Issues in primate foraging and diet. Review of foraging strategies and natural diet in monkeys apes and humans edited by Andrew Whiten and Elsie M. Widdowsonкод для вставкиСкачать
American Journal of Primatology 33155-159 (1994) BOOK REVIEWS Issues in Primate Foraging and Diet Review of Foraging Strategies and Natural Diet in Monkeys, Apes and Humans, edited by Andrew Whiten and Elsie M. Widdowson. New York, Oxford University Press, 1992, Vlll 138 pp, $65,cloth. + These are the proceedings of a Royal Society discussion meeting held in 1991. The papers are generally of good quality, and I found much of interest in the book. I recommend without hesitation that libraries of primatology or human evolution obtain a copy. Prospective individual buyers should realize, however, that despite its title, the book is not actually an analytical review of how primate species in general go about finding and recognizing essential food items. First, it addresses mainly human diet. The nonhuman primates examined in detail (chimpanzees, gorillas, and baboons) are those thought likely to illustrate the background from which human feeding patterns emerged. Second, the emphasis of the book is primarily on diet and nutrition rather than on foraging “strategies” at the behavioral level. Thus, more space is devoted to analyses of food composition than to the foraging tasks posed by the spatial distribution of nutrients in the field or the detailed behavioral responses which primates use to solve these tasks. The volume contains few quantitative descriptions of travel paths or of species-specific activity patterns, and there is no in-depth review of proximate mechanisms underlying the selection or avoidance of particular food constituents by primates. In sum, readers interested in choice behavior rather than in nutrition as such would have expected a more direct focus on the specific, perceived feeding options which primates face, and on the patterns of choice which imply a particular type of evaluative or “decision-making” process. The book contains 14 chapters in four sections. The individual papers are very heterogeneous in content and could have been published in separate journals. Section 1 includes a review of nonhuman primate diet and nutritional requirements, two papers on the diets of present day African apes, and a report on some of the chemical and seasonal factors influencing dietary choices in baboons. Section 2 contains two papers on the archaeological record of human diet and one paper on the energetics of hominid encephalization. Section 3 examines the diet and food gathering patterns of present day hunter-gatherer groups. Section 4 contains one paper on dietary change in humans at the beginning of agriculture and two general papers on nutrition in contemporary humans. The editors view the accurate measurement of nutrient requirements, of nutrient intakes, and of the quantitative relations between these two variables as one of the cornerstones of primate dietary research. In this respect, Whiten and Widdowson align themselves with previous editors and with many current-day researchers. It is interesting, however, to read Oftedal’s critical appraisal of this research aim and his review of the pertinent literature. Although the methods of the reviewed studies are not always described sufficiently for readers to interpret the findings adequately, one message is that the accurate measurement of primate 0 1994 Wiley-Liss, Inc. 156 / Menzel nutrient requirements and nutrient intakes in the field may be very difficult to achieve. Regarding nutrient intakes, one must record the amount of each food item type ingested by animals, not simply the time spent feeding on certain items. More importantly, the energy available from every type of ingested food should be determined by digestion trials rather than simply by bomb calorimetry. For example, commercially prepared fiber is only partially digestible rather than 100% digestible. At present, there are few data available for wild foods to take the issue much further. It is not clear from this paper how one could determine the available energy content of non-eaten items with any accuracy, given that digestion trials are not feasible. Regarding nutrient requirements, Oftedal reports that the U.S. National Research Council has determined the quantitative requirements for 24 of 45-47 required nutrients for primates under laboratory conditions. It would be useful in a future paper to explain in much greater detail the nature and adequacy of these methods. It remains unclear from this review whether the energetic requirements of free-ranging primates could ever be measured accurately. The central question of Oftedal’s chapter is whether physiological requirements in the field predict observed intakes in the field. Thus, do intakes closely match, fall below, or greatly exceed requirements? Oftedal discusses the issue using protein as an example. Because there are few data on the protein requirements of adult primates, Oftedal is forced to estimate protein requirements based on assumptions about the digestibility of protein and about the energy concentration of wild foods. He suggests that if these assumptions are reasonable, then free-ranging primates are usually not protein limited and typically obtain sufficient amounts for growth and reproduction from the leaves they consume. The analysis, however, is based only on the leaves which primates select and ingest rather than on all available leaves. In other words, the analysis takes the animal’s selectivity in choosing foods entirely for granted. I suggest that a further question of interest is whether Oftedal’s conclusion holds in relation to all leaf species, such that the the protein content of all non-eaten leaves is also higher than required. If this conclusion holds true, then in principle animals could meet their protein requirements by feeding a t random. This result would be interesting because in fact, howling monkeys and baboons deviate from a random feeding pattern and appear to select high protein items. One implication of Oftedal’s review is that there may be gross errors in the measurement of the energy content of uneaten “potential” foods. It would be useful in a future report to examine the consequences of measurement errors for approaches based on optimal foraging theory. Although substantial errors might seem to undermine the practicability of approaches which assume that animals maximize their long-term rate of energy intake, the relative importance of the energy content of single items depends critically on the state of other ecological variables. The potential energy gain from including food type X in the diet is not only a matter of the chemical composition of single items; it also depends on morphological variables such as shell hardness and on spatial variables such as the number of items per patch [Leighton, 19931. For example, the median number of figs per plant can vary from 8 to 85,000 depending on the species [Leighton, 19931, and the number of items per patch may outweigh modest differences in energy value. In sum, the relative importance of nutritional measures versus patch size and other variables for making theoretical predictions of behavior is in need of clarification. Two papers on African apes are included for possible insights into the diet of Primate Foraging and Diet / 157 the most recent ancestor shared by humans and nonhuman primates. These are specialized data papers rather than broad reviews. Wrangham, Conklin, Chapman, and Hunt conclude from fecal analyses that Kibale forest chimpanzees respond to shortages of tree-fruit by increasing their intake of piths from terrestrial herbaceous stems. The authors hypothesize that piths provide a n important source of energy from fermentable fiber. They speculate that differential reliance on piths was correlated with the divergence of thin-enamelled African apes from other, thick-enamelled hominoids in the Miocene. Tutin, Fernandez, Rogers, Williamson, and McGrew present findings on diet from a seven-year study on sympatric lowland gorillas and chimpanzees in Gabon. Again, most of the analysis is based on fecal samples. At the Lope Reserve, both chimpanzees and gorillas are generalized, opportunistic frugivores. There is extensive dietary overlap, with more than 90%of eaten fruit species shared in common. The authors discuss the notions that among sympatric frugivores, dietary divergence is greatest when succulent fruit is scarce and that such divergence between gorillas and chimpanzees a t Lope is due t o the ability of gorillas to survive on a n almost exclusively folivorous diet. In contrast to Wrangham e t al., Tutin e t al. do not draw special attention to the role of piths as compared to leaves or seeds in explaining chimpanzee responses to fruit scarcity. Baboon diet is covered by Whiten, Byrne, Barton, Waterman, and Henzi to illustrate how a medium-sized catarrhine adapts its food selection patterns to savannah habitats “similar to those exploited during important phases of hominid evolution.” The paper provides a clear, interesting descriptive-analytic approach to identifying combinations of specific food components (protein, lipids, fiber, phenolics, and alkaloids) which jointly influence diet selection. This report illustrates the use of discriminant analysis. The method of comparing the nutrient content of closely related plant species which are eaten versus not eaten deserves careful attention. The second section, “evolution of hominid foraging and diet,” is intended to characterize the transition from the diet last shared with other primates (as described in the first section) to the diet of human hunter-gatherers (as described in the third section). A review by Andrews and Martin infers hominrlid dietary evolution from tooth enamel thickness and, to a lesser extent, from microwear patterns. The authors provide the first published data on enamel thickness in Proconsul africanus and P. major and new data on Dryopithecus, Oreopithecus and Graecopithecus. According t o Andrews and Martin, however, the confidence placed in their own dietary interpretations is limited by a relative lack of fossil material for the time of the human and African ape divergence and by a degree of uncertainty over the functional significance of thick enamel. A report by Blumenschine examines nutritional aspects of scavenging in early humans and the question of whether transport and sharing of carcasses occurred on a regular basis. Data on carcass consumption sequences by living carnivores, and estimates of carcass parts that could have been available to early human scavengers, are used to interpret Plio-Pleistocene archaeological bone assemblages at Olduvai Gorge. The paper assumes a fair degree of familiarity with the topic. if not a working knowledge of the author’s prior studies. Additional explanation of methods would have been useful to help readers interpret the data tables and the many inferences which are made on the basis of indirect evidence. Blumenschine concludes that marrow (fat) yield was more important than flesh (protein) yield in decisions about carcass processing; he provides a discussion of hypotheses on the socio-economic function of archaeological sites. The third paper in section 2 by Foley and Lee treats brain expansion within a n 158 I Menzel ecological framework. The authors examine the energetic costs of encephalization in hominid evolution and how these costs may have been afforded. Foley and Lee discuss meat eating, tool use, and especially a slowing of development rate as possible ways for caretakers t o offset some of the added costs of rearing a larger brained offspring. The paper compares the cumulative energetic costs of brain maintenance in humans, in other hominids and in chimpanzees. Foley and Lee base their calculations on the size of the brain a t birth and at the beginning of each subsequent year, and they assume a stepwise increase in brain size. Recalculating the costs as integrals of a continuous growth curve would be more accurate and would even strengthen their case. An implicit assumption in this paper is that differences in relative brain size (EQ) among species will correlate nicely with differences in their learning and memory skills, even within the same taxonomic family. This should be regarded as hypothesis rather than as established fact. No relevant experimental data on cognitive performance are presented, and speciesspecific capabilities may not be easy to arrange in rank order along a single quantitative scale of measurement. The authors would probably agree that a careful characterization of the diversity of learning and memory skills in primates is a necessary half of any anatomical explanation. The third section, “food of hunter-gatherers,” begins with a review of traditional diet in Australian aboriginal hunter-gatherers. ODea reviews how traditional dietary patterns have contributed to chronic diseases in Aborigines after westernization. Next, Hawkes, O’Connell and Blurton Jones describe an experimental study on the benefits of large game versus small game hunting in the Hadza of northern Tanzania. They ask why men specialize in the hunting of big game even though 1) men obtain meat for their family more consistently by taking small game and 2) men are allowed to take meat from big game kills even if they do not regularly contribute t o the kills. Hawkes et al. provide a game-theoretic analysis of this “collective action” problem and suggest that the adaptive value of big game hunting in such cases does not lie, as is commonly assumed, in nutritional advantages to hunters and their families. The authors speculate that mating advantages accruing to the hunters might provide the better explanation. Milton presents data on diet in four groups of Amazonian forest-dwellers. The systems Milton describes are complex, and the report appears to be an initial effort to identify patterns and to raise hypotheses for future consideration. Milton suggests that there are no single-factor environmental explanations for differences in the primary crops used and in the animal types hunted and that “more attention should be paid t o historical factors. . . local environmental conditions and general patterns of inter- and intra-group cultural dynamics.” Speth briefly reviews data suggesting “the existence of an upper safe limit to total protein intake in pregnancy” in humans and calls for comparative data on protein selection and avoidance strategies in chimpanzees. The fourth section, entitled “human diets: prehistory to present day,” gives accounts of dietary change beginning with the development of agriculture. Ulijaszek reviews the nutritional consequences of the shift from hunting and gathering to animal domestication and crop cultivation. Southgate presents a variety of data on human food composition. Widdowson characterizes nutritional and energetic deficiencies in modern humans. In the last two papers there is little discussion of how evolved or acquired dietary patterns determine food choice and affect health in modern environments. In conclusion, this volume provides a valuable overview of some current research topics on natural diet and nutrition. I recommend it to anyone working on primate foraging or human diets. The fact that wild primates show as few defi- Primate Foraging and Diet / 159 ciency diseases as they do implies that they are capable of picking up a wealth of information about the value of potential foods. My criticism of the present collection is that there is relatively little concrete discussion of the specific behavioral tendencies and forms of “knowing” which contribute to nutritional well-being in nonhuman primates. Some further characterization of the environment in behaviorally relevant terms is desirable. Even if one could describe the spatial array of available calories and of digestible nutrients in the habitat, this would fail to describe the information which directly guides many aspects of foraging. It seems critical, for example, to specify the types of visual information available in the structure of the habitat for discerning the location and properties of potential foods and to show how different species pick up this information. Primates must also assess the value of environmental opportunities in relation to present or future requirements. Some nutritionists might be less intrigued by behavior which “anticipates” and circumvents deficiencies by means of greatly exceeding the minimum nutrient requirements than by the ability of primates to remedy imposed internal deficiencies through changes in diet. The latter abilities, which appear more “reactive” than anticipatory, remain largely unexplored in primates and are of great interest. Nevertheless, if the design of a nutrient deprivation experiment sharply restricts the animal’s sources of environmental information about changes in food quality and simultaneously limits its feeding options, this can be regarded as examining a special case of dietary choice, and the degree to which it models foraging tasks and the operation of perceptual systems in the wild should be examined carefully. Clearly, feeding is more than nutrition. Feeding patterns do not always closely match nutrient requirements or immediate nutritional consequences, as Hawkes et al. point out. The extent to which nutrient requirements predict preferences and activity patterns a t the level of the whole animal remains an open question, and the behavior of choice must be brought more into the picture. ACKNOWLEDGMENTS The writing of this review was supported by Swiss National Science Foundation grant 31.27721.89. Charles R. Menzel Ethology and Wildlife Research Institute of Zoology University of Zurich-Irchel Zurich, Switzerland REFERENCE Leighton, M. Modeling dietary selectivity by Bornean orangutans: evidence for integration of multiple criteria in fruit selection. INTERNATIONAL JOURNAL OF PRIMATOLOGY 14:257-313, 1993.