Melissa J. Remis

Western Lowland Gorillas (Gorilla gorilla gorilla) as Seasonal Frugivores: Use of Variable Resources

The gorillas studied at Bai Hokou, Central African Republic, between August 1990 and October 1992 consumed 239 kinds of foods from 138 species of plants and invertebrates, including the fruits of 77 species. Seeds were present in 99% of all fecal samples (n = 859). Although gorillas ate fleshy fruit whenever it was available, herbaceous plants and fibrous fruits were consumed year‐round and were important during times of fleshy fruit scarcity. At Bai Hokou and across their range, resources are temporally discontinuous, and western gorilla diet exhibits marked seasonal and interannual variation. Although their large body size lends them dietary flexibility relative to chimpanzees, seasonal fruit‐eating shapes the foraging and ranging patterns of western lowland gorillas. Am. J. Primatol. 43:87–109, 1997.

Nutritional Aspects of Western Lowland Gorilla (Gorilla gorilla gorilla) Diet During Seasons of Fruit Scarcity at Bai Hokou, Central African Republic

Traditionally, gorillas were classified as folivores, yet 15 years of data on western lowland gorillas (Gorilla gorilla gorilla) show their diet to contain large quantities of foliage and fruit, and to vary both seasonally and annually. The consumption of fruit by gorillas at Bai Hokou, Central African Republic, is correlated with rainfall and ripe fruit availability (Remis, 1997a). We investigated the nutritional and chemical content of gorilla foods consumed at Bai Hokou during two seasons of fruit scarcity as measured by phenological observations and compared our findings with the nutrient content of gorilla foods at other African sites. We conclude that during lean times, Bai Hokou gorillas consumed fruits with higher levels of fiber and secondary compounds than those of other populations of western lowland or mountain gorillas. Conversely, leaves consumed by Bai Hokou gorillas were relatively low in fiber and tannins. Bai Hokou gorillas appeared to meet their nutritional needs by eating a combination of fruit and foliage. They ate fruits comparatively high in secondary compounds and fiber when necessary. While gorillas are selective feeders, wherever and whenever preferred foods are scarce, their large body size and digestive anatomy enable them to consume and process a broader repertoire of foods than smaller bodied-apes.

Ranging and grouping patterns of a western lowland gorilla group at Bai Hokou, Central African Republic

The ranging and grouping patterns of a gorilla group were studied during 27 months from 1990-1992 at the Bai Hokou study site, Central African Republic. The study group ranged far daily (average = 2.3 km/day) and had a large home range (22.9 km2), relative to mountain gorillas, and ranging patterns differed between years. During 1990-1992, the bimale study group foraged less cohesively and had more flexible grouping patterns than mountain gorillas. The study group sometimes split into two distinct foraging subgroups, each led by a silverback, and these subgroups occasionally slept apart (mean = 950 m apart). Lowland gorillas rely on many of the same fruit resources as sympatric chimpanzees, and under certain demographic situations gorillas, like sympatric chimpanzees, may adapt their foraging group size to reduce intragroup feeding competition. However, the fiber content of the lowland gorilla diet likely relaxes constraints on foraging party size and facilitates group cohesion relative to chimpanzees.

Digesta Passage, Digestibility and Behavior in Captive Gorillas Under Two Dietary Regimens

Gorilla adaptation has been debated in recent years given the wide variation among diets of gorillas in different habitats. Gorillas are the largest of living primates, have large colons and should be capable of processing tough foods. Preliminary captive studies have suggested that they may well have long average gut retention times relative to smaller hominoids, which should facilitate digestive efficiency in their wild counterparts. Indeed, wild gorillas consume large amounts of fibrous foods as staples or fall-back foods across their range, in response to habitat-related or seasonal changes in fruit availability. Fluctuations in diet might be matched by changes in digesta passage and digestibility, with possible selective retention of harder to digest items. We further studied digestive processes via chemical cobalt and chromium markers to track liquid and solids, as they passed through the guts of gorillas at the San Francisco Zoo (SFZ). In addition, we examined the effects of variation in captive diets on intake, digesta passage, digestion and behavior. The SFZ gorillas exhibited high digestibility coefficients, and gut passage was long relative to those of smaller-bodied hominoids. The results permit us to understand more fully the relationships of digestive processes to adaptation and dietary flexibility in the wild and to inform the development of dietary recommendations to improve the well-being of captive gorillas.

Initial studies on the contributions of body size and gastrointestinal passage rates to dietary flexibility among gorillas

Large body size has been traditionally seen as the primary dietary adaptation of gorillas, facilitating their consumption of fibrous foods (Schaller ¿1963 The Mountain Gorilla; Watts ¿1990 Int. J. Primatol. 11:21-45). Nevertheless, recent research has emphasized frugivory among western lowland gorillas, as well as the influence of habitat and seasonality on gorilla diet and behavior across subspecies (Watts ¿1990 Int. J. Primatol. 11:21-45; Tutin et al. ¿1991 Philos. R. Soc. Trans. Lond. Biol. 334:179-186; Remis ¿1994 Ph.D. Thesis, ¿1997a Am. J. Primatol. 43:87-109, ¿1997b Am. J. Primatol. 43:111-133, ¿1998 Primate Locomotion: Recent Advances, p 95-(1)108, ¿1999 Primates 40:383-396; Nishihara ¿1995 Primates 36:151-168; Goldsmith ¿1999a Int. J. Primatol. 20:1-23, Goldsmith [1999b] Nonhuman Primates, p 58-63). This study provides preliminary data to address the physiological underpinnings of dietary flexibility among gorillas, and their consumption of a broad range of fibrous and tannin-rich foods. To date, little is known about the digestive physiology of the African apes (but see Milton ¿1984 Adaptations for Foraging in Nonhuman Primates, p 249-279, Milton [1984] ¿1999Evol. Anthropol. 8:11-20; Milton and Demment ¿1988 J. Nutr. 118:1082-1088; Lambert ¿1997 Ph.D. Dissertation), although gastrointestinal morphology and proportions are roughly similar among species ( Chivers and Hladik ¿1980 J. Morphol. 166:337-386). This study provides additional experimental data on the gastrointestinal passage times of gorillas (Gorilla gorilla gorilla) fed a captive diet in a zoological park setting and discusses results in relation to field research on gorilla feeding ecology. In this study, 480 small plastic markers were fed to six captive gorillas. The mean gut retention time (MRT) of the adult gorillas in this study was 50 hr, longer than the 31 hr reported for chimpanzees fed a similar diet (Lambert ¿1997 Ph.D. Dissertation). These data suggest that gorillas may retain foods in their gastrointestinal tracts longer than smaller hominoids, and that the large body size likely forms the primary basis for consumption of fiber. This research provides additional data to contribute to our understanding of the relationships of body size and morphology to ecology, and the evolution of body size, foraging strategy and social organization among the African apes.

Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns

To understand how the gut microbiome is impacted by human adaptation to varying environments, we explored gut bacterial communities in the BaAka rainforest hunter-gatherers and their agriculturalist Bantu neighbors in the Central African Republic. Although the microbiome of both groups is compositionally similar, hunter-gatherers harbor increased abundance of Prevotellaceae, Treponema, and Clostridiaceae, while the Bantu gut microbiome is dominated by Firmicutes. Comparisons with US Americans reveal microbiome differences between Africans and westerners but show western-like features in the Bantu, including an increased abundance of predictive carbohydrate and xenobiotic metabolic pathways. In contrast, the hunter-gatherer gut shows increased abundance of predicted virulence, amino acid, and vitamin metabolism functions, as well as dominance of lipid and amino-acid-derived metabolites, as determined through metabolomics. Our results demonstrate gradients of traditional subsistence patterns in two neighboring African groups and highlight the adaptability of the microbiome in response to host ecology.

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.

Tree structure and sex differences in arboreality among western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic

The aim of six months of research in 1995 on the gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic, was to study the effects of tree structure, relative numbers of arboreal feeding sites, and sex differences in body size on arboreal foraging. The analysis presented here also documents inter-annual variation in fruit availability and climbing by silverback gorillas by comparing the 1995 results to those from earlier research, 1990–1992. This analysis suggests that female gorillas maintain similar levels of arboreality in fruit-rich and fruit-poor seasons and years, but silverbacks may be more terrestrial when fruit is scarce or difficult to access. Trees of different shapes present different numbers of feeding sites to bigger males and smaller females. Male climbing is affected by the availability of fruit, and small trees with narrow crowns that lend easy access to fruit from the core. This study suggests that the energetics of vertical climbing and biomechanical constraints imposed by small branch feeding sites in the periphery of trees may constrain the arboreal behavior of male gorillas. Fine-tuned comparisons of food availability, tree structure, and variation in social context of behavior across habitats, will assist efforts to understand differences in ecology among populations and species of African apes.

The Gorilla Paradox

Gorillas posses general ape adaptations for climbing yet the best studied gorillas in the Virungas depart from the arboreal, frugivorous pattern seen among the other apes. Terrestriality and folivory among gorillas have traditionally been viewed as consequences of their large body size. This study aims to separate the influences of body size from those of habitat on tree climbing by gorillas by comparing the results of 27 months of study of western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic (Remis, 1994, 1995) to published reports on the positional behavior of mountain gorillas (Gorilla gorilla beringei) at Karisoke, Rwanda (Tuttle and Watts, 1985; Doran, 1996).

Transvalued Species in an African Forest

We combined ethnographic investigations with repeated ecological transect surveys in the Dzanga-Sangha Dense Forest Reserve (RDS), Central African Republic, to elucidate consequences of intensifying mixed use of forests. We devised a framework for transvaluation of wildlife species, which means the valuing of species on the basis of their ecological, economic, and symbolic roles in human lives. We measured responses to hunting, tourism, and conservation of two transvalued species in RDS: elephants (Loxodonta cyclotis) and gorillas (Gorilla gorilla). Our methods included collecting data on encounter rates and habitat use on line transects. We recorded cross-cultural variation in ideas about and interactions with these species during participant observation of hunting and tourism encounters and ethnographic interviews with hunters, conservation staff, researchers, and tourists. Ecologically, gorillas used human-modified landscapes successfully, and elephants were more vulnerable than gorillas to hunting. Economically, tourism and encounters with elephants and gorillas generated revenues and other benefits for local participants. Symbolically, transvaluation of species seemed to undergird competing institutions of forest management that could prove unsustainable. Nevertheless, transvaluation may also offer alternatives to existing social hierarchies, thereby integrating local and transnational support for conservation measures. The study of transvaluation requires attention to transnational flows of ideas and resources because they influence transspecies interactions. Cross-disciplinary in nature, transvalution of species addresses the political and economic challenges to conservation because it recognizes the varied human communities that shape the survival of wildlife in a given site. Transvaluation of species could foster more socially inclusive management and monitoring approaches attuned to competing economic demands, specific species behaviors, and human practices at local scales.