beringei beringei) from the volcanic slopes of the Rift Valley displayed remarkable differences in social behaviour. While in mountain gorillas the rare intergroup interactions frequently resulted in agonistic encounters/displays and even infanticide, aggressive interactions were exceptional among western lowland gorillas. Nonetheless, the scarce accessibility and visibility inside the forests had insofar limited most of the studies on western lowland gorillas to bais, open clearings that work as rendezvous for multiple family groups foraging on plants rich in mineral salts. Even though the frequent intergroup interactions were overtly peaceful at these sites, doubts remained about the real nature of western lowland gorilla ecology and behaviour in the surrounding dense forests where groups spent up to 99 % of their time (Magliocca & Gautier-Hion 2002). In this sense, bais could represent abundant but geographically restricted resources, possibly located outside gorilla ranges and that, as such, do not need to be defended. Moreover, not all western gorilla groups have access to such unique landscape features. Consequently, the interactions between gorilla social units at these sites may not be representative of social behaviour within the forest.

The almost daily observations over 5 years (2013-2017) of three focal gorilla groups habituated to the presence of humans and with overlapping home ranges, allowed us to directly observe encounters between the groups in the forest. During the encounters, individuals from the different groups traveled, fed and even played peacefully together. The interactions were frequently driven by young gorillas, but all age classes participated and silverback males showed remarkable tolerance towards these interactions. In some encounters the three gorilla groups were found together, adding up to more than 50 individuals.

One could think that these non-aggressive interactions were exclusive for these habituated gorilla groups. However, the analysis of the population structure revealed that this high tolerance was a widespread phenomenon. The genetic analyses of fecal samples collected in night nests of social groups and lone individuals allowed the identification of more than 120 gorillas, the study of the relatedness between them, and the determination of the gorillas present in each social group. The field monitoring took place in a very reduced time period, from May to August 2013, to obtain a snapshot of the composition of the population at that time. Also, the monitoring took place in a small study area of ca. 40 km² to try to identify the great majority of the gorillas then present in the population. Surprisingly, we identified individuals of different age and sex moving from one group to another within just a few days, as well as other individuals found alone on some occasions and then integrated within groups on others. Some adult females found in one group had offspring in another group, showing that they had moved between reproductive units and that immatures were admitted within a group even if their mother was not there, confirming the lack of infanticide suggested for this species (and instead common in mountain gorillas). Groups sampled on multiple days had quite variable individual composition, showing that not all individuals stayed together at all times. Immatures, the individuals that were observed involved in many of the inter-group interactions, were the ones that more frequently moved temporarily out of the group. This evidenced a very dynamic social system that goes beyond the group dynamics described in previous studies spanning multiple years (Arandjelovic et al. 2010, 2014; Hagemann et al. 2018).

The emerging picture is that of a modular society resulting from the interplay of moderately strong ties which do not prevent the transfer of individuals between different social units, and a high degree of tolerance between groups. This could have promoted information exchange between groups and may have been important in the evolutionary history of the species. However, this behaviour could have also increased the impact of infectious diseases that have killed more than 95 % of the individuals in some western lowland gorilla populations in the Republic of the Congo (Bermejo et al. 2006; Caillaud et al. 2006). These events of high mortality warranted the inclusion of the species as "critically endangered" in the Red List of threatened species by IUCN (International Union for Conservation of Nature).

Overall, the results of this research evidence the importance of integrating in situ monitoring studies with non-invasive genetic analyses to understand the structure and social dynamics in secretive or cryptic animal species. Also, the findings show the key role of social behaviour in disease transmission and establishment of effective conservation strategies in the long term.

Giovanni Forcina, Dominique Vallet, Pascaline J. Le Gouar, Rubén Bernardo-Madrid, Germán Illera, Guillem Molina-Vacas, Stéphane Dréano, Eloy Revilla, José Domingo Rodríguez-Teijeiro, Nelly Ménard, Magdalena Bermejo and Carles Vilà

Original article
Forcina, G., Vallet, D., Le Gouar, P. J., Bernardo-Madrid, R., Illera, G., Molina-Vacas, G., Dréano, S., Revilla, E., Rodríguez-Teijero, J. D., Ménard, N., Bermejo, M., Vilà, C. (2019): From groups to communities in western lowland gorillas. Proceedings of the Royal Society B: Biological Sciences 286 (1896)

References

Arandjelovic, M. et al. (2010): Effective non-invasive genetic monitoring of multiple wild western gorilla groups. Biological Conservations 143, 1780-1791

Arandjelovic, M. et al. (2014): Genetic inference of group dynamics and female kin structure in a western lowland gorilla population (Gorilla gorilla gorilla). Primate Biology 1, 29-38

Bermejo, M. et al. (2006): Ebola outbreak killed 5000 gorillas. Science 314, 1564

Caillaud, D. et al. (2006): Gorilla susceptibility to Ebola virus: the cost of sociality. Current Biology 16, R489-R491

Hagemann, L. et al. (2018): Long-term group membership and dynamics in a wild western lowland gorilla population (Gorilla gorilla gorilla) inferred using non-invasive genetics. American Journal of Primatology 80, e22898

Magliocca, F. & Gautier-Hion, A. (2002): Mineral content as basis for food selection by western lowland gorillas in a forest clearing. American Journal of Primatology 57, 67-–77