Shelly Masi

Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory

The most important environmental factor explaining interspecies variation in ecology and sociality of the great apes is likely to be variation in resource availability. Relatively little is known about the activity patterns of western lowland gorillas (Gorilla gorilla gorilla), which inhabit a dramatically different environment from the well‐studied mountain gorillas (G. beringei beringei). This study aims to provide a detailed quantification of western lowland gorillas activity budgets using direct observations on one habituated group in Bai Hokou, Central African Republic. We examined how activity patterns of both sexes are shaped by seasonal frugivory. Activity was recorded with 5‐min instantaneous sampling between December 2004 and December 2005. During the high‐frugivory period the gorillas spent less time feeding and more time traveling than during the low‐frugivory period. The silverback spent less time feeding but more time resting than both females and immatures, which likely results from a combination of social and physiological factors. When compared with mountain gorillas, western lowland gorillas spend more time feeding (67 vs. 55%) and traveling (12 vs. 6.5%), but less time resting (21 vs. 34%) and engaging in social/other activities (0.5 vs. 3.6%). This disparity in activity budgets of western lowland gorillas and mountain gorillas may be explained by the more frugivorous diet and the greater dispersion of food resources experienced by western lowland gorillas. Like other apes, western lowland gorillas change their activity patterns in response to changes in the diet. Am. J. Primatol. 71:91–100, 2009.

Wild Chimpanzees on the Edge: Nocturnal Activities in Croplands

In a rapidly changing landscape highly impacted by anthropogenic activities, the great apes are facing new challenges to coexist with humans. For chimpanzee communities inhabiting encroached territories, not bordered by rival conspecifics but by human agricultural fields, such boundaries are risky areas. To investigate the hypothesis that they use specific strategies for incursions out of the forest into maize fields to prevent the risk of detection by humans guarding their field, we carried out video recordings of chimpanzees at the edge of the forest bordered by a maize plantation in Kibale National Park, Uganda. Contrary to our expectations, large parties are engaged in crop-raids, including vulnerable individuals such as females with clinging infants. More surprisingly chimpanzees were crop-raiding during the night. They also stayed longer in the maize field and presented few signs of vigilance and anxiety during these nocturnal crop-raids. While nocturnal activities of chimpanzees have been reported during full moon periods, this is the first record of frequent and repeated nocturnal activities after twilight, in darkness. Habitat destruction may have promoted behavioural adjustments such as nocturnal exploitation of open croplands.

Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: Role of sociality and physiology on learning process

Certain toxic plants are beneficial for health if small amounts are ingested infrequently and in a specific context of illness. Among our closest living relatives, chimpanzees are found to consume plants with pharmacological properties. Providing insight on the origins of human self-medication, this study investigates the role social systems and physiology (namely gut specialization) play on learning mechanisms involved in the consumption of unusual and potentially bioactive foods by two great ape species. We collected data from a community of 41-44 wild chimpanzees in Uganda (11 months, 2008), and a group of 11-13 wild western gorillas in Central African Republic (10 months, 2008-2009). During feeding, we recorded food consumed, its availability, and social interactions (including observers watching conspecifics and the observers subsequent activity). Unusual food consumption in chimpanzees was twice higher than in gorillas. Additionally chimpanzees relied more on social information with vertical knowledge transmission on unusual foods by continually acquiring information during their life through mostly observing the fittest (pre-senescent) adults. In contrast, in gorillas observational learning primarily occurred between related immatures, showing instead the importance of horizontal knowledge transmission. As chimpanzees guts are physiologically less specialized than gorillas (more capable of detoxifying harmful compounds), unusual-food consumption may be more risky for chimpanzees and linked to reasons other than nutrition (like self-medication). Our results show that differences in sociality and physiology between the two species may influence mechanisms that discriminate between plants for nutrition and plants with potential therapeutic dietary components. We conclude that self-medication may have appeared in our ancestors in association with high social tolerance and lack of herbivorous gut specialization.

The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest.

To understand the evolutionary histories and conservation potential of wild animal species it is useful to assess whether taxa are genetically structured into different populations and identify the underlying factors responsible for any clustering. Landscape features such as rivers may influence genetic population structure, and analysis of structure by sex can further reveal effects of sex‐specific dispersal. Using microsatellite genotypes obtained from noninvasively collected fecal samples we investigated the population structure of 261 western lowland gorillas (WLGs) (Gorilla gorilla gorilla) from seven locations spanning an approximately 37,000u2009km2 region of mainly continuous rain forest within Central African Republic (CAR), Republic of Congo and Cameroon. We found our sample to consist of two or three significantly differentiated clusters. The boundaries of the clusters coincided with courses of major rivers. Moreover, geographic distance detoured around rivers better‐explained variation in genetic distance than straight line distance. Together these results suggest that major rivers in our study area play an important role in directing WLG gene flow. The number of clusters did not change when males and females were analyzed separately, indicating a lack of greater philopatry in WLG females than males at this scale. Am. J. Primatol. 76:868–878, 2014.

Seasonal Effects on Great Ape Health: A Case Study of Wild Chimpanzees and Western Gorillas

Among factors affecting animal health, environmental influences may directly or indirectly impact host nutritional condition, fecundity, and their degree of parasitism. Our closest relatives, the great apes, are all endangered and particularly sensitive to infectious diseases. Both chimpanzees and western gorillas experience large seasonal variations in fruit availability but only western gorillas accordingly show large changes in their degree of frugivory. The aim of this study is to investigate and compare factors affecting health (through records of clinical signs, urine, and faecal samples) of habituated wild ape populations: a community (Nu200a=u200a46 individuals) of chimpanzees (Pan troglodytes) in Kanyawara, Kibale National Park (Uganda), and a western gorilla (G. gorilla) group (Nu200a=u200a13) in Bai Hokou in the Dzanga-Ndoki National Park (Central African Republic). Ape health monitoring was carried out in the wet and dry seasons (chimpanzees: July–December 2006; gorillas: April–July 2008 and December 2008–February 2009). Compared to chimpanzees, western gorillas were shown to have marginally greater parasite diversity, higher prevalence and intensity of both parasite and urine infections, and lower occurrence of diarrhea and wounds. Parasite infections (prevalence and load), but not abnormal urine parameters, were significantly higher during the dry season of the study period for western gorillas, who thus appeared more affected by the large temporal changes in the environment in comparison to chimpanzees. Infant gorillas were the most susceptible among all the age/sex classes (of both apes) having much more intense infections and urine blood concentrations, again during the dry season. Long term studies are needed to confirm the influence of seasonal factors on health and parasitism of these great apes. However, this study suggest climate change and forest fragmentation leading to potentially larger seasonal fluctuations of the environment may affect patterns of ape parasitism and further exacerbate health impacts on great ape populations that live in highly seasonal habitats.

Behavioral variation in gorillas: Evidence of potential cultural traits

The question of whether any species except humans exhibits culture has generated much debate, partially due to the difficulty of providing conclusive evidence from observational studies in the wild. A starting point for demonstrating the existence of culture that has been used for many species including chimpanzees and orangutans is to show that there is geographic variation in the occurrence of particular behavioral traits inferred to be a result of social learning and not ecological or genetic influences. Gorillas live in a wide variety of habitats across Africa and they exhibit flexibility in diet, behavior, and social structure. Here we apply the ‘method of exclusion’ to look for the presence/absence of behaviors that could be considered potential cultural traits in well-habituated groups from five study sites of the two species of gorillas. Of the 41 behaviors considered, 23 met the criteria of potential cultural traits, of which one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. There was a strong positive correlation between behavioral dissimilarity and geographic distance among gorilla study sites. Roughly half of all variation in potential cultural traits was intraspecific differences (i.e. variability among sites within a species) and the other 50% of potential cultural traits were differences between western and eastern gorillas. Further research is needed to investigate if the occurrence of these traits is influenced by social learning. These findings emphasize the importance of investigating cultural traits in African apes and other species to shed light on the origin of human culture.

The influence of seasonal frugivory on nutrient and energy intake in wild western gorillas

The daily energy requirements of animals are determined by a combination of physical and physiological factors, but food availability may challenge the capacity to meet nutritional needs. Western gorillas (Gorilla gorilla) are an interesting model for investigating this topic because they are folivore-frugivores that adjust their diet and activities to seasonal variation in fruit availability. Observations of one habituated group of western gorillas in Bai-Hokou, Central African Republic (December 2004-December 2005) were used to examine seasonal variation in diet quality and nutritional intake. We tested if during the high fruit season the food consumed by western gorillas was higher in quality (higher in energy, sugar, fat but lower in fibre and antifeedants) than during the low fruit season. Food consumed during the high fruit season was higher in digestible energy, but not any other macronutrients. Second, we investigated whether the gorillas increased their daily intake of carbohydrates, metabolizable energy (KCal/g OM), or other nutrients during the high fruit season. Intake of dry matter, fibers, fat, protein and the majority of minerals and phenols decreased with increased frugivory and there was some indication of seasonal variation in intake of energy (KCal/g OM), tannins, protein/fiber ratio, and iron. Intake of non-structural carbohydrates and sugars was not influenced by fruit availability. Gorillas are probably able to extract large quantities of energy via fermentation since they rely on proteinaceous leaves during the low fruit season. Macronutrients and micronutrients, but not digestible energy, may be limited for them during times of low fruit availability because they are hind-gut fermenters. We discuss the advantages of seasonal frugivores having large dietary breath and flexibility, significant characteristics to consider in the conservation strategies of endangered species.

Response to bitter substances in primates: Roles of diet tendency and weaning age

In primates, the perception of bitter taste may be an essential mechanism for avoiding the ingestion of bitter, and often toxic, substances. Bitterness sensitivity varies across the different primate species and, for bitter thioure substances (e.g., phenylthiocarbamide—PTC), within species. Primates respond to bitterness by displaying aversive affective reactions, and whether these serve for conspecifics as information on the taste of food is still unclear. The aim of this study was to investigate the response to two bitter substances (quinine and PTC) in 11 primate species (N = 29 individuals) hosted at the Ménagerie du Jardin des Plantes, in relation to their main diet tendency and weaning age. We tested primate reactions to bitterness with a two-bottle method. The study individuals showed a strong aversion to bitter taste, minimizing consumption of both bitter solutions. All of the individuals were PTC-taster phenotypes, but the degrees of sensitivity to PTC varied among the individuals. Across-species comparisons revealed that whereas the degree of frugivory of the species had a negative effect on the consumption of bitter solutions by the individuals, a later weaning age seems to be a better predictor for the occurrence of aversive affective reactions. Although the low sample size does not allow for excluding interindividual variability, our results support the hypothesis that affective reactions to bitterness may be trustworthy information for conspecifics during the learning process. Thus, the evolution of the appropriate perceiver systems to convert affective displays into true affective signals could be a shared trait among human and nonhuman primates.

Odor signals in wild western lowland gorillas: an involuntary and extra-group communication hypothesis.

Odors constitute one of the most ancient ways of communication among animals. Whereas the key role of olfactory communication is well established in insects or rodents, its contribution to primate behavior remains very speculative. In a recent report, Klailova and Lee [1] studied the variations of intensity of the typical steroid musk odor produced by wild adult male gorilla silverbacks during encounters with opponents from other social units (lone males or other groups). The odor intensity increased in situations of potential conflicts, when the silverback encountered another male gorilla, which constitutes a potential threat for his infants and mate competitor for his females. Importantly, the odor intensity was greater when the silverback reacted with a demonstrative threat display, and milder when he decided to react quietly and avoid the conflict by sneaking away. According to the authors, this indicates that silverback gorillas can flexibly adjust the odor signal to the social context, and the mild signal associated with the quiet response is used within the silverbacks group to promote cohesion. Rather, based on both physiological and behavioral data, we propose that (1) the odor intensity varies monotonically with arousal, across all situations, and (2) that the function of the odor signal is most relevant for the interactions between males of different groups. In such framework, the odor stimulus might also constitute a non-visual signal indicator of the emitters identity, and therefore play a role in the regulation of the interactions with other gorillas. Establishing the balance among those potential functions is critical to understand the role of odors in the regulation of social and ecological interactions in primates.

Observational Monitoring of Clinical Signs during the Last Stage of Habituation in a Wild Western Gorilla Group at Bai Hokou, Central African Republic

Anthropozoonotic disease transmission to great apes is a critical conservation concern, and has raised ethical doubts regarding ape habituation. We monitored over a 3-year period clinical signs within a group of wild western gorillas (G. gorilla) undergoing habituation at Bai Hokou, Central African Republic. The majority of observations consisted of singular coughs and sneezes among the gorillas. These were the only clinical signs that significantly and positively increased over the years. No changes in the demography of the study group were observed. While clinical signs are not necessarily indicative of ‘disease or other health-related problems, we discuss how long-term records of clinical signs provide useful information when health monitoring, and the importance of the rigid application of preventive disease transmission protocols.