Tropical rainforests are characterized by seasonal fluctuations in fruit availability with important inter-annual variations in tree productivity. These seasonal fluctuations can thus greatly challenge the foraging efficiency of frugivorous mammals, impacting their nutritional and energy balance across the year. Being rich in soluble sugars, fruit is a very high-quality resource providing animals with readily accessible energy. When compared to leaves and herbs, however, fruiting trees are challenging to find in the forest since they are spatially scattered and ephemeral in time (e.g. each species fruiting at a given time of the year).

Site-faithful animal species such as primates respond to the seasonal variation in food availability by flexibly changing their behaviour. To cope with the changes in fruit availability many frugivorous species seasonally adjust their behaviour in terms of activity budget, diet or ranging patterns. The temporal changes in fruit availability can be fairly predictable within a year, thus frugivorous mammals need to know what food they can find, where is located and when across the year. When compared to folivorous/herbivorous species, frugivorous species should thus have higher spatio-temporal knowledge of food resources distribution and availability, a concept known as Ecological Intelligence Hypothesis. This would allow them to better cope with seasonal and fairly predictable environments having spatiotemporal patterns repeated over time (i.e. seasons).

Among frugivorous primates, western gorillas (G. gorilla) should be not exceptional on this. They inhabit the lowland rainy forest characterized by the seasonal changes in fruit availability. In contrast to the folivorous/herbivorous mountain gorillas (Gorilla b. beringei; subspecies of eastern gorillas) western gorillas are mainly frugivorous (70 % of the feeding time) during the season of high fruit availability. Then, they become mainly folivorous/herbivorous during the low fruit season. Western gorillas are thus seen as seasonal frugivores preferring high-sugar fruit when fruit is more available in the forest. The long gut and gut retention time provide gorillas with higher fermenting and detoxifying abilities which enable western gorillas to extract energy also from a more fibrous (herbivorous) diet. To cope with the seasonal changes, they can thus flexibly change the diet and rely on a high-quality diet also when fruit is scarce.

The impact of ecology on western gorillas is evident also at the brain anatomical level. Western gorillas have larger volumes of the cerebellum and hippocampus than G. beringei. These two brain areas are involved in the movements, and in the processing and retention of spatio-temporal cues, respectively. The higher arboreal locomotion, the higher frugivory diet and the larger home ranges may consequently imply more spatial mapping functions of the hippocampus in western gorillas, thus likely shaping the brain differences between the gorilla species.

The alternating periods of fruit scarcity and richness greatly affects western gorilla biology not only in terms of diet. Western gorillas show also seasonal variation in the nutritional intake suggesting that they may face nutritional challenges in response to the seasonal environment. Quantity and diversity of macro- and micro-nutrient intake decrease when gorillas prioritize an energy-rich diet based on fruit. On the other hand, during the low frugivory season, western gorillas consume food with lower metabolizable energy content, and alongside the lower frugivory they likely experienced lower intake of certain vitamins. Such seasonal nutritional stress seems to impact also their microbiome and health, with higher occurrence of parasites and urinary infections during the low frugivory season.

In addition, frugivory seems to increase also within-group feeding competition in western gorillas. When fruit is less available, larger groups show great behavioural flexibility in terms of diet, becoming less frugivorous and more insectivorous when compared to smaller group. Because of the spatial dispersion of fruiting trees, larger groups need to feed less on fruit in order to minimize group spread and reduce infanticide risks. If group size triggers high dietary flexibility both at the group and the population level, activity budget does not differ among the groups between the two seasons.

When being more frugivorous, western gorillas spent less time feeding and more time travelling independently to the group size, when compared to periods of low frugivory. This is also reflected in their space-use patterns. Their movements in the home range are highly dependent on the seasonal diet in addition to the group size and composition. Daily path length and weekly range are larger during the high frugivory season because of the higher frugivorous diet. The daily path length, on average 1.7 km, increases up to 9 km during the high frugivorous season.

When feeding on fruit, western gorillas travel longer distances to locate fruiting trees dispersed within their home ranges. During this season, they thus experience higher travel expenditure and lower diversity of nutrient intake, rising the questions whether this will affect the overall energy budget. Surprisingly, despite these fluctuations they manage to balance their energy budget across the year. How do they achieve to forage efficiently in both seasons?

To meet their nutritional and energy needs across the year, western gorillas likely rely on efficient foraging strategies. Indeed, they do not randomly choose the trees to visit. Like other primates, they prioritize the closest trees (i.e. shorter travelling distance) with the highest probability to provide ripe fruits. In addition, they move linearly when moving between feeding sites. These highly linear movements seem to reflect an ahead planification of foraging movements towards specific feeding sites, rather than being the result of movements in a random direction (until a feeding site is found). Their linear movements are indeed linked to an overall advection (e. g., a forward tendency across the day), especially when they travelled long distances. The optimal foraging strategy of western gorillas is also associated to an effective communication system allowing to drive the whole group towards specific and valuable feeding trees. When discovering high quality and abundant fruit at a tree, western gorillas emit higher frequency of food calls to attract the other group members. Particularly, adult females stop calling when their offspring and the silverback arrived at the tree.

In addition to the high and low fruit abundance, some fruit species are more difficult to predict, since they synchronously produce fruits only once every few years. This is the case for the fruits of Dialium spp. and Gilbertiodendron dewevrei, both figuring importantly in the western gorilla diet. Particularly, when the fruiting season is ending Dialium fruits provide western gorillas with key nutritional elements both via direct ingestion and coprophagy. This species is thus crucial during a period of nutritional transition, thus with higher nutritional needs for the gorillas. Furthermore, some other fruit species are available only for a couple of weeks or just a month, with individual trees fruiting for just few days a year. Do western gorillas forage efficiently because they can track food availability over time?

Independently from the food type (i.e. fruit or young leaves), western gorillas revisit a given individual tree only few times a year. For ephemeral food such as fruit and young leaves from trees, tree visits by the gorillas occur in bursts and within the appropriate season (i.e. when fruit are available), as opposed to the visits to the sites providing year-round available food (i.e. mature leaves from shrubs). Gorillas revisited the same tree every few days and then never did it again during the year.

This foraging pattern shows that gorillas consider the food renovation level of the individual trees till complete depletion of it (i.e. more fruit ripening or leaf shooting over time). Western gorillas seem thus to be able to predict or infer food availability. They likely remember depleted feeding sites at the individual trees by relying on the recent experience of what is available in the environment. They do so also for the fruit of the aquatic tree speciesof Nauclea. Since these trees are present only at clearings or swamps, it is almost impossible to infer their fruiting period by randomly encountering them in the forest. Like wild chimpanzees, overall western gorillas seem to possess an advanced botanical knowledge of tree phenology. Likely, they rely on multiple ecological variables to infer food availability, like the humans who share the same forest with them, the forest people, the Aka.

Given that memory is energy demanding, western gorillas may be selective on what it is worth to remember (e.g. specific trees or feeding tree locations), as it was shown in chimpanzees. The position of some food resources may be worth to remember as opposed to other food that they may eat seasonally but more opportunistically, like insects. Since their ranging patterns and feeding ecology are highly affected by the seasonality in fruit availability, we would expect that western gorillas may have different spatial foraging strategies in each season. They may forage efficiently during the high frugivory season by memorising specific fruit-associated patterns. On the other hand, they may feed more opportunistically during the low frugivory season, when they rely mainly on herbs and leaves.

Even though the feeding sites repeatedly visited by western gorillas differ in each season, surprisingly, no seasonal differences are observed in their spatial movement patterns in terms of revisitation patterns, straightness and speed. Even though they increase travel straightness and speed when feeding on fruit and aquatic herbs, as opposed to leaves, they travel as straight and as fast in both seasons, showing also the same global forward tendency. Western gorillas seem indeed to use an efficient foraging strategy in both seasons in relation to the different seasonal food. This is likely the result of a certain degree of dispersion of the food they eat during the low frugivory seasons. During this period, western gorillas remain selective feeders, feeding on herbs and on specific species of young leaves from trees.

Even though terrestrial herbs are present year-round, they are also concentrated in high density in smaller and larger scattered patches of secondary vegetation. Like for finding fruiting trees, it is likely profitable for western gorillas to use spatial memory also to locate particularly large and herb-rich patches (these being also their preferred sites for night nests). In addition, production of young leaves may not be synchronous at the individual tree level, and trees offering highly proteinaceous young leaves may be as hard to find as fruiting trees. In terms of spatiotemporal availability, young leaves show more similar phenological features to fruit, being more scattered and ephemeral, when compared to widely abundant herbs and mature leaves from shrubs (also eaten by the western gorillas).

Finally, western gorillas feed on year-round aquatic herbs in both seasons. This is often associated to the longest daily journeys towards dispersed and, sometimes, distant clearings or swamps. By providing unique food such as the highly mineral-rich aquatic herbs (and the seasonal flashy fruits of the aquatic species of Nauclea) these areas are likely worth remembering for the gorillas. Overall, the scattered spatial distribution of all this "non-fruit" food may explain the lack of seasonal differences observed in the spatial foraging strategies of western gorillas. They seem to rely on spatiotemporal memory to forage efficiently and to balance their nutrient and energy intake across the year. Their spatial foraging movements are likely based on specific decision rules according to the most complex and nutritionally interesting food in each of the seasons.

In sum, despite western gorillas’ diet, activity budget and ranging are greatly affected by seasonality, they are able to balance the energy budget by relying on similar spatial foraging strategies between the seasons, in addition to an advanced communication capacity allowing high-level group coordination. Western gorillas seem to possess advanced spatiotemporal cognitive abilities to cope with seasonal changes in food distribution and availability. Overall, they show a high degree of behavioural flexibility in response to the environmental changes. In addition to high cognitive abilities, certainly the specific physiological adaptation of a long and enlarged gut allows gorillas to rely on a particular large dietary breadth and flexibility. Their behavioural flexibility highlights also the evolutionary potential that led our common ancestors to cope with environmental constraints.

The higher ecological and behavioural flexibility of this critically endangered species provides us with some hopes for its long standing. Such behavioural flexibility is crucial for the survival of endangered species, providing high resilience towards unpredictable environmental changes. This is particularly relevant in the current context of alarming global climate changes, currently exacerbating the unpredictability and seasonal fruit shortage and abundance for forest animals.

Shelly Masi

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