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«Nutritional Aspects of tlie Diet of Wild Gorillas How Do Bwindi Gorillas Compare? Jessica M. RothmaUy Alice N. Pell^ J. Bosco Nkurunun^fiy and Ellen ...»

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CHAPTER NINE

Nutritional Aspects of tlie

Diet of Wild Gorillas

How Do Bwindi Gorillas Compare?

Jessica M. RothmaUy Alice N. Pell^

J. Bosco Nkurunun^fiy and

Ellen S. Dierenfeld

INTRODUCTION

The foraging behaviors and diet selection of animals in their natural habitats

have been the focus of ecological field studies for decades. Diet affects the lifetime fitness of primates and reproductive performance, an essential consid- eration for highly endangered species (Altmann, 1991, 1998).

The abundance of tropical arboreal folivores is positively correlated with the protein content of leaves and negatively correlated with fiber (Waterman et ^/., 1988; Gates et al., 1990; Ganzhorn, 1992; Chapman et aL, 2002; Chapman et ^/., 2004). Mountain gorillas in Rwanda prefer foods that are high in pro- tein and their movement patterns are related to the quality and availability of foods (Vedder, 1984). There is evidence that some primates in tropical forests Jessica M. Rothman and Alice N. Pell • Department of Animal Science, Cornell University, Ithaca, NY 14853, USA J. Bosco Nkurixnungi • Department of Zoology, Makerere University, Kampala, Uganda Ellen S. Dierenfeld • Department of Animal Science, Cornell University, Ithaca, NY 14853 and St. Louis Zoo, 1 Government Drive, St. Louis, MO 63110, USA.

Primates of Western Uganda, edited by Nicholas E. Newton-Fisher, Hugh Notman, James D. Paterson, and Vernon Reynolds. Springer, New York, 2006.

153 154 Primates of Western Uganda have difficulty obtaining required amounts of certain minerals such as sodium (Rode etal.^ 2003). In western forest clearings, gorillas groups congregate with other animals to seek out water plants that are high in minerals (Magliocca and Gautier-Hion, 2002). Understanding of nutrient requirements and which plants are preferentially consumed can be used to establish priorities for habitat conservation.

Approximately 320 gorillas live in Bwindi Impenetrable National Park (BINP), a 360-km^ forest "fragment" in southwestern Uganda (McNeilage et al.^ 1998, 2001). Bwindi gorillas are currently classified as mountain goril- las {Gorilla berin£fei) (Groves, 2001). They are genetically similar to popula- tions of mountain gorillas in the Virunga Volcanoes area in Rwanda (Garner & Ryder, 1996; Jensen-Seaman & Kidd, 2001), although some have ques- tioned their taxonomic classification at the subspecies level (Sarmiento et PCL^ 1996).

Here, we review the nutritional ecology of gorillas through a discussion of diet, food choice, and digestive anatomy. We compare the nutritional content of foods eaten by gorillas living in different habitats to those consumed by the Bwindi gorillas and discuss the nutritional factors that may influence food selection. The effects of the physical environment on the nutritive value of gorilla foods and some of the analytical challenges that arise on cross-study comparisons are also considered.

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The composition of the diet of wild gorillas has been studied at several sites across central Africa. An initial understanding of gorilla feeding ecology was obtained from the mountain gorillas (Gorilla heringei beringei) in the Virunga region on the borders of Rwanda, Democratic Republic of Congo, and Uganda, an area characterized by afro-alpine vegetation with few or no fruiting trees.

These gorillas are folivores whose diet consists primarily of a few species of herbaceous leaves, vines, stems, and shoots (Schaller, 1963; Fossey & Harcourt, 1977; Vedder, 1984; Watts, 1 9 8 4, 1 9 9 0, 1 9 9 6 ; McNeilage, 1995,2001). Thistle, wild celery, and Galium spp. are primary components of the diets of these gorillas (Watts, 1984). Diet remains relatively constant throughout the year, except for the seasonal consumption of bamboo shoots. Groups of mountain Nutritional Aspects of the Diet of Wild Gorillas 155 gorillas at lower elevations in the Virungas eat different, more varied foods and more fruit than those at higher altitudes (McNeilage, 2001).

In the Kahuzi-Biega National Park of the Democratic Republic of Congo, eastern lowland gorillas (Gorilla heringei grciueri) eat more fruit than the Virunga population, reflecting the greater distribution and availability of fruit in the Kahuzi-Biega habitat (Yamagiwa et al. 1994, 2003). When fruits are unavailable, these gorillas supplement their diet with herbaceous vegetation and the bark of trees and woody lianas (Casimir, 1975; Yamagiwa et al.^ 1994).

Overall, the western gorilla {Gorilla gorilla gorilla) diets are more diverse than those of the mountain gorillas; as many as 230 different plant parts of 180 species are consumed at some locales (e.g. Williamson et al.^ 1990; Tutin & Fernandez, 1993; Nishihara, 1995; reviewed in Doran & McNeilage, 1998;

Doran etal.^ 2002; Rogers etal.^ 2004). If fruits are available, they are consumed regularly. Sweet fruits are preferred, but astringent fruit is eaten when sugary fruits are scarce (Tutin & Fernandez, 1985; Rogers et ^/., 1990; Williamson et al, 1990; Nishihara, 1995; Remis, 1997; Remis et al., 2 0 0 1 ; Goldsmith, 1999; reviewed in Doran & McNeilage, 1998, Doran etal., 2002, Rogers etal., 2004). Along with fruit, western gorillas also eat large quantities of terrestrial vegetation throughout the year (Doran & McNeilage, 1998; Rogers et al.^ 2004). In some areas, gorillas forage in swampy open forest clearings regularly to consume the readily available ripe fruits (Doran-Sheehy etal.^ 2004), a n d / o r mineral-rich water plants (Kuroda et ^/., 1996; Magliocca & Gautier-Hion, 2002).





The altitude of the range of the Bwindi gorillas, between 1160 and 2600 m above sea level is similar to that of the gorillas living in the lower ranges of the Virungas and the higher ranges of the eastern lowland populations. Bwindi gorillas eat more diverse diets than do the gorillas in the Virungas. Between August 2002 and 2 0 0 3, a single Bwindi group (Kyagurilo) consumed at least 160 parts (leaves, stems, fruits, etc.) of 105 different plant species (J. M. Rothman, unpublished data), and, in earlier years, the same group consumed at least 133 parts of 96 species, some of which differed from those eaten in the later study (Stanford & Nkurunungi, 2003). Gorilla groups at different sites within Bwindi consumed a more varied diet than the Kyagurilo group (Ganas et ^/., 2004).

The Bwindi gorillas consume more fruit than the Virunga gorillas, but less fruit than the eastern and western lowland gorillas (Goldsmith, 2003;

156 Primates of Western Uganda Robbins & McNeilage, 2003), an observation based on the presence of seeds in fecal samples. Greater fruit consumption is likely a result of fruit availability (Goldsmith, 2003; Robbins & McNeilage, 2003; Stanford & Nkurunungi, 2003; Nkurunungi, 2005). Bwindi gorillas depend heavily on terrestrial herbaceous vegetation (Goldsmith, 2003) and consume it daily, even when fruit is in abundance.

In addition to herbaceous vegetation and fruits, Bwindi gorillas also consume mature and young true leaves, woody lianas, bark, epiphytes, moss, and a fungus. Bwindi gorillas spend some of their foraging time eating dry, decaying wood and bark (Goldsmith, 2003; Stanford & Nkurunungi, 2003), which has little obvious nutritional value (J. M. Rothman et ^/., in press).

Insectivory and geophagy have been recorded at most study sites (Insectivory: Tutin & Fernandez, 1983, 1992; Harcourt & Harcourt, 1984; Carroll, 1986; Watts, 1989; Nishihara & Kuroda, 1991; Yamagiwa etal, 1991; Kuroda, 1992; Nishihara, 1992; Kuroda ct al,, 1996; Remis, 1997; Deblauwe et aL, 2003; Geophagy: Schaller, 1963; Fossey & Harcourt 1977; Watts, 1984,1989;

Mahaney et al.^ 1990, 1995a,b; Williamson et al.^ 1990). Insect consumption has been observed rarely, among both Bwindi and Virunga gorillas (Fossey & Harcourt, 1977; Harcourt & Harcourt, 1984; Watts, 1984, 1989; Stanford & Nkurunungi, 2003; Ganas & Robbins, 2004). In Bwindi, groups at lower elevations in Bwindi seasonally ate ants more frequently than did a group living at a higher elevation (Ganas & Robbins, 2004). Western gorillas eat insects more frequently than do mountain gorillas. In Cameroon, 74% of 34 fecal samples contained insect remains (Deblauwe etal.^ 2003). Geophagy may be a means to adsorb plant toxins in the diet or relieve stomach discomfort (Krishnamani & Mahaney, 2000). Occasionally, gorillas consumed rocks and soil in Bwindi, either deliberately or accidentally (Stanford & Nkurunungi, 2003; J. M. Rothman, unpublished data).

Coprophagy by wild gorillas is rare. In the Virungas, only 25 instances of coprophagy occurred over thousands of hours of observation (Harcourt & Stewart, 1978). Similarly, the Bwindi gorillas were observed reingesting their own feces only twice during a year of regular observations and a juvenile ate the feces of another individual once (J. M. Rothman, unpublished data). Because this behavior is so uncommon, its nutritional significance is limited. Proposed reasons for gorilla coprophagy include boredom or the craving for warm food on cold days (Harcourt & Stewart, 1978). The rare instances of coprophagy in Bwindi occurred when the gorillas were eating fruit, and the ingested feces Nutritional Aspects of the Diet of Wild Gorillas 157 contained large amounts of seeds. It is possible that the gorillas were reingesting the feces to gain nutrients from the seeds (Kritf et al.^ 2004).

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Gorillas are the largest extant nonhuman primate. Male gorillas weigh between 139 and 278 kg, and mature females weigh between 72 and 98 kg (National Research Council, 2003). Mountain gorillas are larger in size and mass compared to lowland gorillas. Captive gorillas weigh more than wild gorillas, but the weight of the latter tends to be estimated (Leigh, 1994).

The anatomy of the gorilla provides a large capacity for microbial fermentation and subsequent energy gain through the absorption of volatile fatty acids and microbial protein (Stevens & H u m e, 1995). Gorillas have a large, pouched colon, which, based on a male specimen, is about 200 cm long and has a maximum width of approximately 30 cm in the lower ascending colon (Steiner, 1954). While gorillas are frequently considered to be ceco-colonic fermenters, their cecum is relatively small: cecal volume is only about 14% that of the colon, typical of animals that are folivorous and frugivorous (Chivers & Hladik, 1980).

On a captive zoo diet of cultivated fruits, commercially prepared primate biscuits, mixed greens, and hay, captive lowland gorillas had a mean retention time of 50 h, with a range of 16.5-136 h measured with a chromium marker (Remis, 2000). Particulate material is retained longer than liquid material (Remis & Dierenfeld, 2004). When gorillas were fed a diet of 30% neutral detergent fiber (NDF) and 7% acid detergent fiber (ADF), N D F digestibility was 70% but, when the diet contained 30% N D F and 19% ADF, the apparent digestibility of the diet decreased to 45% (Remis & Dierenfeld, 2004). Energy derived from microbial fermentation in the form of short-chain fatty acids may provide between 30 and 60% of the maintenance energy requirements of gorillas (Popovich et al.^ 1997). Most fiber digestion in the gorilla probably occurs in the colon, but there is no research on sites of fermentation in the gorilla. Although gorillas preferentially consume nutritious, readily digestible fruits and herbaceous leaves, they can subsist on fibrous fruit and vegetation when succulent fruits are not in season or available in a habitat. Mobilization and repletion of body reserves provide nutritional safety nets to many species of animals faced with recurring feast or famine conditions. The extent to which 158 Primates of Western Uganda gorillas lose weight during lean times and regain it during times of abundance has not been established.

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Environmental Effects on Nutritional Composition The nutritional composition of plants is affected greatly by external factors in the environment. Soil, water, carbon dioxide, soil nutrients, stress, disease, predation, and weather all influence plant metabolism and the production of resistant structures (Van Soest, 1994). For example, plants that grow at higher temperatures accumulate structural cell wall more quickly than those that grow at lower temperatures. In cooler eastern afro-alpine gorilla habitat, leaves contained more protein and less fiber, were more digestible and richer in phosphorous than foliage from western rain forest trees (Waterman et al.^ 1983).

Considerable between- and within-plant variation in chemical composition has been observed in Kibale forest trees (Chapman et al.^ 2003). Canopy leaves eaten by lemurs in Madagascar contained more protein than leaves from undisturbed areas in the same forest (Ganzhorn et al.^ 1995). The nutrients in the leaves eaten by colobus monkeys changed seasonally, which influenced the monkeys' food choices (Baranga, 1983). Therefore, a chemical analysis provides only a snapshot of the nutrient content of a particular plant at a single point in time.

Careful sampling protocols are needed to ensure that the samples collected reflect what the target animal actually consumed, and that seasonal and spatial variation in food composition are accounted for (Chapman et al.^ 2003).

Standardizing Analytical Techniques

Standardization of the techniques used to measure the nutrient content of primate foods and nonfoods in habitats is necessary to ensure that cross-site comparisons are valid (Chapman et al.^ 2003). Freeze-drying, a very effective means of preserving plants, frequently is not an option at field stations, but drying at temperatures less than 45°C in low light minimizes the effects of temperature and oxidation (Palmer et al.^ 2000). Physical processing, including the type of mill and size of the screen used, also is an important consideration because particle size affects many chemical analyses (Mullin & Wolynetz, 1995).

Choosing an appropriate analytical technique is essential. While a comprehensive analysis of appropriate techniques for measuring the nutrient content of Nutritional Aspects of the Diet of Wild Gorillas 159 primate foodstuffs is beyond the scope of this review, there are a few problems with commonly used analytical techniques that merit consideration.

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