Influence of Plant and Soil Chemistry on Food Selection, Ranging Patterns, and Biomass of Colobus Guereza in Kakamega Forest, Ke

International Journal of Primatology, Vol. 28, No. 3, June 2007 (C 2007) DOI: 10.1007/s10764-006-9096-2 Influence of Plant and Soil Chemistry on Food Selection, Ranging Patterns, and Biomass of Colobus guereza in Kakamega Forest, Kenya Peter J. Fashing,1,2,3,7 Ellen S. Dierenfeld,4,5 and Christopher B. Mowry6 Received February 22, 2006; accepted May 26, 2006; Published Online May 24, 2007 Nutritional factors are among the most important influences on primate food choice. We examined the influence of macronutrients, minerals, and secondary compounds on leaf choices by members of a foli-frugivorous popula- tion of eastern black-and-white colobus—or guerezas (Colobus guereza)— inhabiting the Kakamega Forest, Kenya. Macronutrients exerted a complex influence on guereza leaf choice at Kakamega. At a broad level, protein content was the primary factor determining whether or not guerezas consumed specific leaf items, with eaten leaves at or above a protein threshold of ca. 14% dry matter. However, a finer grade analysis considering the selection ra- tios of only items eaten revealed that fiber played a much greater role than protein in influencing the rates at which different items were eaten relative to their abundance in the forest. Most minerals did not appear to influence leaf choice, though guerezas did exhibit strong selectivity for leaves rich in zinc. Guerezas avoided most leaves high in secondary compounds, though their top food item (Prunus africana mature leaves) contained some of the highest condensed tannin concentrations of any leaves in their diet. Kakamega 1Department of Science and Conservation, Pittsburgh Zoo and PPG Aquarium, One Wild Place, Pittsburgh, Pennsylvania 15206. 2Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania 15206. 3Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania 15206. 4Department of Nutrition, Saint Louis Zoo, One Government Drive, St. Louis, Missouri 63110. 5Department of Ecology, Evolution, and Environmental Biology, Columbia University, 1200 Amsterdam Avenue, New York, New York 10027. 6Department of Biology, Berry College, Mt. Berry, Georgia 30149. 7To whom correspondence should be addressed; e-mail: [email protected]. 673 0164-0291/07/0600-0673/0 C 2007 Springer Science+Business Media, Inc. 674 Fashing, Dierenfeld, and Mowry guerezas periodically traveled great distances to exploit rare foods (bark from exotic Myrtaceae trees and soil) outside their normal home ranges. Our results suggest that these journeys were driven by the fact that these rare foods contained exceptionally high sodium concentrations, a mineral believed to be deficient in the guereza’s usual diet. Lastly, our results are consistent with the pattern established across other Paleotropical rain forests in which colobine biomass can be predicted by the protein-to-fiber ratio in mature leaves. Of the 8 rain forests for which the relevant data are available, Kakamega features the second highest mature leaf protein-to-fiber ratio as well as the second highest colobine biomass. KEY WORDS: colobines; macronutrients; minerals; protein-to-fiber ratio; secondary compounds. INTRODUCTION As eclectic omnivores typically occurring in species-rich tropical en- vironments, most primates must choose between a great many potential food items (Harding, 1981). These choices are influenced by a variety of ecological, morphological, and physiological factors including patterns of food abundance and distribution (Oates, 1987), intra- and inter-specific food competition (Janson, 1988; Waser, 1987), risk of predation (Miller, 2002), body size (Gaulin, 1979), gut morphology (Chivers, 1994; Milton, 1998), energetic requirements (Dasilva, 1992), macronutrient and mineral requirements (Silver et al., 2000; Yeager et al., 1997), and ability to cope with secondary compounds (Glander, 1982). Because food is essential to survival and reproduction, natural selection is expected to exert a strong influence on the food choices of animals, favoring either individuals that maximize their net intake rates of energy or those that optimize the mix of nutrients they consume while foraging (Pyke et al., 1977; Stephens and Krebs, 1986; Westoby, 1974). Indeed, empirical studies have demonstrated that disparities in food intake and foraging efficiency within groups of several primate taxa are associated with interindividual differences in repro- ductive success (Altmann, 1991; van Noordwijk and van Schaik, 1987, 1999; Whitten, 1983). The strong selective pressure on primate food choice sug- gests that patterns of food selection observed during studies of wild primates are adaptive and can provide important insights into primate evolu- tionary ecology (Altmann, 1998; Milton, 1993). Nutritional factors are among the most powerful influences on food choice, posing several challenges that primates must overcome if they are to obtain suitable diets. First, few individual plant food items contain ade- quate concentrations of all the major essential nutrients (protein, fats, car- bohydrates, water, vitamins, and minerals), forcing most primates to forage Plant and Soil Chemistry Effects on Colobus guereza in Kakamega Forest 675 widely for a variety of food items from many species (Milton, 1993; Richard, 1985). Second, primates must take fiber content into account when selecting food items. Items with high concentrations of fibrous components (partic- ularly lignin, cellulose, and hemicellulose) are difficult to digest and many primates avoid them (Milton, 1979; Rogers et al., 1990; Yeager et al., 1997). Third, primates, especially those feeding heavily on leaves or seeds, must cope with the fact that many plants produce secondary compounds intended to deter herbivores from consuming them (Freeland and Janzen, 1974; Glander, 1982). Many primates largely avoid these compounds, including tannins, which bind with proteins to reduce the digestibility of foods, and alkaloids, which act as toxins that disrupt metabolic processes, while other primates have evolved specialized digestive physiologies that allow them to consume some secondary compounds (Lambert, 1998). Because the tropical forests where most primates live are so diverse and each potential food item has its own distinctive combination of essential nutrients, fiber, and secondary compounds, the effects of nutritional variables on food choice can be complex. Researchers have studied the influence of nutrition on food choice in primates most intensively in the Colobinae (Chapman et al., 2004; Davies et al., 1988; Kool, 1992; McKey et al., 1981; Mowry et al., 1996; Oates, 1980; Yeager et al., 1997). Colobines are primarily arboreal monkeys living in Africa and Asia that are characterized by a digestive physiology unique among the primates (Chivers, 1994; Oates and Davies, 1994). They possess an enlarged, sacculated forestomach containing large quantities of anaer- obic bacteria, protozoa, and fungi that ferment ingested food items (Kay and Davies, 1994). The capacity for microbial fermentation in the forestomach offers colobines unusually acute abilities to extract nutrients contained within the fibrous cell walls of plants and to detoxify some plant secondary compounds (Kay and Davies, 1994). Though originally believed to be an adaptation solely to the challenges of a leafy diet, forestomach fermentation also allows colobines to exploit foods such as seeds that are also often rich in secondary compounds (Chivers, 1994). In fact, in recent decades, researchers have upended the traditional view of colobines as obligate leaf- eaters and it is now clear that many colobines are capable of expanding beyond the specialist folivore niche to consume large quantities of whole fruit, seeds, or lichen on a seasonal or even annual basis (Kirkpatrick, 1998; McKey, 1978;Starin,1991). Still, leaves make substantial contributions to the diets of nearly all colobines (Fashing, 2006; Kirkpatrick, 2006) and their fundamental importance to colobines is reflected in the robust link that has been established between the protein-to-fiber ratio in mature leaves and colobine biomass across forests in the Paleotropics (Waterman and Kool, 1994). 676 Fashing, Dierenfeld, and Mowry One colobine species known to exhibit considerable dietary flexibil- ity is the eastern black-and-white colobus or guereza (Colobus guereza). Guerezas subsist heavily on leaves at some sites (Kibale, Uganda: Chapman et al., 2004; Harris, 2005; Oates, 1977a; Ituri, D.R. Congo: Bocian, 1997) and on a more varied diet of leaves and whole fruits or seeds at others (Kakamega, Kenya: Fashing, 2001b; Dja, Cameroon: Poulsen et al., 2002; Budongo, Uganda: A. Plumptre, unpub. data). Researchers have studied the influence of nutritional factors on food choice among guerezas only at the sites where they are most folivorous (Kibale: Baranga, 1982, 1983; Chapman et al., 2002, 2003, 2004; Oates, 1978; Oates et al., 1977; Rode et al., 2003; Wasserman and Chapman, 2003; Ituri: Bocian, 1997). At these sites, levels of protein (Bocian, 1997; Chapman et al., 2004); fiber (Chapman et al., 2004); tannins (Oates et al., 1977); and several minerals including zinc, man- ganese, and sodium (Oates, 1978; Rode et al., 2003) in food items appear to affect food choice. Sodium content also appears to exert a powerful influence on the ranging patterns of guerezas at Kibale, causing them to travel long distances intermittently to access sodium-rich swamp plants and Euca- lyptus sp. (Myrtaceae) trees believed to make up for sodium deficiencies

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