Human Diet: Its Origin and Evolution [1 ed.] 0897897366, 9780897897365

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Human Diet

Human Diet Its Origin and Evolution

EDITED BY Peter S. Ungar and Mark F. Teaford

BERGIN & GARVEY Westport, Connecticut • London

Library of Congress Cataloging-in-Publication Data Human diet : its origin and evolution / edited by Peter S. Ungar and Mark F. Teaford. p. cm. Includes bibliographical references and index. ISBN 0–89789–736–6 (alk. paper) 1. Prehistoric peoples—Food. 2. Hunting, Prehistoric. 3. Agriculture, Prehistoric. 4. Hunting and gathering societies. 5. Diet—History. I. Ungar, Peter S. II. Teaford, Mark Franklyn, 1951– GN799.F6H85 2002 930.1—dc21 2001043790 British Library Cataloguing in Publication Data is available. Copyright © 2002 by Peter S. Ungar and Mark F. Teaford All rights reserved. No portion of this book may be reproduced, by any process or technique, without the express written consent of the publisher. Library of Congress Catalog Card Number: 2001043790 ISBN: 0–89789–736–6 First published in 2002 Bergin & Garvey, 88 Post Road West, Westport, CT 06881 An imprint of Greenwood Publishing Group, Inc. www.greenwood.com Printed in the United States of America

The paper used in this book complies with the Permanent Paper Standard issued by the National Information Standards Organization (Z39.48–1984). 10 9 8 7 6 5 4 3 2 1

For Diane, Rachel, and Maya, and Karen, Kelly, and Michael

Contents

1. Perspectives on the Evolution of Human Diet Peter S. Ungar and Mark F. Teaford

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2. Evolution, Diet, and Health S. Boyd Eaton, Stanley B. Eaton III, and Loren Cordain

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3. Post-Pleistocene Human Evolution: Bioarcheology of the Agricultural Transition Clark Spencer Larsen 4. Early Childhood Health in Foragers Sara Stinson 5. Meat-Eating, Grandmothering, and the Evolution of Early Human Diets James O’Connell, Kristen Hawkes, and Nicholas Blurton Jones 6. A Two-Stage Model of Increased Dietary Quality in Early Hominid Evolution: The Role of Fiber Nancy Lou Conklin-Brittain, Richard W. Wrangham, and Catherine C. Smith

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7. Plants of the Apes: Is There a Hominoid Model for the Origins of the Hominid Diet? Peter S. Rodman

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8. Hunter–Gatherer Diets: Wild Foods Signal Relief from Diseases of Affluence Katharine Milton

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9. Hominid Dietary Niches from Proxy Chemical Indicators in Fossils: The Swartkrans Example Julia Lee-Thorp

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10. Paleontological Evidence for the Diets of African Plio-Pleistocene Hominins with Special Reference to Early Homo Mark F. Teaford, Peter S. Ungar, and Frederick E. Grine

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Bibliography

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Index

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About the Editors and Contributors

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Chapter 1

Perspectives on the Evolution of Human Diet Peter S. Ungar and Mark F. Teaford

“You are what you eat.” The adage is so commonly used nowadays that people rarely think about its implications. In essence, “diet” is a key to understanding our past, present, and future. Much of the evolutionary success of our species can be attributed to our ability to procure, process, and consume a wide range of foods. However, recent changes in our diet (e.g., increased intake of such things as saturated fat, refined carbohydrates, and sodium, and decreased intake of nonnutrient fiber) may lie at the root of many of the health problems swamping our health care systems (O’Dea and Sinclair, 1983; Angel, 1984; Eaton and Konner, 1985; Hamilton, 1987; Eaton et al., 1988a,b; Burkett and Eaton, 1989; Cohen, 1989; Eaton et al., 1997). Moreover, if we are to understand and successfully cope with the world population pressures and potential food shortages looming on the horizon in the next century, we need every bit of information we can gather on diet and its influence on our lives. Fortunately, over the past few decades, there has been a veritable explosion of data generated by scientific research. This has brought a flood of new information to the study of what we eat, how we eat, and why we eat it, and it has included data from a variety of fields, ranging from studies of traditional peoples, nonhuman primates, human fossil and

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archeological remains, nutritional chemistry, evolutionary medicine, and others. The problem is that, with this range of perspectives, researchers have often traveled in different circles, with one group being unaware of the other’s recent work. Nutritional anthropologists, ethnographers, physiologists, primatologists, functional morphologists, and paleontologists are all key to monitoring what we eat; how we eat, and why we eat what we eat. On the one hand, such subdivisions of expertise give some indication of the variety of interests and approaches that can be brought to bear on the topic of the evolution of human diet. On the other hand, no one perspective can convey the complexity of the topic—we need insights from every possible perspective. Unfortunately, by its very complexity, such an array of approaches is hard to pull together into a coherent whole, for, as data analyses and applications become more specialized, researchers become more narrowly focused and isolated. This book follows from a symposium that brought together researchers with different approaches to the study of the evolution of human diet. The symposium, entitled “Origins and Evolution of Human Diet,” was held at the Fourteenth International Congress of Anthropological and Ethnological Sciences. The idea was to bring together people schooled in a variety of academic disciplines so that we might begin to build a more complete view than any one perspective would allow. As Eaton and coauthors (1997) wrote, “to reconcile current nutritional recommendations with the nutrition which shaped our metabolic needs during our evolution, [we need] a comprehensive integration of multiple dietary variables.” CONTENTS OF THIS VOLUME This volume has two principal objectives. The first is to address the question, “why study the evolution of human diet?” How can an understanding of food preferences of our distant ancestors help us today? Chapters by Eaton and coauthors, Larsen, Stinson, and Milton each address these questions directly by examining aspects of evolutionary medicine as it relates health to nutrition. These authors each show links between recent changes in our diets on the one hand, and disease and malnutrition on the other. The second goal of this volume is to demonstrate the principal methods used to reconstruct the diets of our earliest ancestors. Some workers use direct analogy to model the diets of fossil hominids using living traditional peoples (see chapters by Stinson, O’Connell and coauthors, and Milton) and extant nonhuman primates (see chapters by Conklin-Brittain and coauthors, Rodman, and Milton).

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Others study the bones and teeth of human ancestors themselves for clues to their diets (see chapters by Larsen, Lee-Thorp, and Teaford and coauthors). Diet and Health Eaton, Eaton, and Cordain start the discussion with a consideration of the discordance between the diets of human ancestors and those of industrialized peoples today. They argue that many of our medical problems result from this discordance, as diet changes have far outstripped the capacity of genetic evolution to keep pace with changes in what we eat today. Recent increases in saturated fat, high glycemic index carbohydrates, and sodium, together with unbalanced intakes of polyunsaturated fatty acids and other important nutrients, can be linked with health problems afflicting industrialized societies. Larsen’s review of bioarcheological evidence details effects of the transition to agriculture on the bones and teeth of our ancestors. Resulting diet changes have led to a general decline in health, an increase in infection, dental disease, and physiological stress, and alterations in growth and development. This underscores the importance of knowing the diets that preceded the cultivation of cereals and the domestication of animals; that is, reconstructing the foods we evolved to eat. Stinson’s chapter also tackles relationships between nutrition and health, but focuses on children. Her examination of !Kung and Ache children shows that slowed growth and high mortality rates are highly correlated with nutritional status. As reproductive status ultimately depends on individuals surviving to adulthood, Stinson argues that evolutionary medicine should include studies of children. Reconstructing Early Hominid Diets O’Connell, Hawkes, and Blurton Jones begin this section of the book by using modern hunter–gatherers as analogs for the ancestral human diet. They note that Hadza children rely largely on plant foods gathered by mothers and grandmothers. They then argue that certain unique aspects of the human life histories (for example, long postmenopausal life spans, long childhoods, and high fertilities) might already have been present in Homo erectus. These are then linked with an emphasis on the gathering and consumption of underground storage organs (e.g., tubers)—not with hunting and the consumption of meat, as is so often portrayed in textbooks. They claim that the technology to produce digging sticks, evidence of fire, and the coincidence of the distribution of

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H. erectus and historic foraging economies based on tuber use are consistent with the exploitation of tubers. Conklin-Brittain, Wrangham, and Smith also suggest that underground storage organs might have been important food resources for early hominids, turning this time, however, to living chimpanzees as analogs. Data on the nutritional ecology of modern chimpanzees are used to speculate on both the macronutient compositon of the australopithecine diet and on the mix of plant parts these hominids might have exploited to obtain these nutrients. While chimpanzee protein needs are limited, their fiber intake is high compared with modern humans. Conklin-Brittain and coauthors project that australopithecines would have had an intermediate level of fiber, such as would be available with the inclusion of underground storage organs in the diet. Rodman also uses a comparative approach, suggesting that plant families consumed by all living great apes would likely also have been eaten by early hominids. Rodman develops a list of common food sources and establishes some boundaries that may help us define, if not limit, the early hominid common ancestor dietary adaptation. Milton rounds out the discussion of comparative methods, proposing that analyses of digestive physiology of humans and nonhuman primates may provide another key to understanding the evolution of human diet. Her nutritional analysis of wild foods routinely consumed by living nonhuman primates and of domesticated foods eaten by humans today show some important differences that may help explain some of the health problems identified by Eaton and coauthors, Stinson, Larsen, and others. The final two chapters look directly to the fossils themselves for evidence of early hominid diet. First, Lee-Thorp considers new chemical analyses of the bones and teeth of the early hominids. She describes studies of carbon, oxygen, and strontium isotopes, as well as ratios of strontium to carbon in the bones and teeth of South African hominids. Taken together, her data suggest the consumption of open veldt resources (including some animal foods) by the early hominids. Finally, the chapter by Teaford, Ungar, and Grine reviews the craniodental evidence for diets of the early hominids. We consider commonly examined aspects of functional anatomy such as tooth size and shape, and enamel thickness and jaw biomechanics. Changes in the teeth and jaws of these species through the Plio-Pleistocene suggest changes in material properties of foods eaten by the hominids. For example, a broadening of the dietary niche to include harder, more brittle foods is evident in the “gracile” australopithecine lineage through the Pliocene. These data suggest that the trend toward harder, more brittle foods continued

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for australopithecines through the Pleistocene, whereas inclusion of more soft, tough foods, such as meat characterized the diets of the earliest members of our own genus, Homo, undoubtedly with the aid of tools. DISCUSSION Several of the chapters in this volume suggest that many common health problems relate to a discordance between what we eat today and what our bodies have evolved to eat. Should we return to the diets of our ancestors? If we do, which hominid species should we use as a model for what we should eat? The studies presented here consider taxa ranging from the last common ancestor of apes and humans to modern apes and modern humans. Where along the continuum do we look? One answer might be to consider diets just prior to the agricultural revolution—the major shift that led to many of the health problems we see today. The problem with this approach, however, is that there was no single dietary regime that characterized preagricultural peoples. One of the hallmarks of our species is the variety of foods we can eat. Thus, our “species-specific” dietary adaptation (Sussman, 1987) seems to involve the consumption of many foods. Even in the past, people lived in a wide range of environments and made use of a broad spectrum of resources. This ability stems in part from biological adaptation and in part from cultural innovations to procure, process, prepare, and store foods (McGee, 1984; Stahl, 1984; Toth, 1985; Ulijaszek, 1991; Stiner and Kuhn, 1992). We submit that the key to understanding our unusual dietary breadth rests in the study of the evolution of human diet. Evidence suggests that we began to evolve our unique ability to take a broad spectrum of foods more than four million years ago, shortly after our evolutionary split with chimpanzees. Thickened dental enamel and jaws, larger, flatter teeth, and other biological innovations increased the range of foods that our earliest ancestors could process. The earliest preserved tools suggest that cultural innovations were also key, allowing later hominids access to foods that they would not otherwise have been able to procure or process. If our dietary variability has evolved through time, we must examine the paleobiology of all of our immediate ancestors to understand it. Our ability to make use of such a broad range of resources has in many cases evolved more quickly than our biology. This, in turn, has led to many of the health problems alluded to in this volume. Thus, its significance cannot be overstated. Our dietary adaptations have allowed us a measure

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of success unrivaled in the primate order. We have spread to the ends of the earth, and our population has increased at a record pace. These are two of the most common measures of evolutionary success. What about other measures of evolutionary success, such as increased lifespan and species longevity? The answers may well depend upon diet. The study of the evolution of human diet can teach us many things about what we should be eating. The first lesson is that variety can be a good thing. We evolved to eat a broad range of foods, so no single food item is a panacea. Studies of human remains from the time of the agricultural transition teach us that a diet restricted to only a few staple foods, such as cereal grains, is a poor-quality diet that relates directly to a decline in general health. Recent fad diets emphasizing one food item or another are also problematic. For example, high-protein diets have been said to facilitate kidney failure (Klahr, 1989; Pedrini et al., 1996; Hammond and Janes, 1998) and high soy intake, vegetarian diets have been associated by some with enlargement of the pancreas (Liener, 1994) and iron deficiency (Shaw et al., 1995). On the other hand, variety is not necessarily a good thing if left unchecked. Our ability to procure, process, and consume such a wide range of foods comes with a burden of choice. Many of us have chosen to consume foods containing more sodium, saturated fat, and refined carbohydrates and less non-nutrient fiber than eaten by most preagricultural peoples (O’Dea and Sinclair, 1983; Angel, 1984; Eaton and Konner, 1985; Hamilton, 1987; Eaton et al., 1988a,b; Burkett and Eaton, 1989; Cohen, 1989; Eaton et al., 1997). Resulting health problems have been well documented and are summarized in several chapters in this book. These problems stand as roadblocks to future increases in our lifespan. At the same time, human population increases have fueled an almost insatiable appetite for arable land, resulting in the destruction of many environments. How can we persevere in the face of such problems? Studies of the evolution of human diet may provide some of the answers.

Chapter 2

Evolution, Diet, and Health S. Boyd Eaton, Stanley B. Eaton III, and Loren Cordain

The nutritional requirements of contemporary humans represent the end result of dietary interactions between our ancestral species and their environments extending back to the origins of life on earth. Primates of modern aspect are thought to have emerged about fifty million years ago, and appreciating the basic range of primate nutritional patterns over this lengthy evolutionary period is critically important; only when the original simian baseline is characterized can subsequent dietary modifications within the hominid lineage be fully appraised. These nutritional changes have had significant evolutionary impact in the past, and they now affect the health of contemporary human populations. The nature of these interactions can best be understood when the dietary alterations are measured against a fundamental primate benchmark. THE PRIMATE BASELINE With regard to diet, what students of human evolution and advocates of evolutionary medicine need most from paleoprimatologists is an estimate of the nutritional pattern likely to have characterized the last common ancestor of apes and humans—a hypothetical species thought to have existed in Africa between seven and five million years ago.

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If members of this elusive taxon were like current chimpanzees and bonobos, plant foods such as fruits, leaves, gums, and stalks probably comprised at least 95% of their dietary intake, with insects, eggs, and small animals making up the remainder (Milton, 1993; Tutin and Fernandez, 1993). The general nutritional parameters of an eating pattern along these lines can be estimated with modest confidence, although certainly not with mathematical exactitude. Protein would have contributed a greater proportion of total energy than it does for most contemporary humans, but with much more from vegetable sources than from animal sources (Popovich et al., 1997). Simple carbohydrate intake would have been less than at present, coming mainly from fruit. Little or none came from refined flour and sugar, leading sources for current humans. While there would have been relatively more starch and other complex carbohydrates, total carbohydrate contribution to dietary energy would have roughly equaled or, more likely, been somewhat less than is typical in today’s affluent nations. Dietary fiber would have exceeded current levels by an order of magnitude: 200 grams versus 20 grams a day (Milton, 1993). Colonic fermentation of this fiber, by gut flora, probably made a significant contribution to daily energy intake because the resultant volatile short-chain fatty acids are subsequently metabolized by intestinal epithelium and, especially, in the liver. Their contribution to overall energy must have been significant, perhaps 20%– 30% of daily calories (Bergman, 1990). Daily intake of vitamins and minerals is likely to have been considerably greater than at present, with the likely exception of iodine, consumption of which would have varied with geographic location according to oceanic proximity, volcanic activity, prevailing winds, and rainfall. As it is for all other free-living terrestrial mammals, sodium intake would have been only a fraction of that currently consumed and would have been substantially less than that of potassium (Denton et al., 1995). Availability of phytochemicals, like that of vitamins and most minerals, would in all likelihood have been substantially greater than for modern Americans and other westerners. Total fat intake, especially of serum-cholesterol-raising saturated and trans fatty acids, must have been greatly below current American and European levels; cholesterol intake would have been minimal. Within the polyunsaturated fatty acid (PUFA) category, partition between the omega 6 and omega 3 (ω-6 and ω-3) families would have been reasonably equal or skewed slightly toward the ω-3s. Polyunsaturated fatty acids from plant sources are predominantly, if not exclusively, 18 carbons or less in chain length; linoleic acid (LA, C18:2, ω-6) and α-linolenic acid (ALA, C18:3, ω-3) are typical. Accordingly, dietary intake of the longer-chain C20 and C22 PUFAs, such as arachidonic acid (AA, C20:4,

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ω-6) and docosahexenoic acid (DHA, C22:6, ω-3), would have been low (Eaton, 1998). SCAVENGING, HUNTING, AND BRAIN EXPANSION Paleodental evidence suggests that after the divergence of early hominids from the hominoid ancestral line, a gradual increase in consumption of harder and/or more abrasive foods—most likely nuts and seeds— occurred. This change probably increased intake of vegetable fat (mostly non-serum-cholesterol raising in nature) and would probably have facilitated overall access to food energy. About 2.5 million years ago, there is evidence that animal foods began to occupy an increasingly prominent place in our ancestors’ subsistence. Decreased molar size, less mandibular and cranial robusticity, and alterations in incisor shape all suggest greater emphasis on foods requiring less grinding and more tearing, such as meat. An increasing proportion of meat in the diet would obviously have provided more animal protein, a factor perhaps related to the stature increase that appears to have accompanied the transition from australopithecines through Homo habilis to Homo erectus (McHenry, 1992), but greater availability of animal fat was probably a more important dietary alteration. Even crude Oldowan stone tools would have allowed early humans access to brain and marrow from a broad range of animals obtained by scavenging or hunting—including some species larger than those from which chimpanzee hunters avidly extract brain tissue and marrow fat. Chimpanzee males do most of the hunting, making over 90% of all kills, but they commonly exchange meat for access to sexually receptive females (Stanford, 1995). Carcass fats were probably prized by the early hominids as they are by recently observed modern human hunter–gatherers (Stefansson, 1960). More animal fat in the diet increased caloric density (which may have been another factor related to the concurrent stature increase) and, in addition, provided a source of ready-formed long chain PUFAs, including AA, docosatetrenoic acid (DTA, C22:4, ω-3), and DHA. These three fatty acids together make up more than 90% of the long-chain PUFAs (i.e., the structurally significant and physiologically active fat) found in the brain gray matter of all mammalian species (Sinclair, 1975). A cardinal feature of human evolution has been development of increasing brain size: the cranial capacity of Homo sapiens is thrice that of Australopithecus afarensis. A prime selective force driving this increase was almost certainly the complex nature of social interactions among early hominids (Dunbar, 1998). There is, however, no a priori reason

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to assume that such interactions, at first, differed much from those of chimpanzee and gorilla ancestors. Social complexity was thus a necessary, but insufficient, selective pressure acting to increase brain size. Another necessary factor was probably adequate dietary substrate to allow formation of brain tissue (Crawford, 1992). The limiting raw materials, AA, DTA, and DHA, could have been provided by animal tissues as hunting and/or scavenging activities assumed greater importance in human subsistence (Eaton, 1998). Increasing complexity of interpersonal and social interactions, together with availability of animal tissues—to provide the necessary structural lipid—constituted a unique psychonutritional nexus that may explain human brain expansion. Dramatic nutritional, anatomic, and behavioral changes accompanied hunting and scavenging, division of labor by sexes, increased day range, reduced sexual dimorphism, decreased gut size, greater stature, and increasing brain size (Leonard and Robertson, 1994; Aiello and Wheeler, 1995). It is important to recognize, however, that these changes were gradual. H. habilis evolved into H. erectus over the course of several hundred thousand years, and this rate of cultural change, in all likelihood, allowed for concomitant genetic modification. The behavior, subsistence, and biological characteristics of anatomically modern Late Paleolithic humans differed strikingly from those of H. habilis, but these changes developed over a 2.5 million-year period. In contrast, subsequent comparably dramatic changes in both behavior and subsistence have occurred with far greater rapidity, almost certainly overmatching the capacity of genetic evolution to keep pace. THE NEOLITHIC DIET Adoption of agriculture and animal husbandry, while perhaps not explosive enough to justify being termed a “revolution,” nevertheless generally required only a few thousand years and, in some cases, only a few hundred years. Genetic evolutionary responses must have been evoked by the altered circumstances, but given the time frame, only high-order selective pressures (e.g., newly appearing epidemic infectious diseases capable of killing young people before the age of reproduction) would have had sufficient time to significantly impact the human genome. The chief dietary innovation that accompanied agriculture involved cereal grains. Earlier humans probably recognized that grains could be consumed in times of shortage; with primitive technology, however, the work involved in milling grains to render them digestible was sufficient to discourage their routine use. When population density reached the

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point that nomadic exploitation of game and wild plant foods became difficult or impossible and Mesolithic humans adopted a more settled way of living, however, utilization of cereals became attractive. Actual crop cultivation followed and, in most areas, cereals became staples. This nutritional departure was unparalleled, as no other free-living primates routinely consume cereal grains (Milton, 1993). Increasing dependence on cereal grains as an energy source decreased dietary breadth and necessarily reduced consumption of fruits and vegetables, which had been prime foodstuffs throughout primate and hominid evolution. The proportion of total food energy obtained by Paleolithic humans from fruits and vegetables (sometimes as many as one hundred different species over the course of a year) varied inversely with latitude, but, except in subarctic regions, almost always exceeded that typical of contemporary diets. Becoming dependent on grains reduced intake of fruits and vegetables, often to 20% or less of total energy intake. Accordingly, access to micronutrients (vitamins, minerals, and phytochemicals) previously supplied by fruits and vegetables was substantially decreased. Of course, cereal grains also provide micronutrients, but not necessarily those to which human biology became accustomed throughout a multimillion-year evolutionary experience, during which fruits and vegetables were the overwhelmingly dominant plant foods. For pastoralists, consumption of animal protein probably continued at approximately Paleolithic levels, but for most agriculturalists, meat was less available than it had been for Stone Agers. This change may have been one factor among the many (e.g., average caloric availability, frequency of food shortages, prevalence of childhood infectious diseases, etc.) that resulted in the stature decrease that accompanied the transition from foraging to agriculture (Cohen, 1989). Less meat, together with cereal grain preponderance, increased the ω-6:ω-3 PUFA ratio and also reduced intake of preformed longer-chain PUFAs, including AA, DTA, and DHA. The fiber available from rice and wheat is predominantly insoluble, while that from fruits and vegetables is mainly soluble; hence, while total fiber intake probably changed little, in the Old World, agriculture generally increased the insoluble:soluble dietary fiber ratio (Eaton, 1990). Further dietary changes that occurred during the agricultural millennia included development of alcoholic beverages, commercial salt production, and the gradual spread of sugar cane cultivation. Each was new in primate and hominid experience, and each has had profound consequences for human health.

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INDUSTRY AND DIET The industrial era and agribusiness have further distanced human nutrition from its primate and Paleolithic antecedents. Roller-milling has reduced the fiber content of cereal grain-based foods so that total fiber intake has plummeted to levels much below those for agriculturalists, hunter–gatherers, or primates (Eaton, 1990). Cold-pressing has facilitated extraction of vegetable oils (e.g., corn, sunflower, safflower) rich in ω-6 PUFA and thereby exacerbated the ω-6:ω-3 imbalance existing in the diets of affluent nations (Simopoulos, 1991). The pricing structure for beef and other commercial meat has, until recently, rewarded breeding and feeding practices that maximize carcass fat deposition. This fat is deposited as an energy reserve, not for structural purposes, so its content of saturated, serum-cholesterol-raising fatty acids is high. Not only do commercial meat animals have more depot fat than do their wild relatives; because they are now fed grain instead of forage, the ω-6:ω-3 partition of their lipid is highly unnatural, with a marked ω-6 excess (Marmer et al., 1984). Foods popular in late twentieth century affluent nations include a profusion of commercially prepared items. Humans are the only free-living species to consume such foods, whose natural origin is obscure, and the entities created by the food industry commonly provide inapparent salt, refined flour, sugar or corn sweeteners, and trans fatty acids in extraordinary concentration. Another characteristic feature of contemporary nutrition is the unprecedented availability of food energy. If there were some way to judge the human effort necessary to obtain a given amount of food energy, citizens of existing Western nations would almost certainly “enjoy” the highest calorie-to-effort return ratio yet experienced by humans and their hominid, hominoid, or primate ancestors. We have “optimized foraging” to an unprecedented degree, and while an advantage in some respects, this capacity has adverse health implications as well. Because energy expenditure and energy intake have been largely uncoupled in contemporary affluent nations, growth and development are unnaturally accelerated while abnormal body composition (hyperadiposity and musculoskeletal deficiency) have become unprecedentedly common. The consequences range from insulin resistance and diabetes to age-related fractures (Eaton, 1998). DIETARY DISCORDANCE AND CHRONIC DISEASES The altered nutritional parameters that differentiate contemporary diets from Paleolithic and primate patterns impact health in many ways,

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some beneficially (e.g., fewer food shortages contribute to greater life expectancy), but many adversely. Five examples of deleterious effects include: 1. Electrolytes and blood pressure. Humans are the only free-living terrestrial mammals that ordinarily consume more sodium than potassium, the only species to commonly experience rising average blood pressure with increasing age, and the only mammals to commonly develop hypertension. Stone Age humans (and higher primates, generally) consumed only one-fourth the sodium average Westerners now do (Eaton, et al., 1997). About 90% of current sodium intake results from food processing, preparation, and flavoring: Only 10% is intrinsic to the foods themselves. Many groups of hunter–gatherers, pastoralists, and rudimentary horticulturalists that lack commercially available salt have been studied in this century. These ancestral human surrogates experience neither rising blood pressure with age nor clinical hypertension (Eaton et al., 1988). 2. Cereal grains and cancer. No primates other than humans ordinarily consume cereal grains, but from the introduction of agriculture onward, grains have been the single most important contributor to human food energy, providing from 40% to 90% of human caloric requirements. In doing so they have displaced fruits and vegetables that, until the Neolithic, had been the dominant energy source for Stone Agers, earlier hominids, and our antecedent primate ancestors for fifty million years. A recent comprehensive analysis, in which 150 scientists reviewed 4,500 research studies, puts this phenomenon into perspective (World Cancer Research Fund and American Institute for Cancer Research, 1997). The influence of dietary variables on eighteen different cancers was assessed. Vegetables were found to exert a convincing preventive effect for five cancers, a probable preventive effect for four others, and a possible preventive effect for another seven. For fruits, the analysis revealed four convincing, four probable, and four possible preventive relationships. But for cereal grains there were no convincing or probable preventive relationships and only one possible preventive effect, and, for one cancer (of the esophagus), grains may possibly have increased risk. In short, the best available evidence suggests that vegetables and fruits have far more cancer-preventing potential than do grains. This probably reflects the phytochemical content of noncereal plant foods, phytochemicals to which current human biology became

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adapted through many million years of evolutionary interrelationships. The phytochemicals of grains have interacted with the human genome for only ten thousand years. Hence, substitution of grains for vegetables and fruits in human diets might readily diminish our resistance to development of neoplastic disease. 3. Energy intake:output uncoupling and insulin resistance. For primates and other mammals in natural settings, food procurement is inextricably linked to energy expenditure, a relationship that establishes a range of body compositions appropriate for any given species. The ratio of fat to muscle generally varies with season, but typically lies within fairly narrow limits; hyperadiposity, as it exists for many contemporary humans, is rare or nonexistent for other primates. The necessity for physical exertion, unavoidable for most humans until the industrial era and, especially, the twentieth century, ensured substantial muscularity in the proportionate range existing for current free-living nonhuman primates. In the present, however, obtaining food energy is no longer dependent on muscular exertion: From childhood on, calories are available at the lowest cost in human experience without reciprocal energy expenditure. The result is relative sarcopenia—deficiency of skeletal muscle. For many individuals in affluent nations, the proportions of adipose tissue and skeletal muscle are grossly out of line with those during prior evolutionary experience. Both fat and muscle take up glucose from the blood in response to insulin stimulation, but the capacity of muscle in this regard far exceeds that of adipose tissue per unit weight (DeFronzo, 1997). Existing control mechanisms for carbohydrate homeostasis were established over evolutionary time, during which ancestral body composition almost never approached the extremes of hyperadiposity and sarcopenia manifested by many contemporary humans. For such individuals, a given insulin secretory pulse, in response to a carbohydrate-containing meal, now produces less reduction in blood glucose levels than would have been achieved for prior humans with evolutionarily “appropriate” body composition. Additional, “extra” pancreatic insulin secretion is required to produce glucose homeostasis. This constitutes functional insulin resistance, a pathophysiological state exacerbated by low muscular metabolic activity (another result of exercise deficit) (Eaton and Eaton, 1998). In genetically susceptible individuals, the process can proceed to glucose intolerance and overt diabetes. Prevalence of type 2 diabetes (that related to insulin resistance and by far the most common form) has multiplied ten-fold in the United States

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since the 1930s (American Diabetes Association, 1996), as the increasing disconnection between caloric accessibility and energy expenditure has produced an ever-larger number of obese, sarcopenic Americans. 4. Dietary fat and coronary heart disease (CHD). While many other dietary, behavioral, and genetic factors influence the inception and progression of coronary heart disease, hypercholesterolemia is a paramount contributor. Recently studied hunter–gatherers have serum total cholesterol levels averaging 125 mg/dl (Eaton et al., 1988b), a value within the range for free-living nonhuman primates (Eaton, 1992). Human societies with similar average total serum cholesterol levels have vanishingly low prevalences of CHD. Americans and other affluent westerners, conversely, have average total serum cholesterol values exceeding 200 mg/dl—well outside the “natural” primate range. For these populations, CHD is the single leading cause of mortality. Evidence linking dietary fat to total serum cholesterol concentrations is incontrovertible: The prime agents are saturated and trans fatty acids. For ancestral humans, the cholesterol-raising saturated fatty acids constituted about 5% of total energy intake, and trans fatty acid intake was negligible. For Americans, cholesterolraising saturated fatty acids approach 15% of dietary energy, while hydrogenated vegetable fats and oils provide an unprecedented quantity of trans fats (Eaton et al., 1997). The ω-6:ω-3 imbalance in current Western diets also affects coronary disease. Excessive ω-6 AA relative to ω-3 DHA and eicosapentenoic acid (EPA, C20:5, ω-3) adversely affects platelets and arterial walls to promote development of coronary atherosclerosis (Wood et al., 1992). The more balanced ω-6:ω-3 dietary PUFA intake of Paleolithic humans would have minimized this effect. 5. DHA deficiency and the brain. While human cranial capacity tripled over the 2.5 million years after H. habilis first appeared, this trend has recently reversed. Since peaking among Cromagnons and other humans living during the Late Paleolithic, cranial capacity has fallen off approximately 11% (Ruff et al., 1997). This diminution has paralleled a decrease in consumption of animal foods and, consequently, a diminished dietary intake of preformed longchain PUFAs, the building blocks necessary for the formation of brain tissue. These PUFAs can be synthesized by humans from their eighteen carbon precursors, LA, and ALA, but the process appears too slow to supply the amounts of AA, DTA, and DHA needed for

Human Diet

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optimal brain growth during fetal development and infancy (Woods et al., 1996; Salem et al., 1996). DHA deficiency is especially important; first, because its concentration in brain tissue exceeds those of AA and DTA and, second, because our current ω-6 excess tends to promote formation of long-chain ω-6 AA and DTA while inhibiting synthesis of ω-3 DHA. Association is not necessarily causation, but the fluctuations that have occurred in brain size over evolutionary time—both increases and decreases—correlate well with dietary intake of the preformed long-chain PUFAs necessary for formation of brain tissue. It is therefore tempting to speculate on a causal relationship. Current ω-6:ω-3 imbalance, together with absolute dietary DHA intake quite low from a human evolutionary perspective, may be relevant to the frequency of unipolar depression, a debilitating neuropsychiatric disorder that accounts for more “disabilityadjusted lost years” in the total world population than heart attacks, lung cancer, or AIDS (Murray and Lopez, 1996). Prevalence of depression has increased substantially during the twentieth century (Klerman and Weisman, 1989; Weisman et al., 1996), while dietary intake of ω-6 PUFAs has soared relative to that of ω-3 PUFAs, primarily because of increased vegetable oil consumption and corn feeding of commercial meat animals. Fish are good sources of ω-3 PUFAs (including DHA), and national fish consumption is inversely correlated with national rates of depression (Hibbeln and Salem, 1997). Furthermore, studies of plasma ω-6:ω-3 ratios in patients with depression reveal a direct association: Higher ratios of ω-6 to ω-3 PUFAs are correlated with more frequent and severe depressive episodes (Adams et al., 1996; Hibbeln et al., 1997). Early therapeutic trials with ω-3 PUFAs have shown symptomatic improvement (Hibbeln and Salem, 1995). These findings are preliminary and, as yet, only suggestive, but their implication is that an ω-6:ω-3 dietary ratio (and perhaps magnitude) similar to that which obtained throughout human evolutionary experience may be an integral component of mental health. CONCLUSION Deviations from the postulated ancestral primate nutritional baseline have had important evolutionary impact and appear to influence human health in the present. Because of these significant relationships, better understanding of primate nutritional patterns would be desirable. The diets of Miocene and Pliocene apes are particularly relevant, and the goal

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would be to estimate as accurately as possible the nutrition of the last common ancestor of existing pongids and humans. Toward this end, establishing relationships between dentition and nutrient intake would be extremely valuable. While folivorous primates presumably exhibit interspecific nutritional variation, there may be generalizations about such diets that are valid across broad subsistence categories. Bioarcheology, assessing lifetime experience from archeological sites and skeletal–dental remains, may aid in assessing primate diets through evolutionary time. Craniofacial adaptations as well as isotopic and elemental dietary “signatures” may provide important clues (Larsen, 1997). Another area of necessary research involves proximate analyses of the foods consumed, by primates, generally, and by pongids, especially. In order that these can be conveniently related to current and past human nutrition, the analyses should provide wet weight data. Both macronutrient and micronutrient compositional values will be helpful, including analyses not commonly performed (e.g., individual lipid species). Once a sufficient body of proximate analyses for the plant foods, insects, and small mammals consumed by primates has been assembled, and the proportions of such foods making up differing primate diets are determined, modeling representative average nutritional intake for primates with varying subsistence patterns should become possible. In turn, this information will permit estimation of the last common ancestral diet. The above research “wish list” is a tall order, but the potential for expanding understanding of primate, hominoid, hominid, and human evolution, together with the benefit of health promotion based on evolutionary medical principles, should provide more than sufficient incentive for the investigational effort.

Chapter 3

Post-Pleistocene Human Evolution: Bioarcheology of the Agricultural Transition Clark Spencer Larsen

Within a remarkably short period of time following the Pleistocene— when climate, vegetation, and fauna became essentially modern—human populations worldwide adopted plant cultivation as a subsistence strategy. The shift from foraging to farming occurred in at least seven different centers of domestication around the world, and the circumstances for the change are different from place to place (Smith, 1995). Perhaps the widespread extinction of various megafauna and other resources at the end of the Pleistocene may have been an impetus for human populations to begin to develop wholly new means of acquiring food in order to meet protein, fat, and energy requirements. Alternatively, the new environments simply created circumstances for new varieties of plants and animals that naturally lent themselves to domestication by humans. Whatever the cause for this remarkable change in subsistence practices, the change in the means of acquiring food—from collection to production—had profound implications for nutritional ecology, health, and behavior in human beings. This chapter focuses on the growing record of research based on the study of ancient skeletons worldwide and how these skeletons help to document and interpret human biology and health in the post-Pleistocene

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world. One question is addressed: What was the impact of this major dietary shift on humans, especially regarding their well-being and quality of life? For most who have asked this question—scholars and nonscholars alike—the adoption of an agricultural lifeway represented an improvement in the human condition, forming the very foundation of “civilization” and modernity. Specifically, once enlightened humans adopted agriculture, life improved. Farming folk worked less hard, had more spare time and enjoyed better health than their foraging forebears did. Also important, people no longer moved around constantly; rather, with an agricultural base they had the luxury of living in towns and cities where they could bask in the pleasures of civilization. This was the essential “great leap forward, the advance that catapulted us out of the hand-to-mouth, day-to-day existence of hunter–gatherers like the !Kung and Ache and into the complex, cultured, literate existence of modern human beings” (Allport, 2000: 219). Over the last several decades, a large body of evidence has accumulated to show that the above dichotomy between earlier foragers and later farmers is overly simplistic and largely incorrect. Our understanding of hunter–gatherers in particular is now much better informed by a wealth of ethnographic and archeological data (Kelly, 1995). That is to say, foragers—past and present—are far more complex and varied than was previously realized. Indeed, the statement made by Robert Braidwood (1960: 148), that “[b]efore the agricultural revolution most men must have spent their waking moments seeking their next meal, except when they could gorge following a great kill,” seems naive at best. A couple of decades ago, a group of anthropologists began to question the traditional “improvement” model of Holocene dietary change, especially based on the lead provided by various researchers and presented in the pathbreaking “Man the Hunter” conference (e.g., Cohen, 1977; Lee and DeVore, 1968). From my perspective, however, the record that has provided the most comprehensive picture from which to assess quality of life and well-being is that based on the study of archeological human skeletal remains predating and postdating the agricultural transition. Beginning especially with the conference organized by Mark Cohen and George Armelagos in 1982 (Cohen and Armelagos, 1984), and continuing to the present day, a dataset drawn from a variety of settings based on many thousands of archeological human skeletons has been built. Analysis of this growing record has begun to provide an understanding of dietary change and implications for human health in the post-Pleistocene world. This bioarcheological evidence provides the time depth necessary for assessing long-term trends in health. This deep temporal context is an important strength that anthropology brings to

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bear in discussions relating to the emerging picture of the agricultural transition and the history of the human condition. In order to address the above question, this chapter is organized around the following four themes: (1) food composition and nutritional quality; (2) mastication and craniofacial change; (3) sedentism and health; and (4) workload and activity. For each theme, the methods employed by bioarcheologists and others are summarized, and where appropriate, analyses are discussed. FOOD COMPOSITION AND QUALITY OF NUTRITION Bioarcheological Chemistry Valuable information on particular aspects of dietary composition is obtained via analysis of carbon and nitrogen stable isotopes from bone. Field and laboratory investigations indicate that ratios of 12C to 13C (expressed as δ13C values) in bone and other tissues reflect the ratios in diet (Schoeninger, 1995). The variability in values in carbon isotope ratios represents three plant photosynthetic pathways: C3 (CalvinBenson), C4 (Hatch-Slack), or crassulacean acid metabolism (CAM). On average, C4 plants—those adapted to hot and dry climates—have δ13C values that are about 14 parts per million (‰) less negative than C3 plants (plants in temperate climates) and their consumers. Plants with CAM photosynthesis pathways (most cacti and succulents) overlap the values of C3 and C4 plants. Although there are now numerous carbon isotope values determined from archeological skeletons from around the globe, the most comprehensive knowledge about dietary shifts based on isotope analysis is from New World settings, where maize, a C4 plant, was a dominant food in native diets. Maize played a fundamental role in the rise of complex societies prehistorically in the Western hemisphere, and its consumption had important implications for health throughout. The isotopic study of hundreds of bone samples from eastern North America shows when maize was adopted and when it became a central part of diet (Ambrose, 1987; Larsen, 1997). Analysis of stable isotope ratios of carbon indicates that maize played a minimal (or no) role in native diets prior to about A.D. 800. Following that date, maize quickly became a focus of diet, especially after A.D. 1000. Isotopic documentation of maize consumption has also been established in other regions of the New World, including the American southwest, California, Mesoamerica (especially in the Maya), and elsewhere. In the Old World, maize is a post-fifteenth century food, but consumption of other C4 cultigens has been identified in archeological human

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remains. They include millet in central Europe (Murray and Schoeninger, 1988) and northern China (Schwarcz and Schoeninger, 1991) and sorghum in Nubia (White and Schwarcz, 1989). Study of ratios of nitrogen stable isotopes, 14N and 15N, in archeological skeletons also reveals significant patterns of dietary variability in the past, especially regarding consumption of marine versus terrestrial foods, owing to differences in the way that nitrogen enters the biological arena in these different ecological settings. Generally, δ15N values for terrestrial plants are 4 ‰ lower than for marine plants (Schwarcz and Schoeninger, 1991). These differences are passed up the food chain from plant-consuming animals to carnivores, translating into a difference of about 20 ‰ between marine and other aquatic organisms (such as those from lakes and rivers) and terrestrial organisms. Comparisons of δ15N values in coastal populations reveal that dietary patterns are highly localized, with groups living even 5 to 10 km inland having considerably decreased consumption of marine foods (Hutchinson et al., 1998). In several Neolithic coastal settings, isotopic data reveal that food consumption was limited to terrestrial (agricultural) resources, despite close proximity to marine resources (Papathanasiou et al., 2000). Oral Health One of the most profound changes to occur with the foraging-tofarming transition was the widespread decline in oral health, which was almost certainly tied to increased consumption of plant carbohydrates. Especially obvious is the remarkable increase in dental caries in most places where the transition occurred. Dental caries is a disease process characterized by focal demineralization of dental hard tissues by organic acids produced by bacterial fermentation of dietary carbohydrates, especially sugars (Larsen, 1997). Dental caries is manifested as pits (or cavities) in teeth, ranging in size from barely discernible discoloration of enamel to large cavitations or substantial loss of crown matter (Figure 3.1). With a few exceptions, comparisons of the teeth of prehistoric foragers and farmers from many settings globally reveal a consistent pattern of increase in frequency of carious lesions (Larsen, 1995, and reviews cited therein). Eastern North America offers an important perspective on the impact of increased carbohydrate consumption on humans, especially because so many dental samples have been studied from this region. In this region, pre-maize populations have generally less than 5% carious teeth, whereas maize populations have over 15% on average (Larsen, 1997).

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Figure 3.1 Carious lesions in mandibular teeth.

I note that the increase in dental caries may not be universal. In this regard, one important exception to this pattern has been documented in southeast Asia. Study of various prehistoric rice agriculturalists in southeast Asia shows no apparent association between rice consumption and dental caries (Dommett et al., 2000). That is, there is no discernible increase in frequency of carious lesions when rice is introduced to diet. One of the important indicators of periodontal disease in skeletal remains is antemortem tooth loss (Figure 3.2). Periodontal disease results in a weakening of the alveolar bone supporting the dental structures, and as the bone resorbs, teeth loosen and are exfoliated. Although the evidence is not as overwhelming as for dental caries, there is a pattern of increase in antemortem loss that corresponds with cariogenesis in agricultural populations from diverse settings, such as Nubia, eastern North America, western Europe, and southern Asia (reviewed in Larsen, 1995).

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Human Diet Figure 3.2 Extreme case of antemortem tooth loss.

Growth and Development The transition from foraging to farming involved a shift to a subsistence spectrum that became narrow. The narrowing of dietary breadth involved a reduced availability of animal protein in combination with an increased reliance on a limited number of domesticated plants. For most areas, the adoption of cultigens—the so-called superfoods— involved a reliance on one or few plants, such as rice in Asia, wheat in temperate Asia and Europe, millet or sorghum in Africa, and maize in the New World. These plants, especially when they serve as the primary

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part of diet, offer a poor nutritional base. With regard to maize, for example, presence of phytate reduces iron bioavailability, and deficiency of essential amino acids (lysine, isoleucine, and tryptophan) results in poor growth (Food and Agriculture Organization, 1970). Niacin (vitamin B3) is chemically bound in maize, resulting in the reduction of bioavailability of this essential nutrient. Iron absorption is also low in maize-based diets. Milled grains elsewhere in the world are also deficient in iron (e.g., millet and wheat). Even in the unmilled form, rice is deficient in protein. This deficiency also serves to inhibit vitamin A activity (Wolf, 1980). Thus, populations heavily dependent on this plant show a tendency for high levels of iron deficiency anemia and shortened stature. The skeletal indicators of iron deficiency and poor growth consistently show a pattern of poor health in past agricultural populations. Many archeological series have a high prevalence of cribra orbitalia and porotic hyperostosis. These are lesions associated with increased red blood cell production due to iron deficiency anemia (Figure 3.3). The skeletal changes are caused by an expansion of the blood-forming tissues, mostly in the cranium, resulting in a replacement of the outer (ectocranial) table of compact bone with exposed diploic bone. This gives the bone surface a sieve-like appearance and texture, ranging from severe to slight porosity. Skeletal series from the eastern Mediterranean basin, Nubia, eastern North America, Central America, and south Asia express relatively high prevalence of these lesions (Cohen and Armelagos, 1984; Steckel and Rose, in press). Some foraging populations also have high frequencies, including several along North America’s Pacific coast (Cybulski, 1977; Walker, 1986), for example. However, in these settings, parasitic infection—another cause of iron deficiency anemia—is likely a more important contributing factor than diet per se. Moreover, not all agricultural-based populations from archeological settings display elevated levels of porotic hyperostosis or cribra orbitalia. Growth rates are an especially sensitive indicator of poor nutritional quality. Children living in circumstances of poor diet show slower growth than in children with adequate diet. For example, based on the study of archeological skeletons from the lower Illinois River valley, growth of the femur appears to have been impeded in incipient agriculturalists compared to earlier foragers (Cook, 1984). Similarly, circumference of long bones is reduced in agricultural versus earlier populations in central Illinois (Goodman et al., 1984). A great deal of attention has been paid to the study of enamel development in poorly nourished populations, both living and extinct. When

Figure 3.3 Cribra orbitalia (top) and porotic hyperostosis (bottom).

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Figure 3.4 Enamel hypoplasia (grooves in teeth).

comparing foragers with farmers, there is generally a greater frequency of defects of enamel relating to periods of growth disruption. The most common type of defect observed in archeological remains are linear enamel hypoplasias (Figure 3.4). They appear as deficiency of enamel in the form of bands or lines of pits, mostly on the lip side of the anterior teeth (incisors and canines). Various types of physiological stress that result in a disruption of the cells (ameloblasts) that are responsible for enamel deposition cause the deficiency. The enamel defects are nonspecific in that specific causes of the disruption are unknown in most archeological contexts, but usually involve either malnutrition or some type of infectious disease or a combination of the two factors (Larsen, 1997). Studies of living populations often point to severe malnutrition as the leading cause. The temporal patterns with the shift from foraging to farming indicate increases for specific populations in eastern North America, south Asia, the Near East, and South America. There are certainly exceptions to this pattern, but the overall evidence indicates greater occurrence of defects in populations with an agricultural subsistence base (Larsen, 1995).

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MASTICATION The last ten thousand years have witnessed a gracilization of the human cranium—and masticatory complex, in particular. Sir Arthur Keith was among the first to document what he called a “maxillary shrinkage” and general facial reduction in recent humans compared with earlier populations (Larsen, 1997). A range of recent investigations has documented a consistent pattern of facial reduction and cranial shortening with the shift from foraging to farming in New World (e.g., Mexico, southeastern United States) and Old World (e.g., Nubia, western Europe, Japan, Near East) settings (Larsen, 1995, 1997). These changes arose consequent to the shift from chewing hard, tough foods to chewing soft, prepared foods. The soft texture is related to extended periods of cooking and boiling of food in ceramic vessels. With the reduction in facial size, there is a trend toward increase in tooth crowding and various forms of malocclusion. Malocclusion is a complex condition, influenced by a variety of extrinsic (nongenetic) and intrinsic (genetic) factors. The temporal trend of increased frequency of occlusal abnormalities in the past appears to be due to the shift in consumption from hard-textured to soft-textured foods. The association between consumption of soft-textured foods and craniofacial morphology has been well documented in experimental studies comparing animals fed soft foods with animals fed hard foods (reviewed in Corruccini, 1991; Larsen, 1997). In a study of minipigs, for example, Ciochon and coworkers (1997) found consistently smaller faces and jaws in the animals fed soft diets versus the animals fed hard diets. Dental crowding or facial gracilization by themselves do not indicate poor health. However, there is a link between crowding and increased incidence of diseased teeth and poor masticatory function, factors that certainly contribute to the general picture of declining health in the foraging-to-farming transition (e.g., Hanihara, 1981; Calcagno and Gibson, 1991). There is significant reduction in human tooth size in the last ten thousand years (Brace et al., 1991; Calcagno and Gibson, 1991). However, the reduction is not to the same degree as the reduction of the face and jaws, thus creating less space for the dentition. It is this discrepancy that likely causes much of the dental crowding observed in human populations, past and present. SEDENTISM AND HEALTH STATUS In general, agricultural populations are more concentrated, higher in number, and less mobile than foraging populations. Clearly, some hunter–gatherers in the archeological past were relatively sedentary

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(e.g., Chumash of the Santa Barbara Channel Islands region of California), and some agriculturalists were (and continue to be) relatively mobile (Kelly, 1995). One of the important population trends during the Holocene is the profound increase in sedentism in many regions of the globe. The increase in population, and accompanying sedentism, had specific consequences for health. That is, studies of living populations show that under circumstances of increased population size and crowding, conditions are established that are conducive to the maintenance and spread of infectious disease. Diachronic comparisons of nonspecific bony lesions called periosteal reactions or periostitis have been especially informative about patterns of community health in past societies. The lesions are mostly osseous plaques or irregular expansion of bone. Temporal trends show a general pattern of increase in prevalence in many settings where the condition has been studied, for example in Nubia, eastern North America, western Europe, and South America (Cohen and Armelagos, 1984; Steckel and Rose, in press; Larsen, 1995, 1997). For most settings, the increase in prevalence of periosteal reactions is related to population aggregation and sedentism, which establishes conditions that are conducive to poor sanitation, increased risk of infection, and spread of infectious disease. Thus, for this health indicator, the increase in prevalence is not due to the change in diet per se, but rather, the alteration in settlement pattern and lifestyle. There is evidence suggesting that some specific infectious diseases were not present in humans until relatively late in prehistory. For example, Stewart (1940) noted more than a half century ago that treponematosis, the group of diseases that includes both endemic and venereal forms of syphilis, was not present in North America until the few centuries before the arrival of Europeans. This conclusion has been largely borne out by recent research in a variety of settings (Larsen, 1994). Moreover, tuberculosis is now clearly identified in mostly late prehistoric populations in the Americas. It is important to emphasize that the increase in crowd-based infectious disease was not a direct result of dietary change, but rather was a consequence of altered living conditions. The independence of diet and skeletal disease is underscored by the temporal trend of increased bone infection identified in the Santa Barbara Channel Islands region by Lambert and Walker (1991). In this setting, increased population size and decreased mobility resulted in an elevated prevalence of periostitis, but the populations in this region were exclusively foragers. Another important point of these findings is that increased morbidity was due to both nutritional decline brought about by changing diet and to the presence of other stressors (e.g., iron deficiency anemia, disease, warfare, social

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disruption). Indeed, poor diet and disease are synergistic—the combined presence of both poor diet and infection is worse than the presence of either poor diet or infection alone. WORKLOAD AND ACTIVITY Pathology and Activity Osteoarthritis (degenerative joint disease) is one of the key biological concomitants of physical activity. It is a disorder involving degenerative changes of the articular hard tissues, cartilage, and bone. Skeletally, the condition is manifested as either proliferation of new bone along joint margins (lipping) or the loss of bone on joint surfaces (porosity or eburnation) (Figure 3.5). Numerous factors influence the disorder, but mechanical wear and tear—accumulating over a lifetime of activity—is the primary contributor. Unlike some of the other health indicators discussed in this chapter, there is no clear pattern of increase or decrease in diachronically studied skeletal samples representing the foraging-tofarming transition. In some settings, the condition decreases (e.g., southeastern U.S.) or increases (e.g., eastern U.S.) in frequency (Bridges, 1992). The lack of a definitive temporal pattern likely reflects the fact that activity is influenced in highly localized ways, which behooves investigators to understand as well as possible behavioral factors specific to particular geographic regions. Robusticity and Structural Adaptation It is well known that size and structure of bone tissue are highly responsive to mechanical demands. Human populations undergoing mechanically demanding activities have generally larger and more robust bones than populations that are less active (Larsen, 1997). Comparisons of hunter–gatherers with agriculturalists in diverse settings worldwide show that the former are more robust than the latter, virtually in any way robusticity can be measured. Because long bones (e.g., femur, humerus, tibia) are tubular, they can be modeled as hollow beams and subjected to mechanical analysis in the same manner as building materials analyzed by civil and mechanical engineers (Ruff, 2000). The distribution of bone, especially when viewed in cross-section, is strongly influenced by the type and degree of mechanical demand. The greatest mechanical stresses occur in the outermost fibers of the diaphysis, or shaft, of the long bone. Hence, a long bone diaphysis—as in the case of a femur—with a more outward distribution of bone has relatively greater strength or ability to resist

Figure 3.5 Marginal lipping (top) and eburnation (below), representing osteoarthritis.

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bending and torsion during periods of elevated mechanical demand, such as walking or running. In simple terms, then, bones that are wide are stronger than bones that are narrow. This characteristic of strength is not qualitative, but rather, simply indicates the ability of the bone to resist forces. The foraging-to-farming transition has only been investigated in a handful of cases, and virtually all are from North America. Like the analysis of osteoarthritis, the temporal trends are conflicting in comparison of regions. Larsen and Ruff (1994, 2001) have analyzed a temporal series from Georgia and Florida and found that measures of bone strength—called second moments of area—generally decline with the shift from foraging to farming. These findings are consistent with the temporal pattern of osteoarthritis. In contrast, Bridges and coworkers (Bridges, 1989; Bridges et al., 2000) found a pattern of increase in measures of bone strength in Alabama and Illinois, which they interpret to reflect an increase in mechanical demand. As with osteoarthritis, these differences almost certainly reflect contrasting agricultural adaptations in the two areas of the American east. In the case of Georgia, populations are coastal and heavily dependent on marine foods. In Alabama and Illinois, late prehistoric agricultural populations did not use marine foods (although various fishes were exploited from nearby rivers). Finally, Barondess (1998) has found no change in biomechanical properties in his comparison of foragers and farmers in New York state. Thus, in at least this setting, there was no change in activity pattern or workload, at least as the associated behaviors impact skeletal morphology. This finding lends further support for the conclusion that activity and its impact on the skeleton is probably localized. The ratio of two second moments of area, Ix and Iy, in the femur midshaft is especially informative about the degree of mobility in past human groups. The index, Ix /Iy, has been shown by Ruff (1987) to be a sensitive indicator of mobility—such as that involving long-distance travel. Comparisons of populations ranging from highly mobile foragers to sedentary industrial peoples reveal that populations that are sedentary tend to have values of the ratio that are closer to 1.0 than populations that are mobile. This reflects the fact that physically active, mobile populations with increased anterior–posterior bending stresses on the femur tend to have a relatively elongated femur midshaft in the frontto-back (anterior–posterior) direction (which measures bending strength, Ix) than in the side-to-side (medial–lateral) direction (which measures bending strength, Iy). In other words, mobile groups (foragers) have compressed femoral midshafts, whereas sedentary groups (agriculturalists, industrial) have rounded femoral midshafts. These findings indicate

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that although behavioral adaptations vary widely among human populations—even within specific groups or subsistence strategies—there is a clear and consistent trend of skeletal modeling that reflects decreasing mobility in the foraging-to-farming transition. Interestingly, the difference in the mobility index between females and males decreases in the shift from foraging to farming, suggesting that both sexes become increasingly sedentary in the transition (Ruff, 1987). DISCUSSION This chapter presents a body of evidence suggesting that the shift from foraging to farming was a generally negative one, at least with respect to health costs. This conclusion is based in part on the important findings presented by various bioarcheologists on their studies of skeletal remains from around the world presented in Cohen and Armelagos (1984), Paleopathology at the Origins of Agriculture. Contributors to the volume presented skeletal evidence showing temporal trends in health comparing foragers and farmers. Contrary to the traditional notion that the rise of agriculture in the post-Pleistocene world was a generally positive development for humanity, most contributors to the book reported a deterioration of health in the shift from foraging to farming. Although authors in the Cohen and Armelagos book evaluated the same types of data, the results have been called into question because a standardized coding scheme for various pathological conditions was not used. This makes direct comparison of studies difficult (see discussion in Steckel and Rose, in press). However, other bioarcheological research on the transition has tended to support the findings presented in the Cohen and Armelagos volume (see review in Larsen, 1995). Recent evidence from the Western hemisphere supports the general conclusion that health deteriorated with the adoption of an agricultural lifeway. In this regard, Steckel and Rose have directed a large collaborative effort involving a group of historians, economists, and physical anthropologists to address long-term trends in health in the Western hemisphere by the study of archeological skeletal remains from North, Central, and South America (Steckel and Rose, in press). This study utilized a common data-reporting format, using a range of variables (e.g., caries, hypoplasias, anemia, degenerative joint disease, and so forth) and involved the analysis of some ten thousand prehistoric and historic Native American skeletons dating from circa 4000 B.C. to the nineteenth century.1 Importantly, it supports the earlier findings presented in Cohen and Armelagos’s book that the health of Native Americans began to decline long before the arrival of Europeans.

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A key problem remains in our growing understanding of postPleistocene human evolution as it relates to the biological costs of the shift from foraging to farming. That is, outside of the Western hemisphere, the bioarcheological documentation of the foraging-to-farming transition in the world is sparsely reported. For vast regions of Europe, Africa, and Asia, we know relatively little about the health costs of the transition to agriculture.2 In eastern Asia, there are indications of health changes with the adoption of agriculture, such as increase in occlusal abnormalities and dental crowding, factors that promote dental decay (e.g., Hanihara et al., 1981; review in Larsen, 1997). However, as noted above, there is not a clear link between consumption of cultigens (rice) and dental caries in southeast Asia (Dommett et al., 2000). Jackes and coworkers (1997) have questioned the notion that the shift from foraging to farming resulted in universal health decline and whether the model applies to Europe. They note that few studies have documented biological change in western Europe in the Mesolithic-Neolithic transition, the critical period of time when early Neolithic populations adopted agriculture. In their study of remains from Portugal, Jackes and coworkers (1997) document a decline in dental pathology, contrary to other settings. The important point here is that outside of a select few regions in the Old World (e.g., Nubia, and other studies in Cohen and Amelagos, 1984), we know precious little about the impact of agriculture on human health for most of Europe, Asia, and Africa. Bioarcheologists must now seek to study the collections of human remains in these relatively untouched areas of the globe. CONCLUSIONS The shift from foraging to farming was one of the most profound— if not the most profound—changes in diet seen in the history of the genus Homo. This transition took place only within the last ten thousand years. Considering that our genus has been around for some three million years, the time period discussed in this chapter is a very small part of our history. This rapid transition is even more remarkable in light of the fact that the advantages of agriculture and food production—feeding more mouths per unit area of land—far outweigh the disadvantages discussed in this chapter. Thus, to revisit my original question—What was the impact of the transition from foraging to farming on human health and well-being? The answer appears to be an overall decline in health owing to a shift to a poor-quality diet and associated lifestyle changes brought on by increasing sedentism and population crowding. Thus, the decline in health where it has been documented reflects factors caused

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by the dietary change (e.g., dental caries) and by living circumstances (e.g., periosteal reactions). The analysis of structural morphology from various settings indicates that humans adapted in a biomechanical sense to new challenges and altering lifeways. The record is especially compelling for the New World. However, elsewhere in the world—most of Europe, Asia, and Africa—the record is far less complete. Scholars need to begin casting their attention more fully to the skeletons from the Old World in order to build a more comprehensive picture of the global history of health. ACKNOWLEDGMENTS An earlier version of this chapter was presented at the Fourteenth International Congress of Anthropological and Ethnological Sciences in 1998 in Williamsburg, Virginia. I thank Peter Ungar and Mark Teaford for inviting me to participate in their symposium on the evolution of human diet and to the present volume. The research for this chapter was supported largely by funding from the National Science Foundation. NOTES 1. The project—Health and Nutrition in the Western hemisphere—also contains a large sample of Euro-Americans (n = 1304) and African Americans (n = 1380) that was used to evaluate health trends in other major groups in the post-Columbian Americas (Steckel and Rose, in press). In addition to Cohen and Armelagos (1984) and Steckel and Rose (in press), the reader is directed to Cohen (1989) and Larsen (1995, 2000) for discussions of human biological change and health in the foraging-to-farming transition. 2. The health of ancient aboriginal Australia is relatively better known than that of ancient Europe, Asia, and Africa (Webb, 1995). However, prior to the arrival of the first Europeans in 1788, native populations were foragers exclusively. Thus, the issue of the impact of agriculture in prehistory is not an issue for this region of the globe.

Chapter 4

Early Childhood Health in Foragers Sara Stinson

In the discussion of the evolution of human diet, a great deal of attention has centered on the diets of past and present-day foragers. It might be expected that humans would show biological adaptations to a diet based on wild plants and animals since a foraging way of life represents more than 99% of human evolutionary history. When considering the health implications of forager diets, most of the attention has focused on the health of adults. Adults in forager groups are frequently described as healthy and well nourished (Hill et al., 1984; Lee, 1979). The diets of foragers also have been shown to have nutritional properties that would help to prevent many of the chronic diseases, such as heart disease and cancer, that are such major causes of mortality among adults in industrialized countries today (Eaton and Konner, 1985; Eaton et al., 1997). The health implications of forager diets for children have received much less attention. Children’s health is an important concern in any discussion about the evolution of human diet because child health has major ramifications for adult well-being. Most basically, survival through childhood is necessary for reproductive success. Mortality rates are higher in infancy and early childhood than at any other time except old age, and thus we might expect that there would be a great opportunity

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for diet to act as a basis for natural selection during childhood. Even when poor childhood health does not result in childhood mortality, it can have negative consequences later in life, such as a reduced ability to perform energy-intensive activities or a reduced ability to successfully bear children (Martorell, 1989). The purpose of this chapter is to review two indicators of early childhood health in present-day foragers: child mortality and child growth. Ideally, it would be possible to use these solely as indicators of the healthfulness of the diet, but, as will be discussed later in this chapter, mortality and growth are obviously affected by factors other than just diet. CHILD MORTALITY IN FORAGERS Present-day foragers have high infant and childhood mortality rates. Data summarized by Kelly (1995) for about a dozen forager groups show death rates in the first year of life of from 8% to 34%. As shown in Figure 4.1, an additional 12% to 18% of children die in early childhood (between the ages of one and five years). The infant mortality rates in foragers are virtually identical to those in horticulturalists and pastoralists (Hewlett, 1991). The forager groups reviewed by Hewlett have a somewhat higher mortality rate before age 15 (43.4%) compared to horticulturalists (39.3%) or pastoralists (34.0%). All of these mortality rates are astronomical when compared to the rates of infant mortality (0.7%), early childhood mortality (0.03%), or total mortality before age 15 (0.8%) typical of Western industrialized countries such as the United States (Hoyert et al., 1999). All of us would be dismayed if our children had the probability of death early in life that is a regular experience for members of these groups. Although mortality rates are among the most direct indicators of health, they are not specific in terms of identifying particular health problems. It is difficult to determine to what extent the high infant and childhood mortality rates observed in foragers are the result of dietary problems. Studies examining the causes of infant and childhood mortality rarely list nutritional deficiencies as a major cause of death among foragers. Only 5 out of 212 deaths of infants and young children were attributed to malnutrition by the Aka (Hewlett et al., 1986), and in three of these deaths, malnutrition followed the death of the mother, presumably because the child was still nursing. Measles, diarrhea, and convulsions accounted for almost 50% of childhood deaths among the Aka. Howell (1979) reported that almost 90% of deaths of children under age 15 among the Dobe !Kung were probably due to infectious diseases. The causes of Ache child mortality during the period of time before

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Figure 4.1 Infant and early childhood mortality rates in Ache, Kuchin, and !Kung foragers, mixed foraging and horticultural Trio, and Herero pastoralists. All of these populations experience high infant and childhood mortality. Data for Ache are from Hill and Hurtado (1996), for Kuchin from Roth (1981), for !Kung from Howell (1979), for Trio from Gage et al. (1984), and for Herero from Harpending and Pennington (1991).

permanent contact with Euro-Americans were quite different (Hill and Hurtado, 1996). Violence accounted for over 50% of deaths of children aged zero to three years, and almost 75% of deaths of children between the ages of four and fourteen years. Illness accounted for about 25% and 15%, respectively, of deaths in these two age groups. Malnutrition is not given as a cause of death, but in many cases the diarrheal diseases that were the cause of mortality were linked by informants to weaning and the introduction of solid food. The information on causes of death indicates that obvious malnutrition is rarely the immediate cause of death in forager children. This does not mean, however, that undernutrition is not a contributing factor in many deaths. The synergistic relationship between nutrition and infec-

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tion makes it extremely difficult to separate their relative contributions to poor early childhood health (Martorell and Habicht, 1986, and references therein). Diarrheal disease may result from pathogens present in the supplementary foods introduced when breast milk alone becomes insufficient to support nutritional requirements. Poor nutritional status decreases immune function, and thus can make children more susceptible to disease, and disease makes children more likely to become undernourished. Disease is frequently associated with loss of appetite or, especially in the case of diarrheal disease, with direct nutrient losses. Thus, undernutrition is a frequent contributor to deaths from infectious disease. EARLY CHILDHOOD GROWTH IN FORAGERS Growth in early childhood is a health indicator that has been tied more directly than mortality rates to diet and nutritional status. The typical pattern of growth seen in populations suffering from mild to moderate undernutrition is that the length of young infants is close to international reference data, but older children are much shorter and in some cases are excessively thin as well (Martorell and Habicht, 1986, and references therein). Figure 4.2 illustrates this pattern for height using data from one regional and four national samples considered to have varying proportions of mildly to moderately undernourished children. Growth measurements are expressed in terms of height-for-age, the mean height at a particular age. Height-for-age is considered to be an indicator of longterm nutritional status because an individual’s present height is the result of many years of growth (WHO Working Group, 1986). For the five groups illustrated in the figure, height-for-age is closest to international reference data in the first year of life and then decreases relative to reference data. In the shortest population illustrated in the figure, height-for-age decreases to over 2.5 standard deviations below international reference data by the age of four years, which is equivalent to a height below the third percentile of the reference population. Figure 4.3 illustrates weight-for-height in these same populations. Although there is some debate on the subject, weight-for-height is frequently considered to be a better indicator of current nutritional status than is height-for-age since weight can be quickly gained or lost (Victora, 1992; Waterlow et al., 1977; WHO Working Group, 1986). As shown in the figure, children in some populations maintain the same weight– height relationship as in the reference population, while in other populations children become quite thin. In no case, however, is weightfor-height more standard deviations below international reference data than is height-for-age.

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Figure 4.2 Height-for-age in selected populations in which a portion of children are mildly to moderately undernourished. The zero line represents the median for international reference data based on U.S. children. Heights are presented as standard deviations from the U.S. median (Z scores). Height is most similar to international reference data in the first year of life, but at older ages, most children are substantially shorter. Data for Mali are from Dettwyler (1991) and are for several rural villages. The data for other countries are unpublished and come from national surveys kindly supplied by Macro International, Demographic and Health Surveys, USA.

Unfortunately, there are few published data on body size in forager children, but existing data that do exist suggest that the infant and early childhood growth patterns in foragers are frequently is similar to those seen in nonforaging groups suffering from mild to moderate undernutrition. Truswell and Hansen (1976), reporting on their studies of the !Kung in the late 1960s, found that about 40% of !Kung infants under one year of age were below the third percentile of reference data for weight, and 50% were below the third percentile of reference data for length. After the age of one year, about 80% were below the third percentile for height, and from 60% to almost 90% were below the third percentile of reference data for weight (see Figure 4.4). Similarly, studies of the Ache indicate that Ache children are similar in size to U.S. children at birth, but by eighteen months of age they are below the U.S.

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Figure 4.3 Weight-for-height in selected populations in which a portion of children are mildly to moderately undernourished. The zero line represents the median for international reference data based on U.S. children. Weight-for-height is presented as standard deviations from the U.S. median (Z scores). Children in some populations maintain weight-for-height similar to the reference data, but in other populations, children older than one year are thin compared to reference data. Data for Mali are from Dettwyler (1991) and are for several rural villages. The data for other countries are unpublished and come from national surveys kindly supplied by Macro International, Demographic and Health Surveys, USA.

fifth percentile for height and at or slightly above the U.S. fifth percentile for weight (Hill and Hurtado, 1996). Compared to the populations presented in Figure 4.2, the heights of Ache and !Kung children are most similar to those of the smallest children shown in the figure, those in Nigeria and Pakistan. While height data have been described for !Kung and Ache children, such data are rare, and data on weight are all that is available for most forager groups only data on weight are available. This is unfortunate because weight-for-age is more difficult to interpret than either heightfor-age or weight-for-height. In essence, low weight-for-age can be the result of some combination of small body size (low height-for-age) and thinness (low weight-for-height). However, since forager children are generally not described as being excessively thin, it seems reasonable to

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Figure 4.4 Percentage of !Kung children who were smaller than the third percentile of international reference data for height and weight in the late 1960s. A large percentage of !Kung children were very small compared to international reference data. Data are from Truswell and Hansen (1976).

interpret low weight-for-age as indicating overall small body size rather than excessive thinness. Figure 4.5 shows mean weight-for-age in children in several forager groups compared to international reference data. Hadza children, like !Kung and Ache children, have weights well below reference values. Hiwi children are very variable. In some age–sex groups, their weights are above reference values, while in other age–sex groups they are well below reference values. Inuit children are consistently close to or above reference values. These data indicate considerable variation among forager groups. While Inuit children are similar to international reference data, the other forager groups show evidence of substantial growth deficits in childhood. Several questions are raised by these comparisons with international reference data. The first involve the reference data themselves, which are based on the growth of U.S. children. Could or should children in diverse

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Figure 4.5 Weight-for-age in forager children. The zero line represents the median for international reference data based on U.S. children. Weight-for-age is presented as standard deviations from the U.S. median (Z scores). Z scores for forager children were calculated based on the mean weights for each age-sex group. Children in some forager populations have weights well below reference values, while in other populations their weights are much closer to reference values. Data for Hadza, !Kung, Ache, and Hiwi are from Kaplan et al. (2000); data for Inuit are from Auger et al. (1980).

populations be expected to show the same pattern of growth as U.S. children? The question of could relates to what can be termed the genetic growth potential of a population. Would children with different genetic makeups grow to be the same size as U.S. children if they were raised in the same environmental circumstances? Studies comparing the growth of affluent children of differing ethnic groups indicate no major differences in their growth patterns, at least prior to puberty (Figure 4.6). These studies, which suggest there are not substantial genetic differences in growth in early childhood, have been the justification for using one set of reference data for international growth comparisons (Martorell and Habicht, 1986). There are many populations in the world, however, for which affluent representatives do not exist. For these populations, we do not yet know whether they could grow as U.S. children do.

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Figure 4.6 Heights of well off and less well off boys at age 7.5 years in selected populations compared to international reference data based on U.S. children. For these populations, there are no major differences in early childhood growth among affluent children. Data for Nigeria and India are from Eveleth and Tanner (1976), for Jamaica from Ashcroft et al. (1966), for Costa Rica from Villarejos et al. (1971), for China from Lin et al. (1992), and for Guatemala from Johnston et al. (1975), and Bogin and MacVean (1978).

While we do not know if children in most foraging populations would grow exactly as U.S. children grow if they were raised in the same environment, we do have indications that their growth pattern when leading their more or less traditional foraging way of life can change when environmental circumstances change. As shown in Figure 4.7, the percentage of young !Kung children whose heights were below the U.S. fifth percentile decreased markedly from the late 1960s to the mid 1970s as they moved from a foraging diet to a mixed diet of domestic and wild foods (Hausman and Wilmsen, 1985). Ache children adopted by U.S. families are much taller than children raised in their traditional environment (Hill and Hurtado, 1996). These findings indicate that the growth patterns of foraging populations do not always indicate their genetic growth potential.

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Figure 4.7 Increase in the height and weight of young !Kung children between the late 1960s when their diet was based mainly on hunting and gathering and the mid-1970s when they were eating a diet of mixed wild and domestic foods. Data are from Hausman and Wilmsen (1985).

The second question raised by comparisons with international reference data based on U.S. children is should children in diverse populations show growth patterns similar to those of U.S. children? Many have argued that the high growth rates and large body size of children in affluent countries should not be presented as an ideal because they are associated with diets that lead to numerous health problems later in life (see, for example, Walker et al., 1994). It has also been suggested that shortness not associated with excessive thinness should be considered an adaptation to environments with marginal nutritional resources because smaller individuals need fewer nutrients (Seckler, 1980; Stini, 1971), or that small body size is advantageous for foragers because it increases hunting success (Lee, 1979). On the other side of the argument is the evidence that small body size might actually be disadvantageous and that the process of becoming small is certainly detrimental. The major documented disadvantages of small adult body size are reduced capacity to perform energy-demanding

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work and possible limitations on a woman’s ability to bear children (Martorell, 1989). From this perspective growth deficits in early childhood can have consequences that last into adulthood (Martorell, 1995). Impairments in cognitive development are also common in populations in which slow growth in early childhood is frequent, although the extent to which this can be directly attributed to slow growth (rather than the poverty experienced by these populations) is not clear. The poor nutritional status and high rates of disease that lead to slow growth in early childhood are certainly unhealthy (Beaton, 1989; Martorell, 1989). There are no living human populations that combine slow growth in early childhood with measures indicating high levels of health, such as low mortality rates. While the growth rates of U.S. children may not be optimal, neither are the slow early childhood growth rates typical of many forager populations indicative of good health in early life. To what extent is the poor childhood growth of foragers the result of dietary problems? At first glance, the pattern of breastfeeding among foragers appears to be one that should promote good growth. The classic study of Konner and Worthman (1980) describes a pattern of virtually constant contact between mother and infant, with extremely frequent nursing bouts of short duration. Data on most forager groups indicate a similar pattern of on-demand nursing, although the age of weaning is not always as late as the !Kung average of four years (Hrdy, 1999). This is in contrast to breastfeeding patterns among at least some agricultural groups, where the availability of alternative infant foods plus women’s work schedules mean that infants are frequently left with other caregivers while their mothers do agricultural work (e.g., Levine, 1988). However, besides this information on breastfeeding frequency, we have no data specifically on the dietary intake of young children in foraging groups. In fact, it is notoriously difficult to collect accurate measurements of individual food intake because of the disruption to normal behavior that any such attempt necessitates. Studies of forager diet have therefore relied on measuring the total food brought into camp and estimating per capita intake by dividing the total nutrients by the number of individuals in the group. In general, these studies do not indicate major deficiencies in the average diet (Hill et al., 1984; Lee, 1979), but an adequate average diet does not necessarily mean that the nutritional intake of young children is satisfactory. Even in cases where ample food is available, young children may not have acceptable nutrient intakes because of factors such as unequal food distribution, beliefs that certain foods are inappropriate for young children, and expectations that young children should be responsible for feeding themselves (see Dettwyler, 1991, for examples from rural Mali).

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CONCLUSIONS Their high levels of infant and childhood mortality and slow rates of early childhood growth suggest that children in contemporary forager populations frequently experience poor health. The fact that forager patterns of mortality and growth are similar to those of populations considered to be suffering from mild to moderate undernutrition suggests that nutritional problems in childhood are not uncommon among foragers. This is not to say that poor childhood health is totally the result of poor nutrition. Disease and inadequate access to health care are certainly major contributors as well. There are, of course, limitations to the data presented in this chapter. The data on forager populations are sparse, with the most complete information coming from the !Kung and Ache. Obviously, we cannot extrapolate from several well-studied cases to all present foragers. It is also difficult to extrapolate from contemporary foragers to past foragers, among whom selection for dietary adaptation presumably occurred. We must keep in mind that contemporary foragers almost certainly do not represent the full range of foragers in the past, and, as a result, past dietary patterns may well have been different from present ones. While the preponderance of bioarcheological data indicates that health declined with the transition from foraging to agriculture (see Chapter 3), these same data document that health conditions for prehistoric foragers were far from ideal (Cohen and Armelagos, 1984). Thus the poor childhood health observed in many contemporary foragers was probably typical of past foragers as well. Poor health resulting in high mortality rates early in life would produce substantial opportunity for natural selection to operate at this point in the life cycle. Given this fact, it might be fruitful to look for evidence of adaptation to early childhood conditions when we consider the evolution of human diet.

Chapter 5

Meat-Eating, Grandmothering, and the Evolution of Early Human Diets James O’Connell, Kristen Hawkes, and Nicholas Blurton Jones

Meat-eating has long been identified as the primary driving force behind the evolution of early humans (Isaac, 1978; Washburn and Lancaster, 1968). Regular access to large, nutrient-rich carcasses through some combination of men’s big game hunting and scavenging is thought to have fostered what many regard as the basic human behavioral pattern: central-place foraging, a sexual division of labor among adults, nuclear families, paternal provisioning, and long periods of juvenile dependence. Though there are good reasons to be skeptical of this proposition, it continues to enjoy widespread acceptance, partly because of apparent support from the archeological record, partly for lack of a plausible alternative. Here we review and critique some of its salient elements, then outline a very different model—one that makes changes in women’s foraging and food-sharing practices and related adjustments in life history the fundamental agents of change in early human history. CARNIVORY, OFFSPRING PROVISIONING, AND HUMAN EVOLUTION The appeal of carnivory as an evolutionary catalyst lies in the common assumption that paternal provisioning is essential to child-rearing

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among human foragers. Mother is seen as unable to bear, feed, and raise children entirely on her own, largely because of their prolonged juvenile dependence; and is thus said to rely on her spouse for critical nutritional support, especially in the form of meat (e.g., Washburn and Lancaster, 1968). In fact, so the argument goes, the extended period of childhood development typical of modern humans could not have evolved without this paternal support. In recent years, this proposition has drawn support from the coincidence between dates for the first appearance of early African Homo erectus (also cf. Homo ergaster [Wood, 1992]) and those associated with the best-known Plio-Pleistocene archeological sites (Isaac, 1997; Leakey, 1971), all of which fall within the 1.5–1.9-million year (Ma) age range (Feibal et al., 1989; White, 1995). Early H. erectus represents a sharp departure from previous hominid forms in its increased body size, simplified digestive anatomy, and greatly expanded geographical range (Wood and Collard, 1999a,b), collectively read as clear evidence for a significant change in diet. Meat from large animals is widely identified as the new element, primarily on the basis of archeological data: sites of this age often contain the bones of large ungulates in close association with stone tools. Though opinions differ on whether these animals were acquired by hunting or scavenging, most agree that early humans were the principal agents of accumulation. Following Isaac (1978), many argue that the sites so defined were “central places,” similar to the base camps occupied by modern hunters, spots to which meat and marrow were routinely transported, probably by hominid males for distribution to mates and offspring (Rose and Marshall, 1996; Oliver, 1994). Paternal provisioning is a central element of most versions of this argument. Even those who disagree with certain aspects concur with the idea that meat was a significant part of early human diets, crucial to the emergence and subsequent evolutionary success of H. erectus (e.g., Blumenschine,1991; Rogers et al., 1994). Its broad appeal notwithstanding, there are several important problems with this argument. First, although primates other than humans hunt, none display the proposed evolutionary correlates. Chimpanzees are especially active as predators, most of the hunting is done by males, and the meat obtained is shared. Yet the expected consequences—central place foraging, nuclear families, and paternal provisioning—do not follow (e.g., Stanford, 1998). Second, quantitative data on modern human foragers show that big game hunting and scavenging are often highly unreliable provisioning strategies, even in arid tropical Africa where both practices are thought to have evolved. Among the Tanzanian Hadza, for example, men armed

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with bows and poisoned arrows operating in a game-rich savanna woodland habitat succeed in acquiring large animal prey at an annual average of only one every thirty hunter-days (Hawkes et al., 1991). Weeks may pass between kills, even in bands with several active hunters. Clearly, this is not an effective tactic for feeding small children. Though experimental data indicate that Hadza men could probably serve this goal more effectively by taking small game or plant foods (Hawkes et al., 1991), they choose not to, which suggests that their interest in big game hunting serves some purpose other than ensuring offspring survivorship. Whatever it is, everyday support for children must come from elsewhere. Similar observations on the ineffectiveness of men’s big game hunting as a provisioning strategy have been made about other modern foraging groups for which quantitative data are available (Hawkes, 1993; Lee, 1979; Marshall, 1976). Whether early human hunter–scavengers enjoyed higher success rates and were correspondingly more effective at provisioning depends on several factors, notably the encounter rate for large animal prey (hunted and/or scavenged), the probability of capturing them once encountered, and the amount of edible tissue acquired per carcass. Comprehensive modeling of these variables has yet to be undertaken (see Blumenschine, 1987, for a useful beginning), but it seems reasonable to speculate that they did not do even as well as the Hadza, primarily because they lacked the projectile weapons that allow the Hadza to be as good as they are at both hunting and confrontational scavenging (O’Connell et al., 1988). Archeological data are sometimes said to contradict this inference. Bunn (1982; Bunn and Kroll, 1986), for example, claims that the wellknown assemblage from FLK Zinjanthropus, containing the remains of at least forty-eight large ungulates, accumulated in less than two years, implying a minimum carcass acquisition rate of 20–25 per year at this site alone. Assuming that early humans were primarily responsible for these remains, that most of the carcasses represented were taken in complete or nearly complete condition, and that this was only one of many large faunal assemblages created by the local hominid group involved, then a meat consumption rate at least equal to, arguably much higher than, that reported for the modern Hadza is implied. As many have observed, however, the basis for Bunn’s estimated carcass deposition rate is weak: Other, more plausible interpretations imply a much longer period of accumulation, possibly up to several centuries (Kroll, 1994; Lyman and Fox, 1989; Potts, 1988). If most of the carcasses represented here and at other contemporary sites had also been heavily ravaged by other predators by the time hominids took control (Blumenschine and Marean, 1993; Marean et al., 1992), then a lower, even more sporadic

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large animal tissue intake than that enjoyed by the modern Hadza is indicated, one that is far too low to support effective offspring provisioning. Finally, and perhaps most important, recent archeological research strongly suggests that the pattern of carcass acquisition represented at Plio-Pleistocene Olduvai and East Turkana has a much greater antiquity than previously suspected. Reports from Kanjera in southern Kenya indicate that a hominid-created large faunal assemblage comparable to the one at FLK Zinjanthropus was deposited there as early as 2.2 Ma (Plummer et al., 1999): Similar assemblages may also be indicated in Ethiopia by 2.6 Ma (Asfaw et al. 1999; de Heinzelin et al., 1999; Semaw et al., 1997). If on closer analysis these early assemblages do indeed prove to have been deposited by the same hominid-related processes at about the same rates as those at the later sites, then the idea that meateating at this scale played a significant role in early offspring provisioning and the related evolution of early African H. erectus becomes untenable: the 400,000–800,000 year distance between putative cause and effect is simply too great. TOWARD AN ALTERNATIVE HYPOTHESIS: WOMEN’S FORAGING AND FOOD SHARING AND THEIR EVOLUTIONARY CONSEQUENCES Within the last five years, two alternatives to this argument have been developed, both focusing on the implications of changes in women’s foraging and food-sharing practices (Blurton Jones et al., 1999; Hawkes et al., 1997, 1998, 2000; O’Connell et al., 1999; Wrangham et al., 1999). Here we consider the alternative grounded in our work with the Hadza. Several important observations emerge from this research. First, although Hadza children are found to be active, productive foragers from an early age (Blurton Jones, 1993; Blurton Jones et al., 1989, 1994; Hawkes et al., 1995), they have great difficulty in the late dry season (August to October), when resources they can take for themselves in quantity, mainly fruit, are often unavailable. Mothers respond by provisioning with foods they themselves can procure daily and at relatively high rates, but that children cannot, largely because of handling costs. Tubers, which require substantial upper body strength and endurance to collect and in many cases the ability to control fire in processing, are a good example. Women can acquire several species at rates of about 1,000–3,500 kcal/hr, enough to meet their own needs and those of at least one other person in the course of an average foraging day and,

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importantly, with little day-to-day variance in returns (Hawkes et al., 1989, 1995, 1997; Vincent, 1985). Younger children take fewer species by themselves, at rates an order of magnitude lower than those earned by adults, far too low to meet even their own modest requirements (Blurton Jones et al., 1989, 1994, 1996). The effect of mothers’ foraging on children’s welfare is demonstrated by a simple but important correlation: Weight changes among the latter vary directly and significantly with the time their non-nursing mother spends collecting food (Hawkes et al., 1997). Provisioning of this sort has at least two important implications. First, it permits the Hadza to operate in habitats they could not occupy if, as among other primates, young weanlings were responsible for feeding themselves. Second, it lets another adult assist in the provisioning process, allowing mother to initiate the next pregnancy sooner. Though conventional wisdom assigns this role to husband/father, quantitative data reviewed above indicate that he does not perform it effectively, at least not via big game hunting and scavenging. Instead, critical assistance is usually supplied by a postmenopausal woman, typically grandmother. Senior Hadza women represent a significant portion of the adult female population (~40%), forage long hours every day, enjoy high returns for effort, and provision their grandchildren effectively, especially when their daughters are nursing new infants (Hawkes et al., 1989, 1997). Their support is crucial to both their daughters’ fecundity and their grandchildren’s survivorship, with important implications in turn for grandmothers’ own fitness. Again, a simple correlation demonstrates their impact: Weight changes in the younger weaned children of nursing mothers vary not with mother’s foraging effort, but with grandmother’s. Similar observations on the importance of grandmothers’ influence on grandchildren’s nutritional welfare and survivorship elsewhere are reported by Mace (2000). The Connection with Human Life Histories These observations suggest an hypothesis to account for the differences in average adult lifespans that distinguish humans from other hominoids (Blurton Jones et al., 1999; Hawkes et al., 1997, 1998, 2000). Childbearing careers in humans and apes are similar in length, but humans survive far longer after menopause. The dependence of weaned children on food from adults would have allowed ancestral human grandmothers to affect their fitness in ways that other apes could not, increasing the strength of selection against senescence, lowering adult mortality rates, and so lengthening average adult lifespans.

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Appeal to Charnov’s (1993) recent work on life history theory allows us to develop this hypothesis further. It is widely recognized that life histories differ greatly among the mammals: Some grow fast and die young, others mature slowly and live long adult lives (Harvey and Read, 1988). Charnov uses optimization techniques to model the links between adult mortality and other aspects of life history. Specifically, he suggests that declines in adult mortality rates are likely to favor a delay in age at first reproduction, mainly to gain the benefits of a longer period of growth, larger adult body size, and the increased productivity usually associated with it. Larger body size in turn usually leads to the production of larger neonates, later age at weaning, and a related increase in interbirth intervals. In short, longer adult life expectancy generally favors later age at maturity, larger body size, and larger but fewer offspring. If Charnov’s model accurately captures the interaction of key variables, and if “grandmothering” has the positive effect on daughters’ fecundity and grandchildren’s survivorship suggested above, then it should adjust these widely observed linkages in predictable ways among humans relative to other hominoids. Our longer average adult life spans should still predict later age at maturity, but contrary to the pattern in other apes, grandmothers’ help should allow daughters to wean earlier and so produce offspring at a faster rate during their childbearing years. Comparison of averages for modern human foragers and wild populations of chimpanzees, gorillas, and orangutans yields results generally consistent with these expectations (Table 5.1; Alvarez, 2000; Hawkes et al., 1998). Particularly striking are the values for αb, defined as the product of α, the average period of independent growth (weaning through age at maturity) and b, the rate of daughter production. All else being equal, this should approximate a constant: In Charnov’s terms, increased α should lead to lower b, keeping their product roughly the same. Values for nonhuman hominoids are indeed similar, but for humans the figure is three times as high, largely because of our disproportionately high rate of offspring production, driven in turn, we think, by the reliable, day-to-day provisioning efforts of older women who are no longer producing babies themselves. An Evolutionary Scenario Our observations on Hadza women’s foraging and food-sharing lead us to propose a set of closely related hypotheses about the emergence of this distinctively human pattern (Hawkes et al., 1997; O’Connell et al., 1999). Imagine an ancestral hominid with life history characteristics

Table 5.1 Average values for selected life history variables (after Hawkes et al. 1998 and sources cited therein). All age values expressed in years. Mean adult lifespan = average life expectancy at birth in wild ape and modern hunter–gatherer populations; age at maturity = age at first birth minus gestation; α = period of independent growth, weaning to maturity; b = annual rate of daughter production.

Orangutans Gorillas Chimpanzees Humans

Mean adult lifespan

Age at maturity

Age at weaning

α

b

αb

17.9 13.9 17.9 32.9

14.3 9.3 13.0 17.3

6.0 3.0 4.8 2.8

8.3 6.3 8.2 14.5

0.063 0.126 0.087 0.142

0.52 0.79 0.70 2.05

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Human Diet

and foraging patterns similar to those of the modern chimpanzee. Age at maturity was about 10–12 years; fecundity was relatively low. Children were sometimes fed by mothers and older siblings, particularly with items they could not collect for themselves, but the overall importance of these foods was low. Fertility in older females declined sharply in tandem with senescence in other aspects of physiology; maximum life span was about fifty years. There was no pattern of extended postmenopausal life. Now imagine a change in environment that reduced the availability of foods that younger juveniles could take for themselves. Resources that gave high returns to adults, but not juveniles, remained available, yet mothers could have used them only if they provisioned their younger weaned offspring more intensively. Older females at the end of their own fertility, with no young weanlings of their own, could have helped in this process. The more vigorous the older female, the more help she could provide and the greater the resulting advantage to both mother’s fertility and offspring survivorship. Selection against senescence in all aspects of physiology other than fertility would have increased; lower adult mortality rates and longer adult life spans would have followed accordingly. Longer life spans would also have increased the likelihood of reproducing before dying, in turn favoring a longer period of growth before first reproduction, consistent with general mammalian and primate patterns. The one aspect of life history unaffected by these changes would have been the length of the fertile period, any extension of which would have precluded assistance to grandchildren. CONNECTIONS WITH THE HOMINID FOSSIL, PALEOENVIRONMENTAL, AND ARCHEOLOGICAL RECORDS Life history characteristics of fossil hominids are commonly estimated by reference to brain size, dental eruption schedule, patterns of epiphysial closure, body weight, and stature (Smith and Tompkins, 1995). With these criteria, australopithecines and “earliest Homo” (cf. H. habilis and H. rudolfensis) are generally seen to have had ape-like life histories, comparable to those of modern chimpanzees. (The recent move to reassign “earliest Homo” to the australopithecines rests in part on these similarities [Wood and Collard,1999a,b]). These same criteria clearly identify early African H. erectus as the first hominid with a nonpongid life history, though opinions differ on its similarity with that of modern H. sapiens. Some see brain size and dental eruption schedules as indicating an average adult life span and age at

Meat-Eating, Grandmothering, and Early Human Diets

57

maturity intermediate between that of australopithecines and modern humans (Sacher, 1975; Smith, 1993); others see long bone growth and epiphysial closure rates and some of the same dental data as consistent with modern human maturation rates and, by implication, adult life spans (Clegg and Aiello, 1999; Tardieu, 1998). Either way, the appearance of early African H. erectus definitely marks a significant step away from the great ape life history pattern. The sharp increase in estimated body weight and stature, especially the estimated 70% increase in female adult body weights relative to earlier hominids, is consistent with this inference. Whether early African H. erectus also displayed the extended postmenopausal life span and relatively early weaning age anticipated by our evolutionary scenario remains unclear. In principle, it should be possible to monitor age at weaning by reference to changes in trace element composition (especially 18O and 13C) in teeth formed across the weaning period (e.g., Wright and Schwarcz, 1998). Research designed to explore this possibility is currently being initiated. Postmenopausal life span is more difficult to assess in the fossil record, but given the apparent conservativeness of this attribute (fertile periods in chimpanzees and humans are essentially the same [Hill and Hurtado, 1996; Schultz,1969]), it seems simplest to assume the same period in all fossil hominids, including early H. erectus. Given the inferred increase in average adult life span for the latter, an extended postmenopausal life span is implied. Links with Changes in Climate and Environment Our hypothesis leads us to expect that life history changes in H. erectus were driven by a decline in the availability of food resources easily taken by children (e.g., fruit). Such declines should generally be associated with long-term trends toward cooler, drier, more seasonal climates. In tropical Africa, cooler, drier winters would have been especially critical: Plant foods accessible to humans are limited in this season, and those that are available (e.g., seeds, nuts, underground storage organs) typically have heavy processing costs, making them difficult for children to acquire and/or process to edible form (Blurton Jones et al., 1989, 1994; Hawkes et al., 1995). Data from a wide range of sources (e.g., deep marine sediments, soil chemistry, pollen, fossil faunas) consistently indicate that the 1.9–1.7 Ma time period bracketing the first appearance of African H. erectus was marked by an unusually pronounced shift toward cooler, drier, more seasonal conditions and a related trend toward open, less wooded plant communities (Cerling, 1992; deMenocal, 1995; Reed, 1997; Spencer,

58

Human Diet

1997). Especially notable here is the associated evidence for extinctions among frugivorous primates in various east African localities after 1.8 Ma, all probably related to the restriction of closed forest habitats (Reed, 1997). Links with Changes in Diet Our hypothesis also leads us to expect that the life history changes indicated for H. erectus were associated with the exploitation of previously unused or little-used resources, items that were especially suitable as provisioning foods. To serve this purpose, such resources must have been: (1) generally available, particularly in the dry season, (2) capable of yielding returns high enough to support the collector and at least one other person, (3) reliable enough to provide those returns with little or no daily variance, and (4) open to exploitation by adults but not younger children. Many resources meet these criteria, notably certain varieties of small game, shellfish, nuts, seeds, and the underground storage organs (USOs, or tubers) of plants. Though none are especially well-represented in the archeology of early H. erectus, this may reflect problems of preservation, the absence of attention to their recovery by archeologists, or both. The best prospective candidates for increased exploitation may be USOs (Coursey, 1973; Hatley and Kappelman, 1980; Wrangham et al., 1999). Tubers are encountered in many forms across a wide array of habitats, often representing up to 20% of local plant species and sometimes occurring at densities greater than one metric ton per hectare (Raunkiaer, 1934; Thoms, 1989). Carbohydrate content varies within and between taxa, but generally represents 50%–90% of dry weight. Wild forms of tubers are widely exploited by humans in tropical through cool temperate habitats on all continents (Coursey, 1967; Hladik and Dounias, 1993; Johns, 1990; Malaisse and Parent, 1985; O’Connell et al., 1983; Thoms, 1989; Wandsnider, 1997). Data from African, Australian, and North American settings indicate returns of 1,000–6,000 kcal/hour, which commonly translates to about 8,000–12,000 kcal/ forager-day, all with very low day-to-day variance—easily enough to support at least two consumers (Blurton Jones et al., 1994, 1999; Couture et al., 1986; Hawkes et al., 1995; O’Connell et al., 1983; Thoms, 1989; Vincent, 1985). Despite these appealing characteristics, USOs present certain problems to prospective consumers: They may be heavily defended mechanically or chemically and their carbohydrate content may be difficult to digest

Meat-Eating, Grandmothering, and Early Human Diets

59

without preconsumption processing (Coursey, 1973; Thoms, 1989). These considerations limit children’s access to tubers among modern human foragers: They can only collect forms found close to the surface that require little or no processing (Blurton Jones et al., 1989; Hawkes et al., 1995). The same factors probably also limit tuber use among primates: Chimps rarely take them; baboons do so only in highly arid environments and even then only target forms that juveniles can handle easily on their own (McGrew, 1992; Whiten et al., 1992). Archeological evidence of tuber exploitation is often limited and indirect. Still, we can point to at least four lines of evidence consistent with increased use of tubers beginning with the appearance of H. erectus: • Geographical range. H. erectus occupied a far broader range of habitats than any previous hominid and was the first to disperse beyond Africa. Early examples are found as far east as Java and as far north as latitude 50 degrees (Dennell and Roebroeks,1996; Gabunia et al., 2000; Swisher et al., 1994). The sharp change in distribution strongly implies access to a new food source. All new habitats occupied were likely to have offered tubers in variety and quantity; 50 degrees north is the approximate limit of reliance on tubers as a staple among ethnographically known hunters in continental habitats (Thoms, 1989). • Digging tools. Efficient exploitation of deeply buried USOs requires, at minimum, a digging tool. The earliest examples known date to about 1.7 Ma (Brain, 1988). • Evidence of fire. Cooking is essential to the use of chemically defended tubers and important to the conversion of the complex carbohydrates they commonly contain, to simpler, more readily digestible forms. Though highly controversial, the earliest dates for humanly controlled fires, suitable for tuber processing, fall within the range of 1.4–1.6 Ma (Bellomo, 1994; Rowlett, 1999). The ability to control fire may be the key factor distinguishing H. erectus resource use from that of australopithecines, at least some of who are also thought to have been involved in tuber exploitation (see Chapter 6). • Digestive anatomy. Reductions in digestive tract size and molar surface area associated with earliest H. erectus clearly point to increased use of resources that require less post-consumption processing (Aiello and Wheeler, 1995; Suwa et al., 1996), implying either a narrower range of foods exploited or increased investment in preconsumption processing. Tuber cooking is a good example of the latter strategy.

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SUMMARY The appearance of early African H. erectus marks an important evolutionary threshold—in many respects, the first definitive step away from ancestral hominoid patterns of life history and ecology. Though conventional wisdom identifies meat-eating as the driving force behind this move, recent research increasingly indicates that this is unlikely to have been the case: Carnivory (1) does not produce human patterns of mating and reproduction in chimpanzees, (2) does not provide the essential daily rations needed to support early weaning and delayed maturity in modern human foragers, (3) does not appear to have been any more capable of providing such support in the Plio-Pleistocene, and (4) (if recent archeological discoveries develop as it now seems they might) does not even coincide with the first appearance of H. erectus. Though the evolution of this hominid form was almost certainly correlated with, and probably driven by, a significant shift in diet, men’s big game hunting and scavenging and related meat consumption seem unlikely to have been the catalyst. Other alternatives deserve more serious consideration. Recent work with the Hadza draws attention to the important role of women’s foraging and food-sharing in supporting young children, particularly in lean seasons when foods that the latter can procure and process on their own are in limited supply. Detailed studies of women’s time allocation, foraging returns, and children’s weight changes point to the positive effect of mothers’ provisioning on offspring survivorship. The same data also underline the importance of grandmother’s support when mother is occupied with a nursling. This in turn suggests an hypothesis for the evolution of the long postmenopausal life spans that distinguish us from other primates. Framing the hypothesis in terms of Charnov’s life history model adds important dimensions. Initial reference to pertinent paleoenvironmental, fossil, ethnographic, and archeological data yields results consistent with expectations: Shifts in several aspects of hominid life history correlated with the appearance of early African H. erectus coincide with predicted changes in climate and vegetation, as well as in H. erectus ecology. Further development of this line of argument is clearly in order.

Chapter 6

A Two-Stage Model of Increased Dietary Quality in Early Hominid Evolution: The Role of Fiber Nancy Lou Conklin-Brittain, Richard W. Wrangham, and Catherine C. Smith

There is considerable evidence that modern humans evolved from a chimpanzee-like ancestor (Pilbeam, 1996). Consequently, Pan has become an important and instructive modern analog for modeling many aspects of early hominid biology and behavior. Here we use our data on the nutritional ecology of modern chimpanzees to speculate on both the macronutrient composition of the australopithecine diet and on the mix of plant parts these hominids might have exploited to obtain these nutrients. These speculations are informed by australopithecine dental morphology and enamel chemistry, as well as by the nature and composition of diets consumed by Homo sapiens. Although modern chimpanzees eat some meat (Teleki, 1981; Stanford, 1998), we will consider only the plant component of the chimpanzee diet; plant foods provided the great majority (~99%) of the food eaten by these primates during our year-long study in Kibale National Forest, Uganda. Chimpanzees observed at other field sites have been estimated to eat as much as 3% of the diet in the form of meat, but little of this goes to the females or juveniles (Wrangham et al., 1989). Consequently, meat appears to have relatively little impact on the overall nutritional quality of the chimpanzee diet.

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Human Diet

Our aim is to bridge the dietary gap between chimpanzees and early Homo, specifically proposing food options for the australopithecinegrade hominids. Milton (1987) and others (Leonard and Robertson, 1997; Aiello and Wheeler, 1995; Wrangham et al., 1999) have suggested that early Homo in some way circumvented the nutritional constraints affecting the apes. These constraints relate to the fact that, generally, large mammalian herbivores consume diets relatively high in fiber (low in quality) compared to smaller herbivores, whereas modern humans, despite being larger than chimpanzees, consume a relatively low-fiber, high-quality diet (Milton, 1999b). We suggest that the australopithecines obtained a diet of intermediate quality, setting the stage for early Homo to incorporate additional improvements. In this chapter, we will explain how the underground storage organs (USOs) of plants are expected to improve the quality of a chimpanzee-like diet by reducing overall fiber content and therefore represent a key way in which early hominids could have improved diet quality and predictability. Fiber content is the principal measure we will use here to define diet quality. Ideally, we would also discuss secondary plant compounds (alkaloids, tannins, terpenoids, etc.), but there are practically no quantitative data on the secondary plant compound intake of humans. The influence of fiber on diet quality is two-fold. First, mammals consume a limited weight of food each day, for example ranging from 3% to 5% of body weight for adult herbivores (Van Soest, 1994). The higher the percentage of fiber contained in the finite number of grams an animal is capable of eating per day, the lower the percentage of nutrients present. Thus, fiber dilutes the nutrients with indigestible material. Second, especially when insoluble fiber is formed by the growing plant’s cell walls, it irreversibly bonds with a certain amount of the protein, starch, and other nutrients also present in the plant cell walls (Van Soest, 1994). Since insoluble fiber is very poorly digested, it will not release many of the nutrients so trapped, thus reducing the overall availability of those nutrients. In summary, not only is fiber itself fairly indigestible, but it also decreases the availability of nutrients trapped within its matrix. FIBER IN APE AND MONKEY DIETS We have recently completed a study comparing the diet of chimpanzees with that of three sympatric frugivorous cercopithecine species in Kibale Forest, Uganda (Wrangham et al., 1998; Conklin-Brittain et al., 1998). The study species were chimpanzee (Pan troglodytes), blue monkey (Cercopithecus mitis), redtail monkey (C. ascanius), and graycheeked mangabey (Lophocebus albigena). The four species were studied

A Two-Stage Model of Increased Dietary Quality

63

in fully overlapping ranges and simultaneously, i.e., under the same conditions of food availability. Six principal plant food categories were recorded: ripe fruit pulp, unripe fruit pulp, seeds, leaves, flowers, and pith. There was little diet overlap in species lists between chimpanzees and cercopithecines. Seeds and leaves of more species were consumed by monkeys, while pith of more species was consumed by chimpanzees. Even within the fruit categories, there was little species overlap (Wrangham et al., 1998). The proportion of each food type in each primate species’ annual diet is shown in Conklin-Brittain et al. (1998). In summary, chimpanzees were ripe fruit specialists (about 75% of time spent feeding), while the monkeys split their time fairly equally among ripe fruit, unripe fruit and seeds, and leaves. Chimpanzee feeding choices also coincided with the availability of ripe fruit quite closely, while those of the monkeys did not. When ripe fruit was not available, the principal fallback food of chimpanzees was herbaceous stem piths (Wrangham et al., 1991). The fallback food of monkeys varied among species (redtails: unripe fruit and seeds; blues: leaves; mangabeys: diverse diet at all times) (Wrangham et al., 1998). Given that chimpanzees and monkeys ate different items, we considered how these differences affected their intake levels of macronutrients (Conklin-Brittain et al., 1998). We calculated weighted monthly averages of different nutrient intakes. The weighting coefficient was the percentage of time spent feeding on the different foods. During our study the primates mostly consumed food types that required little manipulation, so that the time spent feeding appeared not to be influenced strongly by foraging/handling time. We found some striking similarities among the four primates. For example, the crude lipid or fat content of the different primate diets was not significantly different across species, and it was very low even at peak consumption levels. Peak lipid was only about 8.5% of dry matter (DM), and the average annual intake was only about 2.5% of DM (ConklinBrittain et al., 1997). As a point of reference, human fat intake probably does not need to be more than about 5% of DM, enough to provide the essential fatty acids (linoleic and α-linolenic acids) and the fat-soluble vitamins (Mann and Skeaff, 1998; RDA, 1989). Modern, westernized humans consume fat far in excess of need or recommendations (Butrum et al., 1988), e.g., 15%–25% of DM (usually referred to as 30%–45% of calories consumed) (Mann and Skeaff, 1998; RDA, 1989). We also found striking differences among the primate diets. Crude protein (CP) content was higher in monkey than in chimpanzee diets (annual percent of DM averages: ~15% for monkeys, 9.5% for

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chimpanzees) (Conklin-Brittain et al., 1998; Conklin-Brittain et al., 1997). The value 9.5% of DM is consistent with Oftedal’s (1991) suggestion that primates have relatively low protein requirements compared to other mammals, perhaps because they have slower growth rates (Case, 1978). As a point of reference, adult humans are thought to need a maximum of 9.5% protein on a DM basis, assuming a diet containing 5% fat, which is similar to the wild chimpanzees’ (RDA, 1989). Consequently, the chimpanzees’ plant diet was probably not deficient in protein. The high protein content of the monkey diet was the result of eating leaves as a fall-back food since leaves are generally protein-rich (ConklinBrittain et al., 1998). The chimpanzees, on the other hand, consumed pith as a fallback food, which contained on average low-to-moderate protein. We hypothesize that chimpanzees ate piths because they were high in one of the more easily digested insoluble fiber fractions (hemicellulose), therefore contributing to their carbohydrate and energy intake (Wrangham et al., 1991). Total nonstructural carbohydrates include the simple sugars as well as the complex carbohydrates—starch and most soluble fibers. Most starch is easily digested. Soluble fibers include pectins, gums, betaglucans, and other nonstarch polysaccharides, as well as resistant starch. Humans can digest (via hind-gut fermentation) from 0% to 100% of soluble fibers (Bourquin et al., 1996; Eastwood et al., 1986; Siragusa et al., 1988), depending on the fiber. We assume that because chimpanzees probably have a larger capacity for hind-gut fermentation (Chivers and Hladik, 1980; Milton, 1987; Milton and Demment, 1988), they can digest/ferment most soluble fibers, so we included soluble fibers in the category of carbohydrates digestible by chimpanzees. The chimpanzees showed significant seasonality, increasing their total nonstructural carbohydrate intake during times of high ripe fruit availability (ConklinBrittain et al., 1998). This coincides with what is believed to be the healthiest human diet, one that contains high amounts of complex carbohydrates and only small amounts of fat and protein (Butrum et al., 1988). Neutral-detergent fiber (NDF) is also referred to as total insoluble fiber or total structural carbohydrates. This chemical category showed surprising similarity in diets among all four primates; they all consumed around 32% of DM throughout the year based on weighted averages that take selectivity into account (Conklin-Brittain et al., 1998); 33.6% was the annual average fiber content of the chimpanzees’ diet. This was surprising because the monkeys are small, about 10%–20% the body weight of the chimpanzees. In general, smaller animal species consume diets lower in fiber than those of larger animals (Cork, 1994; Demment

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65

and Van Soest, 1985; Parra, 1979). Therefore, compared to the monkeys, the chimpanzee diet was relatively low-fiber (Conklin-Brittain et al., 1998), possibly already starting to circumvent the body size constraints discussed by Milton (1999b). Compared to modern humans, however, the chimpanzee diet was still extremely high in fiber (discussed later in this chapter). For the purpose of comparing the quality of different plant parts contributing to the chimpanzee diet, simple averages for chemical composition of the food items are summarized in Table 6.1. No plant part was high in lipid; seeds were the highest, but 8.4% is not high compared to seeds eaten by specialized seed-eaters like the saki monkey (where lipid values can reach 35%; Norconk et al., 1998). Leaves, which were mainly young, had the highest crude protein. Piths on average contained less than half the amount of protein in leaves. Flowers, like leaves, were high in protein, but were eaten only sporadically due to availability. The average ripe fruit had exactly the same protein content as the annual average intake for the chimpanzees. Ripe fruit was the “sweetest,” and piths were the second sweetest. Ripe fruit was also the lowest in fiber, but 33.6% is quite high for a fruit pulp, especially compared to domestic fruit and vegetables. Wild fruit was much lower in simple sugars than either domestic fruit or vegetables and was much higher in fiber. Modern humans have clearly selected for simple, sweet sugars and against fiber while domesticating their plant foods. The fiber values for the domestic fruit and vegetables are estimated from crude fiber values provided by Watt and Merrill (1963). Crude fiber is a measure that is rarely used anymore, but NDF values have not been published for many domestic fruit and vegetables. Crude fiber underestimates fiber content by an average factor of two or three (Van Soest, 1994). To be conservative, therefore, we used two as a correction factor on the average value of all ten fruits and eleven vegetables. To summarize, all of our study species consumed a low-fat, high-fiber diet compared to modern humans (e.g., Georgiou and Arquitt, 1992). The chimpanzees’ diet was higher in total nonstructural carbohydrates than the cercopithecine diets and therefore was higher in quality when ripe fruit availability increased. In addition, the chimpanzees maintained a moderately low and constant protein intake, due to their focus on fruit, with pith as a fallback food. HOMINID NUTRITIONAL ECOLOGY In this section, we consider how and when the human diet evolved from a chimpanzee-like diet. We suggest that what human brains and

Table 6.1 Chemistry of Wild Food Categories Consumed by Primates, as a Percentage of Dry Matter (DM). Also included are averages for domestic fruit and vegetables, as a percentage of DM Item

n

Lipid

CP

SS

NDF

Wild Chimpanzee Foods Ripe fruit Unripe fruit Leaf Seed Pith

32 35 75 18 19

4.9 3.1 1.4 8.4 1.2

9.5 12.0 22.1 14.3 9.6

13.9 8.0 5.3 9.8 11.6

33.6 38.7 40.7 46.1 44.1

Flowers

18

2.5

20.8

8.5

35.5

Human Domesticated Foods Domestic Fruit*

10

2.6

5.1

42.8

10.6

Domestic Vegetables**

11

2.3

17.6

25.6

20.1

Source: Wild values were determined in the Nutritional Ecology Laboratory, Department of Anthropology, Harvard University; domestic values from the same laboratory or from Watt and Merrill (1963). CP = crude protein, SS = simple sugars, NDF = neutral-detergent fiber, n = number of species included *Macintosh apple, Granny Smith apple, pear, banana, grape, mango, cantaloupe, orange, pinapple, strawberry **Carrot, cucumber, eggplant, iceberg lettuce, mushroom, onion, potato, red pepper, summer squach, tomato, zucchini

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67

bodies need is a low-fiber, high-nutrient diet compared to wild chimpanzees, and we hypothesize that a key trend repeatedly characterizing evolutionary transitions has been a progressive reduction in fiber content. Thus, we hypothesize that such reductions occurred first from a chimpanzee-like ancestor to an early australopithecine; second, from a late australopithecine to a Paleolithic forager; and finally, as is already substantiated, from Paleolithic foragers to agriculture-based humans. Dietary fiber intake can be reduced in three ways. First, plant foods that are lower in fiber can be selected. We suggest that this occurred with the consumption of low-fiber USOs by australopithecines. Second, lowfiber animal foods, such as meat, can be consumed instead of high-fiber plant foods (with the additional benefit of providing an easily digested source of nutrients [Milton, 1999b]). Meat consumption has probably been important since the genus Homo evolved. Finally, fiber content can be reduced through food preparation and processing techniques, such as cooking. Although the antiquity of these techniques is not known for certain, they may also go back to the origins of Homo (Wrangham et al., 1999). Thus, in the ape–human comparison, all three mechanisms for reducing fiber intake are suggested to have been important. As a prerequisite to considering the australopithecine diet, we first discuss hypothetical ancient hunter–gatherer diets, as well as modern but traditional, or non-westernized, human diets. Paleolithic Hunter–Gatherer Diet In The Paleolithic Prescription, Eaton et al. (1988b) reconstructed a paleolithic forager diet based on average values from current hunter– gatherer diets available in the literature. The data came from only six groups, mostly living in marginal habitats. One of the studies was on the !Kung, whose diet was recorded for a single month (Lee, 1969), and one was on the Eskimos (Eaton et al., 1988b). Despite these limitations, the diet hypothesized by Eaton et al. (1988b) offers an opportunity to consider how hunter–gatherer nutrition may have changed compared to an ancestral chimpanzee diet. The forager diet reconstructed by Eaton et al. contained 35% meat and 65% (wild) plant foods. How often ancient Homo populations would have obtained such a high meat intake is uncertain (see, for example, O’Connell et al., 1999; Wrangham et al., 1999). Many recent or contemporary hunter–gatherer societies have indeed been reported to consume similarly high amounts of meat (Kelly, 1995), but the reliability of such data is limited partly because the estimates rarely include intake of foods consumed out of camp (F. Marlowe, personal

Human Diet

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communication). Additional uncertainties derive from relatively recent influences, such as improvements in hunting technology, acquisition of hunting dogs, and changes in faunal density from the Paleolithic to the present. With these shortcomings in mind, Table 6.2 presents the “Paleolithic prescription” model diet. To make the results comparable to our data on chimpanzee diet, we have calculated the proportion of each major nutrient to total grams consumed. Protein intake in the “Paleolithic prescription” diet is at least three times higher than required by modern Homo sapiens. It is also higher than that recommended for omnivorous primates (NRC, 1978, NRC, 2001). The fat intake is likewise high compared both to the chimpanzee diet and to that required by humans, even though the authors used nutrient values from wild meat, which is much leaner than domestic meat (Eaton et al., 1988). Since neither protein nor fat intake shows a consistent trend across evolutionary time (from chimpanzees to modern humans), their reconstructed values in the Paleolithic diet have little significance for our attempt to understand the larger patterns of dietary evolution. Fiber content, however, provides a more interesting opportunity for comparison. The plant component of the Paleolithic hunter–gatherer diet was calculated by Eaton et al. (1988b) to contain 150 g of fiber daily or 18.5% of DM. This hypothesized high fiber content of Paleolithic diets is supported by coprolite studies (Kliks, 1975). This estimate is substantially higher than in modern humans (Table 6.3). Only two published values for agriculture-based diets have been as high. Bingham and Cummings (1980) reported that modern Ugandans

Table 6.2 Proposed Average Daily Macronutrient Intake for Late Paleolithic Humans

Protein Fat Carbohydrate Total fiber Total grams

Grams

% of total energy

% of total grams consumed

250 70 340

33 [(250g × 4 kcal/g)/3000] 21 [(70g × 9 kcal/g)/3000] 46 [(340g × 4 kcal/g)/3000]

30.9 8.6 42.0

150

—

18.5

810

Total energy consumed = 3,000 kcal; values given are percent of dry matter (Eaton et al., 1988b).

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Table 6.3 Macronutrient Levels in a Modern but Traditional Daily Diet Consumed by the Men of the Oto Tribe in the Forests of the Democratic Republic of the Congo

A. Rainy

Grams

% of total energy

Protein Fat Carbohydrate

38.5 60.9 325.3

7.7 [(38.5g × 4 kcal/g)/2000] 27.4 [(60.9g × 9 kcal/g)/2000] 65.0 [(325.3g × 4 kcal/g)/2000]

9.3 13.1 69.8

41.0

—

8.8

Total fiber Total grams

% of total grams consumed

465.0

B. Dry

Grams

Protein Fat Carbohydrate Total fiber Total grams

87.6 24.2 325.3 41.0 478.1

% of total energy 17.5 [(87.6g × 4 kcal/g)/2000] 10.9 [(24.2g × 9 kcal/g)/2000] 65.0 [(325.3g × 4 kcal/g)/2000] —

% of total grams consumed 18.4 5.1 68.5 8.6

Reported total energy consumed = 2000 kcal. Values are percent of diet DM. A Rainy season in the village. B. Dry season in the hunting camp. The original data from Pagezy (1990) were given as percent of diet fresh weight. We estimated content based on table values from Leung et al. (1968) and Watt and Merrill (1963) and converted all data to percent of DM, to make consumption comparable to the chimpanzee diet and the proposed Paleolithic diet.

consume 150 g fiber daily, but in subsequent publications Bingham (1992) reduced that level to 70 g. She did so because her original analysis used values from the “Southgate method” of fiber analysis, which tends to overestimate fiber levels in most plants and particularly in the Ugandan staple, plantain banana. Another high value, also given by Bingham (1985), was likewise subsequently reduced; 130 g fiber/day for modern Kenyans was reduced to 86 g/day (Bingham, 1992). We have seen that a wild herbivore (specifically frugivore) diet, such as that of the chimpanzee in Kibale Forest, is high in fiber because most wild plant foods are high in fiber (Table 6.1). The “Paleolithic prescription” diet, by contrast, contains only about half the fiber of the chimpanzee diet. Even though 150 g fiber (~18% of DM consumed) is high compared to that for agriculture-based humans, it is low compared to that for chimpanzees (Table 6.1).

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Modern Hunter–Gatherer Diet Modern, westernized diets normally include only 10–20 g of fiber per day (Johnson and Marlett, 1986; Georgiou and Arquitt, 1992), although the National Cancer Institute strongly recommends 35 g (Bourquin et al., 1996). This low fiber intake is also linked to several pathological conditions, so it may be more useful to consider a modern but traditional diet from the tropical rain forest of the Democratic Republic of the Congo, where the only domesticated component of the diet is cassava, a tuber very low in fiber (Pagezy, 1990). The rest of the diet is wild—either game or wild plant food (Table 6.3). Fat intake levels in “B,” the hunting camp, were at the 5% level, referred to previously as adequate for humans. The men in camp ate more game and fish, about 20% of DM intake, but their diet was still dominated by cassava in these comparisons. Fiber levels have dropped from 33.6% NDF for chimpanzees to 18.5% for a hypothetical ancient hunter–gatherer diet and now to about 9% for this modern but traditional diet. This traditional diet contained meat but was dominated by cassava, a low-fiber root crop. Modern Non-Westernized Diets We next consider modern but traditional human diets that perhaps represent early agricultural diets, but that are still not westernized. The composition of these diets further reinforces the progression of successively lower fiber in the diet. Figure 6.1 compares seven such diets against the Kibale primates, the proposed Paleolithic hunter–gatherer diet, and a Western diet, specifically that of U.S. college women (Ethangatta et al., 1996; Grewal and Hira, 1995; Walker, 1995; Georgiou and Arquitt, 1992; DeLisle et al., 1991; Pagezy, 1990; Eaton et al., 1988a; Rosetta, 1986; Hassan and Ahmad, 1984.). We have then inserted into this comparison our projected nutrient levels for the australopithecine diet. The protein content of all of these diets is adequate or high and shows no consistent trends through time or across subsistence strategies. The reconstructed Paleolithic diet stands out as being perhaps unrealistically high in protein as a year-round diet. The fat content ranges from the minimum recommended 3%–4% in some of the non-westernized diets (and in all of the Kibale primate diets) to about 17% of DM for U.S. college women. Even the high-meat Paleolithic diet contains only about 8.6% fat. There is suggestion of increased fat intake through time or across subsistence strategies. Among modern diets the fiber content reflects the dominant carbohydrate source; rice-based diets or refined wheat-based diets have the

Figure 6.1 Nutrient changes over time or subsistence strategies. Data for ape/ monkey from Conklin-Brittain et al. (1998); “australopithecines” from our conjecture; “Paleolithic” from diet proposed by Eaton et al. (1988); non-westernized from Ethangatta et al. (1996); Grewal and Hira (1995); Walker (1995); DeLisle et al. (1991); Pagezy (1990); Rosetta (1986); Hassan and Ahmad (1984); and U.S. women from Georgiou and Arquitt (1992).

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lowest fiber intakes. Clearly, all modern diets are much lower in fiber than the chimpanzee or hypothetical Paleolithic diet and than the 40 g/ day consumed by the Oto tribe, which appears to be a typical fiber intake for non-westernized people (Bingham, 1992). It is also important to point out that two of the non-westernized diets were considered marginal in their total energy content because of low total food availability. Assuming the people would eat more but in similar proportions, however, the relative amounts of macronutrients would not change. Overall, there is a clear suggestion of decreasing fiber intake through time or across subsistence strategies (Figure 6.1). AUSTRALOPITHECINE FEEDING AND NUTRITIONAL ECOLOGY Milton (1999b) has reviewed in detail the gut structure, plasticity, and kinetics of extant apes and modern humans. She concluded that the diet of the ancestral australopithecine was of similar quality to that of chimpanzees. In other words, no australopithecine species from the last common ancestor (LCA) of apes and humans to the earliest Homo would have significantly improved the quality of their diet compared to the LCA. This has been the traditional view (e.g., Aiello and Wheeler 1995). Variation in fiber concentrations among plant dietary items suggests an alternative hypothesis, however. We propose that the australopithecines significantly improved the quality of their diet compared to their forest ape ancestors as a result of a shift in plant diet. Our proposal starts by noting that the australopithecines could not be expected to have maintained a chimpanzee-like diet because they were living in a different environment from chimpanzees, specifically one in which chimpanzee-eaten fruits and piths would have been less available (Potts, 1998). A common chimpanzee response to seasonal scarcity in fruit is to rely on the consumption of piths of terrestrial vegetation (THV) (Wrangham et al., 1991). Given that these piths were not abundant in the drier and more open woodlands inhabited by the australopithecines, we propose that these early hominids would have adopted alternatives. Underground Storage Organs as Australopithecine Fallback Foods The process could have begun when, during periods of fruit shortage, very early australopithecines gravitated toward parts of the habitat that would have provided them with water and plants most similar to forest THV. Such habitats would have included wetlands, swamps, marshes, and river margins. Once there and attempting to harvest the pithy stems

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of wetland plants (just as gorillas do; Yamagiwa et al., 1992; White et al., 1995), these hominids could also have eaten the surface corms, bulbs, and rhizomes characteristic of some of these plants—especially of the sedges, reeds and rushes. From there, it would be a short step to relying more on USOs. The idea that USOs represented a novel, keystone dietary resource for early hominids is not new. Hatley and Kappelman (1980) suggested that australopithecines may have added USOs (roots, tubers, rhizomes, corms) to their diet, a food source underexploited by apes, past and present. A similar scenario is described by Wrangham et al. (1999) who outline the ecological, botanical, paleontological and anthropological reasons USOs would have made a particularly viable fallback food for early hominids. In addition to the fact that the biomass of USOs is higher in drier woodland and savanna habitats than in rain forests, such organs concentrate and store both nutrients and water underground when conditions are poor for plant growth above ground; this means that USOs are particularly nutritious at just those times of year when most above-ground plant parts are least abundant and least nutritious. Plant storage organs are most often located underground, often quite deep, in order to avoid predation. The fact that most USOs are thus unavailable to the majority of mammalian taxa (Wrangham et al., 1999), with the exception of suids and mole rats, would have meant that competition for these resources would have been low for any hominid capable of extracting them. Finally, both modern hunter–gatherers in tropical climates and savanna baboons and geladas rely heavily on USOs during lean periods. Assuming that australopithecines evolved from a frugivorous ape like the chimpanzee, what would have been the nutritional consequences of consuming roots instead of pith as a fallback food? We have already seen that pith contains 44% fiber (Table 6.1). And we also know that neither chimpanzees nor humans need a high protein intake (RDA, 1980; Conklin-Brittain et al., 1998), but that total nonstructural carbohydrates figure importantly in chimpanzee selectivity (Wrangham et al., 1991). Keeping these variables in mind, would wild roots and tubers add anything to the diet that piths cannot provide? To evaluate the nutritional feasibility of australopithecines consuming USOs, we examined the macronutrient content of wild roots and tubers. Table 6.4 compares the nutrient contents of twenty-eight wild woodland roots and tubers (Malaisse and Parent, 1985; Vincent, 1984) with nineteen domestic and semidomestic roots and tubers (Leung et al., 1968). The pith consumed by Kibale chimpanzees, from Table 6.1, and the average annual diet of chimpanzees are also included in Table 6.4 for comparison.

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Table 6.4 Nutritional Chemistry of Underground Storage Organs, Including Wild African Woodland and Savanna Species %CP

%fat

%TNC

%fiber

Underground Storage organs wild, n = 28 range

8.3 ± 8.8 1.0–39.2

4.0 ± 4.3 0.3–19.8

65.9 ± 16.4 17.4–92.5

16.2 ± 8.5 3.8–38.0

domestic, n = 19 range

7.0 ± 3.4 1.4–14.4

1.7 ± 4.6 0.3–20.0

82.1 ± 10.2 53.8–92.9

10.8 ± 14.0 2.3–63.3

pith, n = 19 range

9.6 ± 6.2 1.4–20.4

1.2 ± 1.6 0.2–7.0

31.9 ± 13.8 11.1–68.9

44.1 ± 14.3 24.5–79.3

whole diet, n = 12 range

9.5 ± 3.1 5.3–15.4

2.5 ± 2.1 0.6–8.2

38.8 ± 7.6 31.1–48.5

33.6 ± 4.5 20.7–37.6

Chimpanzee foods

CP = crude protein, TNC = total nonstructural carbohydrates.

Twenty-five of the wild roots and tubers were Zambian edible plants from an open woodland habitat, and three roots were from the Hadza, in a savanna environment. The domesticated root and tuber data were from various tropical habitats. On average, the wild roots and tubers were marginal in protein, but there is quite a range of values, offering the possibility for selection. Fat was probably adequate. The fiber values were determined using a long outdated method (crude fiber analysis), and values have been corrected by a factor of two, as previously described. Three would be the highest reasonable correction factor and would have resulted in fiber values of about 24% instead of 16%. Nevertheless, 24% is still much lower than that found in the Kibale chimpanzee diet as a whole. In particular, it is considerably lower than the 44% in piths, the chimpanzee fallback food. Consequently, including roots or tubers in the diet would decrease the fiber intake of a potential consumer and increase the nutrient content of the diet, especially the carbohydrate fraction. Our estimates for how this influenced overall diet are shown in Figure 6.1. DISCUSSION If underground roots and tubers were an important nutritional addition to the diet of australopithecines, they would have provided an

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adequate diet, even if eaten as the major food during periods of aboveground food scarcity. That such resources were indeed exploited by the australopithecines is supported by the unique masticatory adaptations characteristic of this hominid grade. Post-canine megadontia and low, rounded, thick-enameled cusps are all compatible with the physical challenges imposed upon the dentition by the consumption of USOs (Hatley and Kappelman, 1980; Wood, 1995; Teaford et al., this volume). The robust gnathic architecture of these hominids is also in keeping with the heavy chewing that would have been required to comminute USOs. Finally, the dental microwear patterns exhibited by these hominids, which indicate that small, hard, and/or gritty objects were being consumed (Grine and Kay, 1988; Teaford et al., this volume), are also consistent with the processing of these subterranean plant resources. There is no indication that australopithecines would have needed additional protein supplements to bring their protein intake to safe levels. Most important, the lower fiber values resulting from a significant USO diet would have improved the overall quality of their diet. We do not mean to imply that a need to decrease fiber in the diet was a driving force in the evolution of the hominid diet, which we assume was driven by changing patterns of food availability. The addition of USOs to the australopithecine diet and the resulting increase in the nutrient content of the diet, however, would have allowed an increase in net energy assimilation. The stage would then be set for Homo to further reduce fiber levels and improve the nutrient content of its diet. What might the implications be of this improved diet quality, specifically of the greater availability of carbohydrates, for the australopithecines? This “extra” energy could have been directed in several different ways, each of which has distinct evolutionary consequences. First, these hominids could have used this extra energy to achieve a faster rate of growth. Unfortunately, our ability to estimate growth rate from isolated and fragmentary fossil elements is extremely limited, but at this time it does not appear that this grade of hominid was any faster growing than Pan (especially in comparisons of females, the “ecological sex”) (McHenry, 1994; Kappelman, 1996; McHenry and Berger, 1998). Another possibility is that these early hominids upgraded their energy budgets and used this energy to range farther. Tantalizing evidence in support of this proposition comes from the newly discovered Australopithecus garhi, which possesses a hindlimb morphology suggestive of increased ranging (Asfaw et al., 1999). Alternatively, the energy surplus may have allowed a reduced gut size and increased brain size, following the arguments presented by Aiello and Wheeler (1995). Indeed, there is considerable empirical evidence that indicates that the later australopithecines

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did possess larger brains than the chimpanzee—perhaps 20% larger (see, for example, cranial capacity or encephalization quotient (EQ) estimates in Tobias 1971, especially for chimpanzees; McHenry 1994; Kappelman, 1996; Falk et al., 2000; Conroy et al., 2000). Classical discussions of increased brain size, both in Homo and australopithecines, always mention meat as the enabler (e.g., Conroy et al., 2000, p. 396). Our discussion presents an alternative and perhaps complementary hypothesis that increased encephalization was made possible by including lower-fiber USOs in the diet. CONCLUSIONS We have shown that the Kibale chimpanzee diet is low in fat, and we conclude that their protein needs are low to moderate since they survive well on a diet containing 9.5% of DM crude protein (Hill et al., 2001). In these respects, their diet is not particularly different from some modern human populations. However, chimpanzee fiber intake is very high compared to modern humans, making their diet substantially lower quality. Consistent with this trend in fiber reduction from chimpanzees to humans, we suggest that australopithecine diets had an intermediate fiber level as projected in Figure 6.1. Inclusion of a variety of USOs would have been responsible for this hypothesized lower dietary fiber content in australopithecine diets compared to chimpanzees. We suggest that greater reliance on USOs may have been an important nutritional contribution to increasing energy availability for australopithecines compared to their forest ape ancestors, and that this paved the way for further reductions in fiber concentration and increases in energy intake during the subsequent evolution of the genus Homo.

Chapter 7

Plants of the Apes: Is There a Hominoid Model for the Origins of the Hominid Diet? Peter S. Rodman

Reconstructing the origin of the diet of hominids has been examined most effectively by applying detailed comparative analysis to the dentitions and masticatory structures of fossil and living primates. The editors of this volume have been particularly important contributors to this work (Teaford and Ungar, 2000; Ungar, 2002). They, among others (e.g., Kay, 1977, 1984; Lucas et al., 1985), have gradually developed sophisticated techniques for examining relationships between size and shape of individual teeth, sub-parts of the dental arcade, the entire dentition, the surface morphology of the dentition, and, in particular, the alterations of the dental surfaces by differing patterns of diet in living primates (Ungar, 1994a, 1996b; Ungar and Teaford, 1996). There is a long history also of attention to the structural and chemical composition of primate foods (Agrawal et al., 1997; Hill and Lucas, 1996; Lucas et al., 1997; Lucas and Teaford, 1994) and to digestive structures associated with diets in living primates (Chivers and Hladik, 1980; Milton, 1987; Milton and Demment, 1988; Remis, 2000). Study of the feeding ecology of nonhuman primates appears to provide a strong comparative basis for reconstructing the history of primate diets with the promise of shedding light on the origins of the human diet (Milton, 1993) and even perhaps on dietary aspects of human health (Milton, 2000 and Chapter

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8 in this volume). Of course, any attempt to use comparative analyses of primate diets to understand healthy human diets must keep in mind that considerable cultural evolution has intervened between what may have been a human diet in evolutionary history and what we see as a human diet in the world today (Milton, 1999b; Stahl, 1984). Indeed, the diversity of diets on which humans persist, even in healthy conditions, suggests there is probably no single healthy diet, nor is there much likelihood that we may discover a narrow range of diets that will provide maximum health for all humans. This chapter does not address the nature of the human diet directly. Instead, I aim to use comparative analysis of the diets of our closest relatives—the great apes—to see if there might have been any unusual, derived hominid diet at the outset of hominid history. A Great Clade of Apes . . . The logic of comparative analysis in evolutionary studies suggests that examining the diets of close, living relatives may shed light on the diet of their common ancestors. The earlier separation of orangutans from the African clade, including proto-humans, is well established (Goodman et al., 1998; Ruvolo, 1997). Fossil evidence for the separation remains difficult to interpret at best, but the autapomorphies of teeth, face, and lower limb of Pongo and the clear synapomorphies of Gorilla and Pan (Huxley, 1870), as well as the great geographic separation of southeast Asia from Africa, indicate an earlier divergence of orangutans from the rest of us. Biomolecular studies confirm that orangutans belong to a sister clade to the African clade, and molecular dating has long placed the divergence of Pongo at somewhere before 10 million years before present (mybp) (Sarich and Cronin, 1976). . . . and the African Clade Divergence within the African clade clearly has occurred, although debate over the details of branching continues. Fossils do not yet clarify the history or timing of phylogenetic divergence among African apes, for there are few, if any, from the relevant time periods. Morphology tends to associate Pan troglodytes, P. paniscus, and Gorilla gorilla in a separate clade from humans, but molecules provide different, sometimes contradicting, results to different investigators. Molecular studies indicate a separation among the four African phyla five to eight mybp. Hominid fossils dating to 4.6 mybp or earlier do not contradict the

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molecular clock, and the primitive faces and teeth of those early hominids suggest a later rather than earlier split from Gorilla and Pan. Do the living great apes provide useful models for the earliest hominid diet? The phylogenetics of living hominoids suggests two important questions about diets of the apes vis-à-vis the diet of the human ancestor. First, is the diet of orangutans essentially the same as the diet of living apes of Africa? If so, a general conclusion will be that there is no special diet of African apes, although possibly there is a special diet of all great apes, and that the earliest diet of Hominidae probably was a general hominoid diet with no informative special characters. Second, if diets of Pongo and the African clade differ in any perceptible way, what are the different, possibly derived, primitive characteristics of African diets that probably were shared by the ancestral hominid? The answer to the first question seems to be “no.” A conclusion of this chapter will be that there is little need to pursue the second question.

Apes eat plants. Despite other incidental foods, the diets of great apes are comprised mainly of plant parts. They rarely eat other things, such as insects and meat, compared to the daily, even hourly, fare of plant parts. Chimpanzees, which by some analyses have a close phylogenetic relationship to humans (Ruvolo, 1997), hunt vertebrate prey and consume large numbers of social insects from time to time. These dietary items are very exciting, both to the chimpanzees and to the humans who watch them. They vary in presence and quantity from population to population, as well as from season to season within a population, however, and are not staples or significant components of daily intake. While the latter observations may not preclude a special nutritional role of fauna in the diet of Pan or the earliest hominid ancestor, the wide variation indicates that neither chimpanzees nor bonobos are obligate faunivores. It is unlikely that the common ancestor would have shared any special physiological or morphological adaptation to faunivory since no such adaptations are apparent in Pan, Gorilla, or Pongo. Others have approached this issue with much greater care from different perspectives and arrived at this conclusion (Milton, 1987; Milton, 1993; Milton, 1999b; Milton, 2000; Teaford and Ungar, 2000; Chapter 8 in this volume). My approach to the central questions about great apes and the origin of hominid diets is to examine the composition of diets of the great apes by plant taxon and plant part and to describe as precisely as possible the taxonomic overlap of the floral component of diets of the four great apes. Taxonomic accuracy is fundamental to this effort. A large part of the value of this investigation has been reconciling and

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standardizing taxonomic details of plant lists and correcting published errors in plant classification to allow confident comparisons among studies and sites. The detailed results of these taxonomic revisions are available upon request to anyone who wishes to use the database. METHODS Data Sources Lists of plants and parts consumed by great apes came from twentynine sites in thirty-six studies (Table 7.1 and Figure 7.1), including twenty-three sites for gorillas, chimpanzees, and bonobos and six sites for orangutans (Figure 7.1). Most lists have been published or presented in dissertations, but in a few cases the investigators kindly provided unpublished results. These are reported as personal communications.

Taxonomic identifications. The precise method of identifying taxa of plants in each study is important and includes at least the following variations: 1. Indigenous names of plants reported to be foods by reliable local assistants (but not directly observed), converted to Latin binomina according to an existing list of correspondence between Latin and local names; 2. Local names of foods observed during a particular study, again converted using Latin-local correspondences; 3. Identifications in the field by observers referring to local collections previously identified in some way or another; 4. Latin names assigned to specimens collected during the study at herbaria by botanists familiar with the flora of the study area; or 5. Identifications by herbaria enlisting the assistance of experts in the family of each specimen. The equivalence of indigenous names and scientific identifications and consistency of indigenous identifications among local assistants are important to many of us because we have often relied on the names and one or more assistants to identify plant taxa. The subject has been discussed formally by Richards (1996). Often we have little information about consistency and error by local informants or among several local people, since those who rely on local assistants rarely assess this source of error. I have chosen to accept the judgment of each investigator. To do otherwise is beyond the scope of this paper.

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Species epithets no doubt are often assigned to less-than-perfect samples without the particular specimen being examined by the reigning expert(s) on the taxon. If so, it is more likely that similar morphologies belonging to distinct species may be assigned the same name within sites or between sites. If so, species diversity within sites or for each ape may be underestimated, and species overlap between sites and between apes may be overestimated. Generic assignments are probably reliable, however, and family assignments are reliable. Future analysis at lower levels will be important and possibly more revealing, but the current analysis relies primarily on identifications of plant families.

Plant parts. Identifications of parts of plants from diverse studies devolve here to a set of seven, including: Fruit: The pulp, or mesocarp, of the fruit of a plant. Some investigators either could not or did not separate ingestion of pulp alone from ingestion of pulp and seed, and in some cases, the seed was likely to have been digested. Seed: The seed of the plant if consumed rather than eliminated prior to or after passing the gut. Again, actually consuming the seed should imply the seed was digested, but the distinction between seed and fruit is not consistent among studies. Seed and fruit might be combined for comparisons since there are so few taxa identified only for seeds. Flower: There is probably not much variation among identifications of this part, although the form of some flowers is confusing and might be confounded with fruits by the nonexpert (e.g., Rodman, 1973, for “fruits” of Dillenia). Leaf: Many investigators separate young and mature leaves for good reasons, but here I combine all leaves into a single category since not all investigators made the distinction. Pith: This item has quite special meaning in some studies of African apes (White et al., 1995; Wrangham et al., 1993). In other studies, pith includes the stems of many plants, and I have classified leaf stems and petioles as pith since they are often not distinguished. Bark: The actual structure consumed is usually not the whole bark, but is the inner layer (cambium, or, more precisely, phloem) of the bark, but for some plants is the whole bark. These distinctions are seldom made, although some investigators describe details of consumption while classifying the item simply as bark. Other: The rest of plant parts, including, most frequently, roots and dead wood.

Table 7.1 Sites and Sources for Plant Lists Analyzed in this Chapter Country

Position

Hominoid Species

References

01° 28′ S, 29° 29′ E 01° 04′ S, 29° 38′ E 03° 52′ N, 16° 30′ E

Gorilla g. beringei Gorilla g. beringei Gorilla g. gorilla

Watts, 1984; McNeilage, in press; Schaller, 1963 Berry, 1998 Remis, 1994; Goldsmith 1996

02° 23′ N, 10° 3′ E 03° 22′ N, 16° 10′ E

Gorilla g. gorilla Gorilla g. gorilla

Calvert, 1985a Fay, 1997

02° 21′ N, 16° 16′ E

Gorilla g. gorilla

D. Doran, personal communication, 12/01/2000

KAHUZI

Rwanda Uganda Central African Republic Cameroon Central African Republic Central African Republic D. R. Congo

02° 16′ S, 28° 45′ E

Casimir, 1975; Yumoto et al. 1994

ITEBERO

D. R. Congo

01° 42′ S, 27° 55′ E

LOPE

Gabon

00° 10′ S, 11° 35′ E

NDOKI

R. P. Congo

02° 18′ N, 16° 22′ E

MT. ASSERIK BELINGA

Senegal Gabon

12° 53′ N, 12° 46′ W 01° 10′ N, 13° 10′ E

Gorilla g. graurri Pan t. schweinfurthii Gorilla g. graurri Pan t. schweinfurthii Gorilla g. gorilla Pan t. troglodytes Gorilla g. gorilla Pan t. troglodytes Pan t. verus Gorilla g. gorilla Pan t. troglodytes

KARISOKE BWINDI BAI HOKOU

82

CAMPO NDAKAN MONDIKA

Yamagiwa, 1994 Tutin, 1994 Nishihara, 1995, Moutsambote et al. 1994 McGrew et al. 1988 Tutin and Fernandez, 1985

OKOROBIKO SEMLIKI UGALLA GOMBE MAHALE KIBALE NGOGO LOMAKO WAMBA YALOSIDI LILUNGU MENTOKO

Equatorial Guinea Uganda Tanzania Tanzania Tanzania Uganda

83

Uganda D. R. Congo D. R. Congo D. R. Congo D. R. Congo East Kalimantan, Indonesia ULE SEGAMA Sabah, Malaysia SUNGAI WAIN East Kalimantan, Indonesia TANJUNG Central Kalimantan, PUTING Indonesia KETAMBE Aceh, North Sumatra, Indonesia GUNGUNG West Kalimantan, PALUNG Indonesia

01° 30′ 00° 50′ 05° 19′ 04° 40′ 06° 07′ 00° 34′

N, 09° 53′ E N, 30° 20′ E S, 30° 37′ E S, 29° 38′ E S, 29° 44′ E N, 30° 22′ E

Pan Pan Pan Pan Pan Pan

t. t. t. t. t. t.

troglodytes schweinfurthii schweinfurthii schweinfurthii schweinfurthii schweinfurthii

00° 30′ 00° 51′ 00° 11′ 01° 52′ 01° 22′ 00° 24′

N, 30° 26′ E N, 21° 05′ E N, 22° 28′ E S, 22° 57′ E S, 23° 56′ E N, 117° 16′ E

Pan t. schweinfurthii Pan paniscus Pan paniscus Pan paniscus Pan paniscus Pongo p. pygmaeus

Sabater-Pi, 1979 Kevin Hunt, personal communication, 9/14/2000 Moore, 1994 Wrangham, 1975 Nishida and Uehara, 1983 Richard Wrangham, personal communication, 9/18/2000 Mitani, in press; Ghiglieri, 1984 Badrian and Malenky, 1984 Idani, 1994 Kano, 1983 Sabater-Pi and Vea, 1994 Rodman, 1973; Rodman et al., unpublished data

05° 11′ N, 117° 54′ E 01° 10′ S, 116° 50′ E

Pongo p. pygmaeus Pongo p. pygmaeus

MacKinnon, 1974 A. Russon, personal communication, 9/16/2000

2° 45′ S, 111° 57′ E

Pongo p. pygmaeus

Galdikas, 19778

3° 40′ N, 98° 00′ E

Pongo p. abelii

Manullang, 1999; Rijksen, 1978; Ungar, 1995

01° 13′ N, 110° 07′ E

Pongo p. pygmaeus

Cheryl Knott, 1999 personal communication, 10/15/2000

Figure 7.1 Equatorial Africa and Malesia, indicating the locations of twenty-nine studies of apes from which lists of food plants have been analyzed in this study.

84

85

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None of these categories is either unequivocal or completely consistent between studies. The extent of consistency depends entirely on the detail given by original investigators. Resolution and information would be best if all parts had been clearly identified in the same way across studies, but this has not been done and will not be fixed entirely without input from original investigators or additional detailed field research. Certainly one lesson from the attempt to compile work from multiple studies is that those who carry out field studies should adopt some standard procedures for reporting information about dietary items. Reconciling and Standardizing Taxonomy I entered one record per plant part for each species identified in each study. Each record consists of sixty-one items, including the record number, family, genus, and species of the plant and a “1” or “0” for the presence or absence of each of the seven plant parts for each of the four apes and “1” or “0” for presence or absence at each of twenty-nine sites. Each distinct “unidentified” species was entered as a separate record; “unidentified” species included any species indicated as “unidentified,” as “?” as “cf. ”, or as any other indication of uncertainty. If the investigator recorded multiple different species or morphotypes with numbers (e.g., “Ficus sp. 1, Ficus sp. 2 . . .”), these were entered as different records initially for the purpose of counting species at each site, but only one unidentified species per genus and one unidentified genus per family remained in the set as it was summarized at higher levels of classification. The records were sorted by genus and species and inspected visually and digitally to discover any names that differed only slightly. Spelling errors frequently occur in the published records, and I introduced new errors while transcribing lists into my database. Common errors of reporting include omitting vowels (e.g., omitting the “i” in endings such as “-ia”), doubling consonants that should not be doubled or omitting consonants that should be doubled, and substituting various vowels for each other. Common discrepancies among sites and investigators included using different “standard” endings for names (e.g., “-a” for “-um” and “-um” for “-on”). Discrepancies were resolved with reference to several electronic databases (Dallwitz, 1980; Dallwitz et al., 1993 onward; Dallwitz et al., 2000 onward; Farr et al., 1979; Farr and Zijlstra, 1996 onward; Royal Botanic Gardens et al., 1998 onward; Watson and Dallwitz, 1991; Watson and Dallwitz, 1992 onward). If multiple spellings of a very similar name occurred in the original lists, but only one spelling matched in, for example, the list of taxa in the

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International Plant Names Index (Royal Botanic Gardens et al., 1998 onward), the latter spelling was used. Once internal consistency of names seemed adequate, I checked the lists of species epithets and names of genera against the largest lists of plant names I could obtain. Names reported for foods of apes that did not match any name in an existing compendium were checked further. In virtually all cases, I could determine either that the questioned plant name reported is in use, but omitted from the reference lists, or I could conclude reasonably confidently that the spelling in my database nearly matched an existing name in a standard list from the family to which the plant had originally been assigned. If so, I corrected the name of the species or genus for all records in the database. Original investigators have assigned a few existing species names to genera that do not approximate names in standard references, but they have assigned the species to families in which the species epithets are used. Occasionally the name reported could be found as a synonym or other outdated or defunct name within a family, and often the species name might be found assigned to only one existing genus in the same family. In either case, I assigned the species to the most likely genus. The former correction is highly likely to be valid. The latter corrections are less satisfactory, but if a species epithet had been assigned to only one genus of a family, I felt confident that substituting the generic name in use for the reported species was reliable. Otherwise, the species and genus were converted to “unidentified.” Analysis Results presented here are primarily descriptive. The nature of the data does not lend itself to parametric tests. Methods of assessing confidence in the answers to the few central questions are addressed in conjunction with the results presented as answers to those questions. RESULTS Plant Diversity Among Sites and Apes

Diversity of plants at different sites. The full database currently consists of 2,948 records that sort into 1,760 species in 770 genera and 144 families. Table 7.2 enumerates families, genera, and species reported for each site, with sites ranked from highest number of species per family to lowest. Diversity measured by total families, total genera, or total species, as well as by numbers of genera per family and numbers of species per genus are highly correlated with species per family (minimum

Table 7.2 Plant Taxa Enumerated by Site Genera Site

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Sungai Wain Ndoki Wamba Gunung Palung Mahale Kahuzi Mentoko Tanjung Puting Gombe Mondika Lomako Lilungu Karisoke Bai Hokou Lope

Species

Families

Total

Identified

Total

Identified

54 47 38 53 64 38 34 54 51 38 28 44 27 42 36

124 120 98 121 156 83 63 98 110 78 60 100 53 86 75

111 114 98 121 153 82 59 96 110 78 59 98 53 83 73

201 173 138 183 196 116 102 154 145 107 75 116 71 105 89

125 154 129 80 176 106 63 120 130 100 61 100 63 71 79

Genera Species per Species per Per Family Family Genus 2.30 2.55 2.58 2.28 2.44 2.18 1.85 1.81 2.16 2.05 2.14 2.27 1.96 2.05 2.08

3.72 3.68 3.63 3.45 3.06 3.05 3.00 2.85 2.84 2.82 2.68 2.64 2.63 2.50 2.47

1.62 1.44 1.41 1.51 1.26 1.40 1.62 1.57 1.32 1.37 1.25 1.16 1.34 1.22 1.19

89

Ndakan Kibale Ule Segama Ketambe Belinga Ngogo Itebero Mt. Asserik Campo Okorobiko Yalosidi Ugalla Semliki Bwindi

35 49 35 44 30 12 52 24 31 24 23 17 13 37

77 90 57 80 59 20 86 36 42 31 33 22 16 43

70 90 56 74 58 20 86 36 42 31 33 21 16 42

85 119 84 105 71 28 120 41 50 37 33 24 17 47

51 113 48 67 55 27 113 41 36 33 33 12 14 31

2.20 1.84 1.63 1.82 1.97 1.67 1.65 1.50 1.35 1.29 1.43 1.29 1.23 1.16

2.43 2.43 2.40 2.39 2.37 2.33 2.31 1.71 1.61 1.54 1.43 1.41 1.31 1.27

1.10 1.32 1.47 1.31 1.20 1.40 1.40 1.14 1.19 1.19 1.00 1.09 1.06 1.09

Median Values

37

77

73

102

67

1.96

2.47

1.31

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rs = 0.66, p < 0.02) as is visible more or less by inspection of Table 7.2. One might be concerned that variation in the nature of the studies (duration, intensity of effort to identify plant foods, etc.) might contribute more to differences and similarities among the sites or the apes than variation in the sites or the apes themselves. Several comparisons allow confidence that the variation in diversity reported is real. First, although studies at Mt. Asserik, Semliki, and Ugalla were brief compared to the long-term research at Mahale and Gombe, the former sites are all largely dry savanna, which is unusual habitat for chimpanzees (Moore, 1994; McGrew et al., 1988; Hunt, personal communication). Thus, the diversity of plant taxa should be lower at these sites, which it is. Second, variation among Asian sites also indicates biological reality in the data of Table 7.2, because four sites close to the equator (Gunung Palung, Tanjung Puting, Sungai Wain, and Mentoko) have higher measures of plant diversity than do the two sites at somewhat higher latitudes (Ulu Segama and Ketambe).

Diversity of plants and diets of the apes. Table 7.3 enumerates families, genera, and species for each of the apes. Results from all sites for each species are combined. Absolute numbers of each taxonomic level are lowest for bonobos and highest for gorillas. Data from this table are translated into a representation of diets of the apes in Figure 7.2, which shows the percentages of all plant species from which each plant part is taken at least once by each species of ape. One obvious impression from the visual comparisons in this figure is a great similarity in proportions of families from which various parts are taken. The three African species resemble one another and differ from orangutans in the higher proportions of families of plants from which they take leaves, though; G. gorilla stands out for the high proportion of species from which it takes leaves. G. gorilla is also the only one of the four apes that takes fruit from less than 60% of all families from which it feeds. Comparisons at the level of plant genus and family produce more extreme difference between gorillas and the other apes (Table 7.3). Gorillas take leaves from a greater proportion of higher plant taxa than fruits. The opposite is true for Pan and Pongo. This is no surprise, but the result based on a very broad enumeration of plant taxa from all known sites underscores the point that regardless of diversity of fruits in the diets of gorillas at many lowland sites, the gorilla is more of a folivore than any of the other great apes. Table 7.4 shows measures of diversity in plant foods for the apes similar to the measures for sites described previously. Diversity of plants is lowest for bonobos for all measures and generally highest for orangu-

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tans. It may be interesting that diversity in diets of bonobos contrasts with the rankings of diversity for sites where P. paniscus has been studied (Table 7.2). Wamba, Lomako, and Lilungu all fall above the median for ape sites. Yalosidi ranks quite low on the list of sites, however, and so differs strongly from the other sites, either because bonobos at Yalosidi are more selective, plant diversity at Yalosidi is lower, or the study at Yalosidi has been less intense than at the other three sites.

Family representation among sites and among apes. Fifteen families account for 50% of all plant species in the sample. Table 7.5 shows these families and how they are represented among the twenty-nine study sites and the four species of apes. The cumulative percentages of species in these families for each site, for each of the great apes, and for the sample as a whole are presented, with sites ranked by the percentage of total species accounted for at each site by the top fifteen families for the whole sample. The fifteen families in this set are very familiar in primate studies since all are well known sources of food for primates generally. Moraceae clearly are the most speciose of the whole sample, accounting for 6.8% of all species in the sample, but at most, 0.2% at any one site. This discrepancy reflects the great diversity of figs and differentiation among communities of figs from location to location. Euphorbiaceae are common in the whole sample, accounting for 5.3% of all species, consistently high proportions at the Asian sites, and strikingly high proportions at a few African sites, including Wamba, Semliki, and Yalosidi. Several sites stand out as unusual in this measure of plant composition of ape diets. The top families for the whole sample comprise less than 30% of species at Kibale, Bwindi, Kahuzi, and Campo. Overlap Among the Dietary Components of the Apes A central question in this analysis is the extent to which Pongo pygmaeus resembles or differs from the African apes. Many different comparisons may be made among the apes with respect to the composition of their diets as described by the data presented here. As a first step in the comparison for this project, I evaluated the overlap among the four great apes at the family level. There are two aspects to the comparison: actual overlap in use of families and utilization of plant families in relation to the distribution of those families between equatorial southeast Asia and equatorial Africa.

Family overlap. The simple question here is, “what proportion of all families does each of the great apes share with each other?” Figure 7.3 presents this information for the entire set of plant families and apes,

Table 7.3 Enumeration of Plant Taxa by Species of Age and Plant Part No. Genera

No. Species

No. Families

Total

Identified

Total

Identified

Gorilla gorilla

All Fruit Seed Flower Leaf Pith Bark Other

105 66 24 16 86 48 41 57

360 199 37 19 239 93 84 108

347 192 37 18 231 91 83 106

662 366 55 21 354 157 111 150

551 305 52 17 287 130 96 133

Pan troglodytes

All Fruit Seed Flower Leaf Pith Bark Other

94 77 22 32 66 32 27 53

348 226 46 50 177 59 40 125

340 220 46 49 175 58 40 123

631 421 62 58 261 87 57 167

571 382 58 55 236 80 56 157

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Plant Part

93

Pan paniscus

All Fruit Seed Flower Leaf Pith Bark Other

57 44 10 9 30 12 0 19

169 119 21 13 70 21 0 4

167 118 21 13 70 21 0 36

257 179 26 13 86 31 0 47

227 160 24 13 78 25 0 40

Pongo pygmaeus

All Fruit Seed Flower Leaf Pith Bark Other

86 70 37 17 49 13 32 36

283 198 69 22 97 26 62 66

261 190 69 21 86 24 52 64

620 442 105 26 136 39 103 80

425 326 54 13 79 26 59 35

Figure 7.2 Utilization of plant parts. For each species of great ape, the bars indicate the percentage of all identified species from which each plant part has been recorded as a food.

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Table 7.4 Diversity of Taxa in Diets of Four Great Apes

Gorilla gorilla Pan troglodytes Pan paniscus Pongo pygmaeus

Genera per Family

Species per Family

Species per Genus

3.43 3.70 2.96 3.29

6.30 6.71 4.51 7.21

1.84 1.81 1.52 2.19

independent of part taken from each plant family. Figure 7.3E shows the percentage of all families used by each of the apes for any plant part. The percentages come from the same database used to derive Table 7.3, with G. gorilla including the highest and P. paniscus the lowest total number of families. Figure 7.3A to 7.3D show the overlap of G. gorilla, P. troglodytes, P. paniscus, and Pongo pygmaeus with each of the other apes as the percentage of families shared out of the maximum number of families that could be shared in each pair. The maximum number of families that could be shared is, of course, the smaller total of families in each pair. Thus, for example, G. gorilla uses parts of a total of 105 families, but takes parts of 50, or 87.7%, of the 57 families used by P. paniscus. Measured in this way, there is no question that African apes overlap with each other more than each does with P. pygmaeus, which is hardly surprising since the families available to the African and Asian apes are not precisely the same. Within this comparison, it is of some interest that greatest overlap between Africa and Asia is between P. paniscus and P. pygmaeus (Figure 7.3D), and that within Africa, the greatest overlap is between G. gorilla and P. paniscus (Figure 7.3A and 7.3C). Patterns of overlap between apes by plant part used for each family are presented in similar fashion in Figure 7.4, which consists of one chart for each of the seven plant parts. In each chart, overlap is again presented as a proportion of the smaller total of families for the pair of species. In addition, in each chart, a bar indicates the proportion for each ape indicating the proportion of all its total families from which it takes that plant part. In all but one case, this is the highest proportion in each set. G. gorilla shares a higher proportion of families as fruit sources with P. paniscus than the proportion of families in its total set from which it takes fruit. Once again, it is clear that African hominoids share more

Table 7.5 Families Comprising 50% of Species (entries are percentages).

96

97

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Figure 7.3 General overlap of plant utilization among the four great apes. A to D: The bars indicate the percentages of plant families shared by each great ape with each other. These overlaps are calculated using the smaller total families in each pair of apes as the denominator. E: The bars show the proportions of all plant families used by each of the apes.

families with each other for all plant parts, but overlap of families that are sources of leaves, bark, and pith for P. pygmaeus and G. gorilla are notably high (proportions shared are more equal to proportions in the set for P. pygmaeus than for other plant parts). Apes and Angiosperms The primary question to be answered in this meander through the forest of plants of the apes is whether diets of orangutans can in any way be differentiated from diets of African apes as a clade. The answer to the question determines the extent to which we might expect something about food choice within Africa to have characterized the earliest hominids as well as living African apes. Comparing use of plant taxa between equatorial Africa and Malesia in the manner carried out so far shows that African apes do differ from orangutans, although, at least subjectively, none of the differences is particularly striking. The differences between Gorilla and Pan (both species) seem as interesting as those between either African genus and Pongo. The lack of significant differentiation becomes clearer if we consider utilization of plant families in

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proportion to the occurrence of those families in the two regions. I do not have information on all families, but the angiosperms have been coded for geographic region within the Families of Flowering Plants (FFP) database (Dallwitz et al., 2000 onward) so that it is possible to separate out the families that occur in equatorial Africa only, in Malesia only, and in both regions. If families are selected in proportion to their occurrence in the two regions by the apes, the evidence indicates that the apes are selecting similarly from the families available. This might be for one of two reasons. Perhaps hominoids select particular families in both places or, alternatively, simply feed on the products of plants more or less in proportion to the occurrence of those families, whether in Africa or in Asia. In the FFP database 359 angiosperm families are coded as occurring in equatorial Africa, Malesia, or both regions. We already know that the apes take parts of only 144 different families (named according to the family assignments in the FFP), or almost precisely 40% of all families that are known to occur in equatorial regions of the Old World. One part of the answer to the question is that hominoids do select among families that might be available to them as foods. There does appear to be a hominoid diet consisting of parts of 40% of possible families of plants in the Old World tropics. Whether this diet is different from a general catarrhine diet is not known from this simple observation, although direct observations in Africa suggest that it is different in quality (Conklin-Brittain et al., 1998; Wrangham et al., 1998; Chapter 6 in this volume). A second step in answering the question is to ask whether the great apes as a group select from families in proportion to their occurrence in the two regions. In other words, if the angiosperm food sources of all four apes are separated into those that occur in Africa only, Asia only, or both regions, are the proportions the same as the proportions of all angiosperm families in the same categories? Figure 7.5A presents the data comparing families of plants of the African apes as a group with those of P. pygmaeus. A simple χ2 test of proportions reveals that the two distributions are not the same (χ2 = 8.80 with 2 d.f., p = 0.025). Inspection of individual cells of the table for the test shows, however, that proportions of angiosperm families shared between African and Asian great apes do not differ from the proportions of angiosperm families shared between the two regions (χ2 = 1.63 with 2 d.f., p = 0.40). Furthermore, a simple comparison of the distributions of angiosperm families of the genus Pan (both species) with Pongo for the two regions (Fig. 7.5B) shows no difference (χ2 = 2.53 with 2 d.f., p = 0.56). Finally, comparison of angiosperm families used by Gorilla with those of Pongo in

Figure 7.4 Overlap of plant utilization by plant part among the four great apes with proportions calculated using the smaller total families in each pair. In each histogram, the bar for overlap of a species with itself shows the proportion of all families used by that species of ape as a source of that food item.

100

101

Figure 7.5 Proportions of angiosperm families (open bars) occurring in equatorial Africa only, in both equatorial Africa and Malesia, and in Malesia only, compared with the proportions of families used by (A) African apes only, both Pongo and the African Apes, and Pongo only; (B) Pan only, Pongo and Pan, and Pongo only; and (C) Gorilla only, Pongo and Gorilla, and Pongo only (filled bars in each histogram).

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the same way (Fig. 7.5C) reveals a strongly different distribution from the distribution of angiosperm families among the regions (χ2 = 18.32 with 2 d.f., p = 0.00021). The latter difference is entirely due to disproportionately high use of African families by Gorilla. A preliminary interpretation of these few forays into comparative plant use is that the great apes are fundamentally the same in selection of angiosperm families, but that G. gorilla is specially adapted for a new feeding niche in Africa. Special adaptation of G. gorilla is not a surprise given all that is known of dietary capacities of this huge ape. Clusters of Sites and the Geography of Food Lists A conclusion from the previous results may be that the great apes feed more or less on what is available to them rather than selecting a set of plants to which they each are specially adapted. If this is so, the plant lists from different sites should not converge, but instead should reflect differences in the plants available at the sites. I have approached this hypothesis using information on plants included or not included in diets of the apes at each of the twenty-nine sites as variables in a cluster analysis of the sites. The data consist of observations of 117 families that are used or not used at more than one site. Each family is therefore a binary variable. Families occurring at twenty-two or more sites or at seven or fewer sites were treated as asymmetric in the analysis. Asymmetric binary variables are those for which presence or absence is a rare event, and only presence is of importance. The families that occur at only one site (n = 27) convey no information and are omitted from the analysis. Families that occur at eight to twenty-one sites are treated as symmetric binary variables, for which both presence and absence convey information. Thus, the apes have selected foods from families or not at each of twenty-nine sites, and their selections are now treated as variables for hierarchical classification of the sites. If the apes tend to choose the same subsets of foods at different sites, their selections should reflect only their dietary preferences. If, on the other hand, apes select from families more or less as they are available at the sites, their selections should cluster the sites according to similarity and difference among the sites. In other words, if they are not particularly selective in choosing among families, we should expect the sites to cluster in some sensible way related to geography and habitat. Figure 7.6 shows the results of the hierarchical analysis of a simple unweighted group average method of clustering, in which the distance between two groups is defined as the average distance between each of their members, as implemented in NCSS™ (Hintze, 2000). Inspection

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Figure 7.6 Hierarchical clusters of 29 great ape sites using 117 plant families as binary variables (present or absent). The clustering technique is a standard unweighted average grouping. Compare the clusters with the locations of sites in Figure 7.1.

reveals four primary divisions: southeast Asian sites (Ketambe, Gunung Palung, Tanjung Puting, Sungai Wain, Ulu Segama, and Mentoko), mountain gorilla sites (Karisoke, Kahuzi, and Bwindi), forested chimpanzee sites (Kibale, Mahale, and Gombe), and the rest of African sites (n = 17). Clearly, each of the first three clusters is “sensible” geographically (Figure 7.1) and ecologically. Within the Asian sites, Ketambe in North Sumatra is separated from the five sites on Borneo, and within the group on Borneo, the most eastern sites (Ulu Segama and Mentoko) are separated from the rest. Sungai Wain is a bit out of place, but it is also a site populated by rehabilitant orangutans. In a sense, it is impressive that Sungai Wain clusters so closely with the rest of the Bornean sites. That it does supports the inference that these apes select the foods available to them. In southeast Asia, clearly the choice of families for

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foods reflects geographical variation in sites, not special selection by a specialized feeder. Within the large cluster of seventeen remaining African sites, there are several clear geographical and ecological clusters. One lower level cluster consists of rich, wet tropical sites, and within it are three geographically sensible subgroups. The four sites from the same reserve in the southern tip of the C.A.R. (Ndakan, Ndoki, Mondika, and Bai Hokou) cluster together. The four sites of studies of studies of P. paniscus, all located in the southern drainage of the Congo River, cluster closely. The two sites where both G. g. gorilla and P. t. schweinfurthii coexist in Gabon (Lope and Belinga) are paired. Itebero is a lowland site located in the same reserve as Kahuzi, but in quite different environment. G. g. grauri and P. t. schweinfurthii occur at both sites, but Itebero segregates clearly from other sites nearby, as well as from other lowland sites; it is unique in its combination of location and ecology, and the families chosen as foods by the apes at that site mark it as unusual. Mount Asserik, the only West African site and the only site from which data are reported for P. t. verus, clusters with a more eclectic assortment of others, but this subgroup includes both those that are geographically closest (Campo and Okorobiko) and those that are most similar ecologically for chimpanzees (Semliki and Ugalla). Ngogo by all prior expectations should cluster with the other lush East African sites of chimpanzee studies and especially with Kibale, since it is part of a contiguous area with Kibale. Data from Ngogo are unusually constrained because only the top twenty fruit sources are reported by Mitani and Watts (Mitani and Watts, 2001), and Ghiglieri’s observations of unhabituated chimpanzees at Ngogo were highly biased toward large fruiting trees (Ghiglieri, 1984). The data set from Ngogo may not reflect the choices of the resident apes as much as the nature of the reports of their foods so far. The cluster analysis makes geographic and ecological sense. It is as if one had a list of possible families of food plants in hand and then selected those that were available in each site, resulting in a set of foods that fairly accurately reflect the geography and ecology of the locations, even though only a part of all available plants is on the list. The approach may be oblique, but both the congruence of Asian apes and African apes—except for an African specialization in G. gorilla—and the absence of selectivity of plant families that would have obscured the obvious geographical and ecological clusters point to one conclusion: There is no special dietary pattern of African great apes, and in all great apes, the animals choose what is present where they feed, rather than selecting a narrower set of foods at each site.

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A Tree of Apes One final analysis supports the conclusion that dietary selection of the great apes is homogeneous, not heterogeneous, and therefore not reflecting subspecialization within the great ape department. I applied a similar hierarchical analysis to the diets of the four apes, in this case limiting the families to those that occurred in food lists for two or three of the four and treating all as symmetrical binary variables. Figure 7.7 shows the simple resulting tree. Phylogeny or convergence may be reflected in the association of P. troglodytes with G. gorilla; but their association in this analysis may also reflect the reasonable number of studies of sympatric chimpanzees and gorillas in which the available foods would be the same for the two (n = 5; Table 7.2). There is clearly no phylogenetic sense to the association of P. paniscus and P. pygmaeus nor to their splendid separation from the others. With some mental gymnastics one might construct a post hoc ecological hypothesis for the association, but in the context of this analysis, the implication of the tree is simple: The four great apes interdigitate, independent of Asian or African origin. In Figure 7.7 Hierarchical tree of relationships of the great apes based on all families that were used by two or three of the four species for any food part (n = 34 families). The families are treated as binary variables (present or absent). The clustering technique is a standard unweighted average grouping.

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an effort to determine how robust the interdigitation of the apes might be, I tried clustering the four apes using a set of 256 genera shared by two or three of the apes, and the result was similar. Changing the clustering technique had little effect, although it was possible to produce a tree that grouped Pongo with P. troglodytes and G. gorilla, leaving P. paniscus to the side. Since the list of families for P. paniscus is short, it seemed possible that the position of P. paniscus might have resulted from lack of information. I tried randomly removing half the families that did not appear in the list for P. paniscus (thus shortening the lists for the other three apes while not changing the list for P. paniscus), but the result was identical to that in Figure 7.7. There seems so far to be no way to bend the data to isolate Pongo from our African cousins using information on plant taxa in their diets. All four of them, with some minor difference in G. gorilla probably reflecting choices of leaf sources in Africa, constitute a homogeneous set. Great apes are great apes, dietarily, and it is highly likely that the earliest hominid ancestor was simply another of this quite undifferentiated group, exploiting whatever subset of African plant families was left by chance during its initial isolation, wherever that may have been. DISCUSSION AND CONCLUSIONS Direct investigation of the chemistry and structure of diets of coexisting chimpanzees and cercopithecoid monkeys in the Kibale forest has already demonstrated three critically important points (ConklinBrittain et al., 1998; Wrangham et al., 1998): First, the diet of the hominoid differs from the diets of the cercopithecoids; second, the diet of the hominoid is less toxic and of otherwise higher quality than the diet of the cercopithecoids; and third, that our predictions about this difference were wrong. It would have been expected that the large chimpanzee could handle the more toxic, lower-quality diet, while the smaller cercopithecoids would have been constrained to seek out higher-quality intake. These results apply to the current work because they suggest an early divergence of dietary adaptation between the two branches of Catarrhini. It is likely that the subset of families used by hominoids (only 40% of all angiosperm families available in their regions) will turn out to be characterized by the qualities that Wrangham and Conklin have found in diets of chimpanzees of Kibale. Tentatively, with the caveat that only this one study has shown the result, there is a clear hominoid diet. Observations of the three hominoids and three cercopithecoids that coexist at Ketambe show that there is uniformity of food plants comprising the diets of each superfamily, but clear differentiation of the plant

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choices of the two superfamilies (Rodman and Manullang, unpublished date). These results provide further support for the conclusion that there is a true hominoid diet that is distinct from a general catarrhine diet, and certainly distinct within the large set of primate diets. They also suggest that Hylobates is part of the hominoid dietary set, though it will be of great interest to discover where Hylobates falls in a broader analysis than the one introduced here. There is a subset of plants that constitutes the diet of great apes, but selection among the members of that subset appears to be quite free. There is little further specialization among the four great apes. Similarity of Pongo to Pan, and in most respects of Pongo to Gorilla, leads to the conclusion that there is no special diet of the African apes within the hominoid spectrum. Since that appears to be true, it is most likely that the diet of the earliest Hominidae was the same, and that it most resembled the diets of Pan and Pongo. In the past it has been thought that hominid origins were associated with radical changes in habitat and feeding niche (Jolly, 1970; Peters, 1981). Feeding specialization may have been part of the initial differentiation of human ancestors from some Pliocene ancestors of Gorilla and Pan, and Teaford and Ungar (2000) make this case from details of structure and wear on a small sample of teeth of early hominids. Recent evidence that the earliest hominids occupied forested habitat rather than radically different open habitat makes those earlier scenarios less necessary, if not less likely. The homogeneity of hominoid diets shown here suggests it is at least equally likely that the earliest Hominidae retained the hominoid dietary pattern while perhaps obtaining it in a different manner (Rodman and McHenry, 1980). How similar diets may be obtained in very different ways by coexisting primates is well illustrated by the coexisting pig-tailed and long-tailed macaques of southeast Asia (Rodman, 1979; Rodman, 1990). Regardless of the details of the foregoing speculation, this analysis of plants of the apes tentatively suggests that there is no special hominoid model for the human diet. Even if, as seems to be the case, the diets of great apes differ from other primates, the range of possible diets on which apes may live is rather large. As has cautiously been done by Milton (2000), only very general conclusions regarding human diets can be drawn from comparative studies of the nonhuman primates or even of the diets of our closest cousins, the great apes. ACKNOWLEDGMENTS I am grateful to Anne Russon, Kevin Hunt, Richard Wrangham, Diane Doran, and Cheryl Knott for providing unpublished plant lists for their

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study sites. I am particularly grateful to Cheryl Knott for adding the parts of plants to her list of plant species for use in this analysis. Michelle Goldsmith kindly sent an electronic form of the large table of plant species and food parts from her dissertation research. Michael Dallwitz and Les Watson advised me on the use of ANGIO and the Families of Flowering Plants database. I thank them particularly for reviewing my list of families near the end to spot those that might have problems due to variations in use in plant taxonomies. I have stuck with the families, sensu strictu, of the FFP database, and their input was vital to making my assignment of genera to families accurate, using the FFP as a standard. Michael also kindly provided an electronic list of the classifications of all families of flowering plants by regions of the world that facilitated examining angiosperm families of the apes and analyses associated with them. Ellen Farr advised me from time to time on plant taxonomy as I referred to the Index Nominem Genericorum (ING). She kindly sent me a text list of all generic names in the ING to use for checking names in my database. Finally, it is a pleasure to acknowledge my debt to the many field workers whose time, energy, blood, sweat, tears, and good health have provided the lists of plants used by the great apes and other primates. Comparative analyses frequently reduce years of fieldwork to a few data points without adequately acknowledging the extremely high costs of obtaining them. Though the pleasures of fieldwork are many, the voucher specimens are hard to come by and almost always lie somewhere on the other side of a veil of thorns. Obtaining accurate identifications can take years of dogged pursuit of the assistance of just the right experts. I hope that the generation following includes field workers as intrepid as those acknowledged above and all the authors of field studies to which I have had the privilege of access.

Chapter 8

Hunter–Gatherer Diets: Wild Foods Signal Relief from Diseases of Affluence Katharine Milton

There is general consensus that many chronic health problems, first noted in Western nations but increasingly prevalent worldwide, relate to diet (Trowell and Burkitt, 1981; Roe, 1979; Prasad et al., 1998; Bray and Popkin,1998; Lampe 1999). There is far less consensus, however, about the dietary factors implicated in such health problems. This lack of understanding has opened the door to a proliferation of different recommendations as to the best diet for modern humans. For clarification, let me note that all humans alive today are members of the same species, Homo sapiens sapiens, and as such, all are fully “modern” humans. Increasingly, the average consumer has come to regard the American supermarket as a minefield of conflicting and potentially dangerous dietary decisions: low fat, high fat, no fat; no meat, high meat, less fatty meat; no eggs, one egg a week, unlimited eggs; less carbohydrate, more whole grains, no cereal products; more fruit, less sugar; and so on. Too much confusing information is available, too much attention is paid by the popular press and public to fad diets and preliminary dietary findings, and too little attention is paid to serious dietary recommendations advanced by entities such as the National Research Council and U.S. Department of Agriculture (USDA). Clearly, there is considerable room for improvement.

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It is difficult to comment on “the best diet” for modern humans because there have been and are so many different yet successful diets in our species. Humans can thrive on diets consisting almost exclusively of the raw fat and protein of marine mammals (e.g., Arctic Eskimo; Ho et al., 1972) as well as diets composed largely of a few wild plant species (e.g., Australian aborigines of the Western Desert; Gould, 1980)—and there are an almost infinite number of successful dietary permutations between these two extremes. Yet in Western and more westernized nations today, it is also clear that some features of diet or some factors that interact with diet have somehow gotten out of step with modern human biology. It would seem that relatively recent changes in certain features of the modern human diet (e.g., cooking of most foods, heavy reliance on a single domesticated grain or root crop, selective cultivation to “improve” vegetables, fruits, or meat, the heavy consumption of highly processed foods, increased sugar and fat in the diet) may, in an evolutionary sense, have occurred so rapidly and so recently that human biology has not as yet had time to adapt to them (Kliks, l978; Trowell and Burkitt, 1981; Eaton and Konner, 1985; Prasad et al., 1998). WHAT DO WE KNOW ABOUT THE DIET OF EARLY HUMANS? Present fossil evidence places the earliest humans at around 2.4 mya (Groves, 1999). Yet evidence for agriculture is dated at only some twelve thousand years ago. This means that for most of human existence members of our genus (Homo) and species (Homo sapiens) have lived as hunter–gatherers—that is, people using only wild plants and animals as foods. Various attempts have been made to reconstruct features of the average daily macro- and micro-nutrient intake for Paleolithic hunter–gatherers (Eaton and Konner, 1985; Eaton et al., 1998; Cordain et al., 1999). The logic behind such attempts seems to be the belief that over the approximately 2.4 million years of human existence, human biology has somehow become adapted to some type of “Paleolithic diet,” and that by discovering and following such a diet today, we might be able to prevent many “diseases of affluence” (e.g., coronary heart disease, high blood pressure, atherosclerosis, type II diabetes, various cancers, obesity, eating disorders, and so on). There are a number of problems with such an approach. One problem is that ancestral hunter–gatherers did not all eat the same diet. Data from ethnographic studies of nineteenth and twentieth century hunter– gatherers, as well as historical accounts and the archeological record, suggest that ancestral hunter–gatherers enjoyed a rich variety of differ-

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ent diets (Smyth, 1878; Ho et al., 1972; Lee, 1979; Gould, 1980; Hayden, 1981; Kuhnlein and Turner, 1991; Milton, 2000). Thus estimates of nutrient proportions for “the Paleolithic diet” are hypothetical, at best. In fact, we do not know much about the range of foods Paleolithic hunter–gatherers consumed in almost any environment at any time, though it seems likely that periods of relative food abundance alternated with seasonal periods of low food availability in most cases. Perhaps more to the point, however, is the fact that regardless of what Paleolithic hunter–gatherer societies were eating, there is little evidence to suggest that human nutritional requirements or human digestive physiology were significantly affected by such diets at any point in human evolution (Milton and Demment, 1988; Milton, 1999a,b, 2000). To date, we know of few adaptations to diet in the human species that would serve to differentiate humans from their closest living relatives, the great apes. Those identified are largely (though not exclusively) regulatory mutations such as lactase synthesis in adulthood, and the unique selective pressures favoring such diet-associated mutations in humans seem fairly well understood. Perhaps more significant, most or perhaps all such mutations appear to have arisen within the past twelve thousand years—that is, well after the advent of agriculture and animal domestication—and therefore are not associated with Paleolithic hunter– gatherers or their diets. Food has played a major role in human evolution, but in a different way than seems generally appreciated. Humans have an evolutionary history as anthropoid primates that stretches back more than thirty million years, a history that shaped human nutrient requirements and features of human digestive physiology long before there were humans or even proto-humans. Because of these inherited traits, ancestral humans were not free to eat whatever they wanted—their pattern of gut morphology, passage kinetics, dentition, body size, and many other features set limitations on the types of foods they could successfully exploit. Elsewhere, I have argued that in the hominoid line, due to the influence of these inherited traits, dietary quality must be kept high for a physically active and highly social lifestyle (Milton, 1999a). Evolving humans appear to have relied increasingly on brain power as the key element in their dietary strategy, utilizing technological and social innovations to secure and process foods before ingestion. Expansion of human brain size and an increasing dependence on cultural (asomatic) behaviors to secure and prepare foods, in turn, buffered humans from many selective pressures related to diet that other animals must resolve largely through genetic adaptation (Milton and Demment,

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1988; Milton, 2000). It is important to understand here that it is the behavioral trajectory taken by humans to secure high-quality foods— rather than simply the foods themselves—that, in essence, has made humans human. Comparative and experimental data show that modern humans, common chimpanzees, gorillas, and orangutans show close similarity in most features of gut anatomy as well as pattern of digestive kinetics (Milton, 1986, 1987; Milton and Demment, 1988; Caton, 1997; Milton, 1999a,b). Such striking similarities support the view that human nutritional requirements, gut anatomy, and physiology were little affected by the hunter–gatherer phase of human existence. For this reason, if modern humans deviate too strongly from ancestral foodways and simultaneously consume foods at variance with their pattern of digestive kinetics, a pattern predicated on a slow turnover of ingesta, they will likely suffer the consequences—some of which appear reflected in the “diseases of affluence” now affecting many modern humans (Milton, 2000). COMPARATIVE ANALYSES OF PRIMATE DIETS Given all of the above, it would seem that a better understanding of the nutritional composition of plant foods in the diets of extant wild primates could enhance our understanding of modern human dietary requirements. Though the necessary nutrients for human beings have been fairly well established since the 1930s and 1940s, the quantities needed are constantly under revision as new facts become available (Lieberman, 1987), suggesting that there is more to learn in this area. As most primates are arboreal, the plant foods they eat in the natural environment consist largely of the leaves, fruits, and flowers of tropical forest trees and vines (Milton, 1980; Milton, 1999b). Analyses have been carried out on a number of nutritional and other chemical constituents of wild plant foods consumed by anthropoids in both the Old and New World (Milton, 1979, 1999a; Dasilva, 1994; Heiduck, 1997; Conklin-Brittain and Wrangham, 2000). When this information is compared with data on similar features of cultivated plant foods consumed by modern humans, some interesting differences emerge. Wild Fruits Most monkeys and apes include considerable fruit in their diet. These wild fruits are more nutritious than cultivated fruits—they have a slightly

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higher protein content, as well as a higher content of certain vitamins and minerals (Milton, 1999a; Conklin-Brittain and Wrangham, 2000; Nelson et al., 2000). For example, in terms of protein, the average crude protein content dry weight of eighteen species of wild Panamanian fruits eaten by various monkey species was 6.5 ± 2.6%, while that of seventeen species of cultivated fruits of the type sold in American supermarkets was 5.2 ± 2.6% (Milton, 1999a). Average crude protein content dry weight of 50 species of wild fruits eaten by chimpanzees in Uganda was 10.7 ± 5.4% (Conklin-Brittain and Wrangham, 2000), while eight species of wild fruits eaten by lowland gorillas in Cameroon showed a crude protein dry weight of 6.3 ± 0.6% (Calvert, 1985a,b). For this reason, a wild fruit eater should net more protein than would be the case if it were eating the same amount of cultivated fruit. Unlike cultivated fruits, wild fruits frequently contain tiny insects and larvae that are consumed by feeding monkeys and apes. These tiny particles of animal matter probably are not useful protein sources per se, but they can serve as an important source of certain essential micronutrients such as B12 and perhaps also supplement particular amino acids, which tend to be low in fruits, both wild and cultivated (Milton, 1999a,b). Another important difference between wild and cultivated fruits is that sugar in the pulp of wild fruits tends to be hexose-dominated (fructose and glucose), while that of cultivated fruits tends to be very high in sucrose, a disaccharide (Baker et al., 1998). As sucrose is broken down by sucrase into glucose and fructose before it can be absorbed, the difference in sugar composition between wild and cultivated fruits might seem trivial. However, Western diets high in sucrose have been suggested to relate to numerous health problems. The difference in sugar composition between wild and cultivated fruits could affect features of molecule transport and absorption (Vanderhoof, 1998) and perhaps insulin production. Humans clearly come from an evolutionary past in which hexose-dominated, not sucrose-dominated, fruits were consumed, and human digestive physiology should therefore be best adapted to a carbohydrate substrate similar to that of wild fruits. Wild fruits also differ in another important respect from their cultivated counterparts, since they generally have a relatively high content of roughage—woody seeds, thick skins, fibrous strands, and, at times, considerable pectin (Milton, 1991 and personal observation). Wild fruits therefore provide a high ratio of indigestible (or slowly digesting) to digestible (or rapidly digesting) material, traits that might slow sugar digestion and absorption (Vanderhoof, 1998).

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Micronutrients Micronutrient (minerals and vitamins) intake is currently of strong medical and nutritional interest. Many problems formerly associated with malnutrition and child development in third world countries are now believed to involve, at least in part, an inadequate intake of particular vitamins and minerals (Calloway et al., 1992; Widdowson, 1992; Cunningham-Rundles and Ho, 1998). Micronutrient deficiencies are not confined to the third world. Many Americans take in suboptimal levels of particular minerals (or vitamins), and this lack may relate to various health problems (Pao and Mickle, 1981; Murphy et al., 1992; Block et al., 1992; Ames et al., 1995). Comparative data indicate that wild plant foods, both fruits and leaves, often show higher values and more interspecific variation in their content of particular minerals than cultivated fruits and vegetables. For example, Nelson et al. (2000) looked at mineral concentrations for sixteen species of wild and four species of cultivated fruits in American Samoa. Four of the eight minerals examined (Cu, Fe, Na, and Ca) showed significantly higher values in wild fruits; wild fruits also showed more interspecific variation in mineral content relative to cultivated fruits (Nelson et al., 2000). A small sample of wild Panamanian fruits eaten by several monkey species showed higher average values for Ca, P, K, and Fe than in cultivated fruits in the United States, while wild Panamanian leaves showed a higher Ca content than cultivated leafy vegetables from the American supermarket. Wild leafy vegetables consumed by the Kekchi people of Guatemala had generally higher nutrient values than cultivated vegetable foods grown in their gardens (Booth et al., 1992). These and other comparative data suggest that, as a class, wild plant foods, regardless of locale, often show higher values and more interspecific variation in their content of many important minerals than do cultivated plant foods. Most wild primates eat a number of different plant foods each day and over the course of an annual cycle may take foods from 150 or more plant species (Milton, 1987). By taking foods from a variety of different plant species and eating plant parts of different types (e.g., leaves and fruit), monkeys and apes obtain a higher-quality diet than would generally be the case if feeding were focused on only one or two plant species per day (Nagy and Milton, 1979; Milton, 1987). In terms of vitamins, vitamin C is of particular interest because, unlike most mammals that can synthesize their own ascorbate internally, all anthropoids, including humans, lack the enzyme L-gulonolactone oxidase (GLO, EC 1.1.3.8), which catalyzes the final step in ascorbate

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synthesis from glucose (Milton and Jenness, 1987). For this reason, monkeys, apes, and humans must have a dietary source of vitamin C. Wild plant foods consumed by Panamanian primates contain notable amounts of vitamin C (Milton and Jenness, 1987). For example, eating a typical leaf-and-fruit diet, a 7-kg wild howler monkey (Alouatta palliata) is estimated to take in some 600 mg of vitamin C per day. The great apes—and here we are speaking of animals as large or larger than many modern humans—are eating diets estimated to contain from 2 to as much as 6 or more grams of vitamin C per day (Milton and Jenness, 1987). In contrast, the recommended vitamin C allowance for the average adult American is 60–70 mg per day. Vitamin C is widely regarded as a potent antioxidant (Ames, 1998; Prasad et al., 1998; Bengmark, l998). The physiological processes of wild primates appear to be carried out with generous amounts of fresh vitamin C continuously present in the body. Other than vitamin C, information is scarce on the vitamin content of wild plant foods monkeys and apes eat, but they likely are rich in vitamin E and provitamin-A— like vitamin C, regarded as potent antioxidants—as well as vitamin K and folic acid (Potter and Hotchkiss, 1995; Booth and Suttie, 1998). As anthropoids tend to fill up each day largely on plant foods, they generally ingest much higher amounts of many vitamins and minerals on a body-weight basis than most modern humans. Do nonhuman primates require much higher levels of certain micronutrients than modern humans, or is their high daily intake in the wild an unavoidable byproduct of their largely plant-based diet that actually serves no important physiological functions? If these micronutrient levels do serve important functions, why do humans not likewise benefit from similar high levels of vitamins and minerals? Wild plant foods also contain a host of other biologically active compounds besides nutrients (Prasad et al., 1998). The physiological effects of these other compounds in relation to plant nutrients are little known, but could affect nutrient utilization or other functions. These topics seem of relevance for future research in terms of improving our understanding of human nutritional requirements. Fatty Acids Diets of most monkeys and apes tend to be low in fat. For example, dietary fat is estimated to contribute only around 17% of daily energy to the diet of wild howler monkeys (Chamberlain et al., 1993), and the largely vegetarian diets of many other wild primates are also estimated to be low in fat-derived energy. It is recommended that dietary fats not

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exceed 30% of daily energy intake in the U.S. diet, though most Americans take in more energy from fat each day than recommended (i.e., >36% of calories) (Eaton and Shostak, 1986; Horrobin, 1989; Murphy et al., 1992). The diet of wild Panamanian howler monkeys contains saturated (S) and unsaturated (P) fats in fairly equal proportions (P/S ratio = 0.85), a ratio close to the 1.0 P/S ratio recommended for modern humans (Chamberlain et al., 1993). In contrast to wild howler monkeys, Americans have P/S ratios of around 0.4. Panamanian plant parts—basically an opportunistic selection of wild plant foods monkeys routinely eat—also contain notable amounts of alpha-linolenic acid (ALA, 18:3, n-3), as well as linoleic acid (LA, 18:2, n-6). Linoleic and alpha-linolenic acids are 18-carbon chain polyunsaturated fatty acids. These two fatty acids cannot be synthesized internally and require a dietary source. Once ingested, LA and ALA can be modified into various long-chain polyunsaturated fatty acids regarded as absolutely essential for many critical body functions (Adam, 1989; Horrobin, 1989). The ALA/LA ratio of most of the wild samples ranged from between 0.26 to 0.40, but occasionally this ratio was much higher (i.e., 5.65, 6.47) (Chamberlain et al., 1993). The routine inclusion of notable amounts of ALA as well as LA differentiates the diets of wild monkeys and apes from those of most Americans. Much of the fat Americans eat is either saturated animal fat or oil from monocot seeds. Most seed oils are high in LA, but low in ALA ; the few seed oils high in ALA (e.g., soy, canola) tend to be low in LA (Adam, 1989; Horrobin, 1989). A number of cultivated leafy vegetables Americans eat are rich (>50% of total fatty acid content) in ALA (e.g., chinese cabbage, white and red cabbage, kale, brussel sprouts, parsley) (Adam, 1989). But most Americans do not eat large quantities of these foods either fresh or cooked, and cooking tends to destroy ALA (Adam, 1989). The diet of human ancestors, like the diets of extant monkeys and apes, likely contained notable amounts of both ALA and LA. For this reason, a similar intake of both essential fatty acids is likely to be most compatible with human biology. In keeping with this suggestion, the addition of ALA as well LA to infant formula has recently been recommended, though the ratio of ALA/LA and types of oils best suited for this purpose are still a matter of debate (Lien, 1994; Crozier, 1994). Dietary Fiber The strongly plant-based diets of most higher primates tend to be high in dietary fiber. Approximately 44% of the daily dry mass consumption

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of a 7-kg howler monkey, for example, is made up of fiber (some 88 g/d) (Chamberlain et al., 1993). Currently, evidence suggests an average dietary fiber intake in the range of 20 to 40 g/d in the majority of human populations studied throughout the world (Jenkins, 1988). However, some present-day rural African populations are estimated to consume 70–90 g of dietary fiber per day (Jenkins, 1988). Fatty acids produced in fiber fermentation may provide >10% of required daily energy for some individuals, and recent data suggest that important health benefits may be conferred by particular fermentation products such as buteric acid (Vanderhoof, 1998). Data from rehydrated human coprolites estimated to be some ten thousand years old show that these individuals, who were consuming what appeared to be coarse, high-residue diets, appear to have taken in ≥130 g of plant fiber per day (Kliks, 1978). There is little reason to assume that the digestive abilities of humans ten thousand years ago differed to any significant degree from those of present-day humans— all are anatomically modern Homo sapiens sapiens. But a diet containing hundreds of grams of dietary fiber seems unsuited to modern human gut anatomy and physiology (Milton, 1986; Milton and Demment, 1988). Protein Carpenter (1994) has discussed many past misconceptions regarding human protein requirements, particularly those concerning the need for or benefits of large quantities of animal protein in the human diet. The average adult American appears to require less than one gram of highquality protein per kilogram of body weight per day (0.75 g/kg average daily requirement for reference protein; National Research Council, 1989) to meet protein requirements (Potter and Hotchkiss, 1995). When one thinks of protein, wild leaves and fruits do not generally come to mind. If one examines the diets of the larger anthropoids, however, it is clear that leaves and fruits appear to satisfy most or perhaps all their daily protein requirements. Young leaves consumed by wild monkeys in Panama show an average crude protein content dry weight of 12.4% ± 4.2; flowers too are often high in protein (9%–10% to 20%– 25% crude protein dry weight) (Milton, 1979, 1980). Though not particularly high in protein, wild fruits average 6.5% ± 2.6 protein; n = 18 wild Panamanian fruit species). Though many cultivated grains as well as some nuts and seeds are low in one or more essential amino acids humans require (Wardlaw and Insel, 1995), amino acid profiles for the ten major amino acids of young leaf

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protein and animal protein are very similar (Moir, 1994). Regardless of protein quality, however, plant protein generally is digested with lower efficiency than animal protein, a fact that could reflect the influence of secondary compounds on protein digestion. Assimilation studies indicate that 20% or more of the total N in wild plant parts is not available to the primate feeder (Milton et al., 1980). Perhaps for this reason, many primates take in more grams of plant protein each day than seem necessary based on body weight (Milton et al., 1980). In contrast to wild primates, Americans obtain considerable daily protein from the meat (muscle tissue) of domesticated livestock. This meat typically is marbled with fat—often heavily. This is a condition not seen in the muscle tissue of wild animals, which is always lean, irrespective of the season, and does not marble (O’Dea, 1991). Because a high proportion of wild animal fat is structural, it is also relatively rich in longchain polyunsaturated fatty acids, rather than saturated fat (Naughton et al., 1986; O’Dea, 1991). Archeological evidence indicates that even the earliest humans began to incorporate bone marrow, meat, and other animal products from wild vertebrates into the diet (Blumenschine, 1992; Marean and Assafa, l999). Using wild animal matter to satisfy daily requirements for protein, essential fatty acids, some energy, and many micronutrients would have freed up space in the gut for carbohydrate-rich plant foods (the principal energy source for most wild primates) and allow for their use as fuel (glucose) for the increasingly large human brain (Milton, 1999b). OVERVIEW The daily diets of monkeys and apes differ in a number of respects from those of most modern humans. Most wild primates eat a variety of fresh plant foods each day, and larger anthropoids typically consume little animal matter. Most plant foods consumed by monkeys and apes come from dicotyledonous canopy tree species. In contrast, many modern human populations derive almost all of their daily energy from a single cooked cereal grain from a monocotyledonous grass (Calloway et al., 1992; Widdowson, 1992). Most cultivated cereals as well as root cultivars are nutritionally inferior to the plant foods consumed by wild primates (Sakai, l983; Coursey, 1983; Widdowson, 1992; Wardlaw and Insel, 1995), and cereal grains, such as wheat, rye, and barley, contain highly insoluble fiber as well (Vanderhoof, 1998). Cultivated fresh fruits and vegetables also differ nutritionally from their wild counterparts. Furthermore, modern humans typically do not eat large quantities or many varieties of fresh uncooked plant foods each day and take in lower

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amounts of many micronutrients, as well as less dietary fiber and nonnutrient phytochemicals, on a body-weight basis than most wild primates. As noted above, there is considerable interest in better understanding dietary factors that may relate to “diseases of affluence.” As appealing as the notion of “the Paleolithic diet” is as a panacea for such health problems, data suggest that one does not have to be a Paleolithic hunter– gatherer to escape them. Information on the diets and health of recent and contemporary traditional peoples, both hunter–gatherers and smallscale agriculturalists who also eat wild foods, show that all such societies are largely free of diseases of affluence whether the daily diet is made up primarily of wild animal foods, wild plant foods, or a single cultivated starchy carbohydrate supplemented with wild plant and animal foods (Lee, 1968; Ho et al., 1972; Truswell, l977; Neel, l977; Walker, 2000). Thus, it is not some special Paleolithic diet or macronutrient profile particular to (ancestral) hunter–gatherers that signals relief from diseases of affluence, but rather shared features of the diets (and lifestyles) of many different traditional societies that spell the difference between their health and ours in this respect (Milton, 2000). I suggest that it is the relatively low digestible energy density of most wild foods, both plant and animal, in combination with certain panhuman features of gut physiology that have played the critical role in the lack of diseases of affluence in hunter–gatherer and other traditional societies, both past and present (Milton, 2000). As the human gut can hold only a limited amount of food at any one time and as transit time of food through the human gut is protracted (averaging sixty-two hours with low fiber diets and forty hours with high-fiber diets; Wrick et al., 1983), there is a clear upper threshold to the amount of most wild foods the human gut can process per day (Milton and Demment, 1988; Milton, 2000). Recent technology has circumvented this natural barrier to excess energy intake in humans by processing, condensing, refining, and otherwise altering both plant and animal foods such that much more energy can be ingested per day than was possible eating wild foods. In addition, as is often stressed, most westerners lead sedentary lives in comparison with more traditional peoples, who typically carry out physical activities, often strenuous, for eight or more hours per day (Milton, 1984). Lowering the incidence of diseases of affluence would appear to involve turning more to foods similar in composition to foods of wild primates, hunter–gatherers, and more traditional rural societies; that is, natural, unprocessed foods, particularly more fresh fruits and vegetables,

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as well as grass-fed rather than grain-fed livestock—and a more physically active lifestyle. ACKNOWLEDGMENTS The paper presented at the 1998 Williamburg symposium on Origins and Evolution of the Human Diet was published in 1999 in Nutrition (Milton, 1999b). I have drawn on this paper, as well as a shorter summary, also published in Nutrition, to prepare this chapter. Readers wishing more information on specifics of nutrient analyses mentioned in this chapter are referred to the 1999 paper.

Chapter 9

Hominid Dietary Niches from Proxy Chemical Indicators in Fossils: The Swartkrans Example Julia Lee-Thorp

It is a truism that the dietary niche of an animal is a key determinant of many important aspects of its biology. For paleoanthropologists, information about hominid diets and dietary comparisons between different species provide broad clues about biology and ecological niche, and further, help to throw light on evolutionary pathways. The story of our ancestors’ evolving diets is inextricably bound with that of how our species, Homo sapiens, developed. Additionally, an interest in the “natural,” or “ancestral,” human diet, if indeed there is such a singular phenomenon, has emerged because factors associated with Westernstyle diets have been implicated in many modern lifestyle diseases. Yet the nature of hominid diets has proved elusive because hominids were, and modern humans still are, quintessential generalists. Early hominids, furthermore, left few traces of their activities before the establishment of recognizable, patterned stone tool industries, and such traces that do exist are often controversial and difficult to interpret. This is particularly true for the South African early hominid sites, which are karstic cavities comprising a sequence of large-scale sedimentary episodes known as Members, which lack conventional stratigraphy and contextual information (Brain, 1981). Material has fallen into these natural traps and subsequently become calcified (or brecciated). Each

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Member contains material that, although broadly reflecting a particular period of uncertain duration, is essentially a composite. To complicate matters still further, all the evidence points to frequent occurrence of more than one hominid species in the same Member, but lack of contextual information makes it nearly impossible to differentiate between their behavior, including their dietary niches. Indeed, this is not a problem confined to the South African hominid sites; similar difficulties exist for many of the East African hominid sites, where more than one hominid taxon was present in the landscape at the same time. These difficulties have encouraged pioneering development of several direct new tools for investigating early human diets. They represent departures from conventional approaches that have relied largely on comparative morphology of fossils and other primates. One example was the application of occlusal molar microwear studies to study differences in consistency and texture of diets between various taxa (Grine, 1981; Grine and Kay, 1988). Australopithecus (or Paranthropus) robustus showed quantitatively more pitting than earlier Australopithecus africanus, which, together with powerful facial architecture and dental characters, suggested that the former concentrated to a greater extent on small hard objects such as hard fruits. A more recent development, which forms the focus of this chapter, is a series of studies based on chemical tracers in the bones and teeth of the fossils themselves and of the fauna with which they are associated. The main advantages of chemical techniques, in general, include that they provide a direct reflection of what was actually eaten rather than what was discarded, they can provide a means to circumvent many of the taphonomic biases associated with contextual information from classes of material such as animal bones (Brain, 1981), and the results are quantifiable. Moreover, they provide information at the level of individuals, and hence interindividual variability and interspecies differences can be assessed. The approaches discussed here are stable carbon (13C/12C) and oxygen 18 ( O/16O) isotope ratios, trace element (Sr/Ca) ratios, and strontium isotope ratios (87Sr/86Sr) in fossil tooth enamel and bone. The focus is the site of Swartkrans, where all four techniques have been applied in a series of studies that did not always use exactly the same specimen material. These techniques are founded on independent principles, as outlined later in this chapter, but all require a sound understanding of fossil calcified tissue chemistry. No approach is without drawbacks, and the interpretation of isotopic and trace element composition is still subject to debate and development. This is perhaps less the case for 13C/12C because the pathways are relatively well understood, and many successful studies of vertebrate diets and habitats across the globe and stretching back to

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the Miocene have been published. Our understanding of the other tracers is less complete. Finally, one of the overarching concerns when dealing with all chemical signals in fossils is alteration of the original signals, or diagenesis. I provide a brief overview of the salient points of diagenesis as they apply to the Swartkrans studies, without attempting an exhaustive review. SWARTKRANS Swartkrans is one of a trio of excavated sites containing material of paleontological and archeological interest, in the Sterkfontein Valley, Gauteng Province (formerly the Transvaal) of South Africa (Figure 9.1). The high number of sites of broadly similar age in this area is owed to the occurrence of a broad band of Malmani Dolomite (Transvaal Supergroup) stretching from Botswana in the west toward the escarpment in the northeast. At Swartkrans, the dolomite band is less than 10 km wide, with quartzite and shale of the Pretoria Group of the Transvaal sequence to the northwest, and the quartzites, shales, and conglomerates of the Krugersdorp Quartzite formation of the Witwatersrand Supergroup, to the southeast (Sillen et al., 1998). The site occurs in a rocky hillside overlooking a valley, through which flows the Blaaubank stream. Although much of the area is currently farmed, the natural vegetation is “Bankenveld,” an open grassland (Acocks, 1975). A narrow band of riparian vegetation borders the stream, and most woody vegetation is restricted to sheltered areas in the cliffs. The site has been extensively excavated for over twenty years (Brain, 1981; Brain et al., 1988; Brain, 1993). The heavily calcified sediments have been assigned to at least five depositional episodes, or Members, separated in each case by at least as many erosional episodes, which has resulted in an extremely complex stratigraphy. The hominid-containing deposits are Members 1 to 3, with dates between ~1.7 and 1.8 (Member 1) and ~1.0 (Member 3) million years. The time span covered by each Member is not known, but Brain has argued for a rapid rate of deposition, perhaps on the order of several thousand years (Brain, 1993). Members 1–3 contain Early Stone Age tools, a number of worked bone tools, hominid fossils assigned to P. robustus and early Homo, and a relatively large Plio-Pleistocene faunal assemblage on which the chronology is largely based (Vrba, 1975; Brain, 1993). Paranthropus remains far outnumber those of Homo. Clarke originally assigned the Homo specimens discussed later in this chapter to Homo cf. erectus (SK 27, SK 2635, and SK 80) (Clarke, 1977a,b), but following Wood and Collard (1999), I use the terminology Homo ergaster. The nature and

Figure 9.1 Composite map showing (a) location of the Sterkfontein Valley in southern Africa and the extent of the summer rainfall region, (b) the geology of the valley with the hominid sites of Swartkrans, Sterkfontein, and Kromdraai within the central band of the Malmani Dolomite formation, and finally (c) details of the site of Swartkrans showing the Blaaubank stream, three sampling transects for 87Sr/86Sr, and the site itself. Sections (b) and (c) are redrawn from Sillen et al. (1998).

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form of the site have changed physically through the period of formation. Although it acted as a natural trap during accumulation of much of the sediment, Brain argued on the basis of spatial distribution of burnt bones and artifacts that it may have functioned more in the form of a shelter during Member 3 times (Brain et al., 1988, Brain, 1993). CALCIFIED TISSUE CHEMISTRY AND DIAGENESIS The process of fossilization preserves bones and teeth, but carries with it an inevitable component of chemical change. Vertebrate bone is made up of two main phases; the organic phase, about 25%–30% by weight, is comprised mostly of the protein collagen, while the mineral phase, about 70%–75% by weight, is a very poorly crystalline,1 nonstoichiometric, biological apatite. The latter is a calcium phosphate structure with a hexagonal unit cell, into which may be substituted ions such as carbonate and alkali earth metals such as strontium and barium (LeGeros, 1991). The substitutions provide the basic material for isotopic and trace element analysis, although structural phosphate forms the basis for most oxygen isotope ratio determinations. After death, the organic phase disappears relatively quickly on geological time scales, while the mineral becomes more crystalline and resistant. This process occurs mainly via recrystallization and crystal growth, in which ions from hydration layers associated with the crystallites, body fluids, or external sources, may be incorporated, or by Ostwald ripening, in which larger crystals “scavenge” smaller ones (Eanes and Posner, 1970). Tooth dentin is somewhat similar to bone in mineral chemistry and undergoes similar processes, although the higher proportions of organic phase and even poorer crystallinity of the apatite makes it more susceptible to change. Mature tooth enamel differs in a number of ways; the organic phase (enamelin and amelogen phosphoproteins, present in very small amounts; ~1%) provides a template for the large apatite crystallites that are thus organized into enamel rods (Glimcher and Levine, 1966; Bonar et al., 1991; LeGeros, 1991). The number of substitutions within enamel apatite is much lower than those in bone (LeGeros, 1991), and as a result enamel is more crystalline, denser, and more resistant in life and death. Studies of chemical structure based on Fourier Transform Infrared spectroscopy (Lee-Thorp and van der Merwe, 1991; Sponheimer and Lee-Thorp, 1999a), predictable carbonate 13C/12C (Lee-Thorp and van der Merwe, 1987; Koch et al., 1994) and 18O/16O distributions among fauna (Bocherens et al., 1996; Kohn et al., 1996; Sponheimer and LeeThorp, 1999b), and predictable seasonal variation in phosphate 18O/16O

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along toothrows (Bryant et al., 1996b; Fricke and O’Neil, 1996), have demonstrated that enamel retains its original structural and isotopic properties for millions of years, in contrast to bone. Another difference is that signals in enamel provide essentially snapshot views of diet related to the period of mineralization, while bone represents a perspective integrated over several years. The physical and chemical changes occurring after death and burial of an animal are collectively known as diagenesis. The extent to which diagenesis occurs, and how it might alter or obscure original biological signals, must be carefully and appropriately assessed in all studies using chemical signals (Nelson et al., 1986; Lee-Thorp, 1989; Sillen, 1989; Sillen and Sealy, 1995; Koch et al., 1994, 1997; Bryant et al., 1996; Fricke and O’Neil, 1996). The aim in such cases is no longer to determine whether diagenesis has occurred (that is given), but to determine whether biologically sensible and valid patterns of the extracted isotopic or trace element signals are maintained in the fossils. A number of criteria exist for this purpose, usually based on comparisons with patterns in modern food webs and ecosystems. Procedures for eliminating highly altered or intrusive mineral phases are similar in principle to all approaches, since they are based on differences in the solubilities of apatites and typical impurities or diagenetic phases (Sullivan and Krueger, 1981; Lee-Thorp and van der Merwe, 1987, 1991; Sillen and LeGeros, 1991). There are some differences, however, as described in this chapter. Assessment of the effectiveness of these procedures is based on standard characterization procedures used in calcified tissue chemistry (LeGeros, 1991). The studies discussed here have relied largely on Infrared Spectrometry or Fourier Transform Infrared Spectrometry to characterize the fossil apatites (Sillen 1989; Sillen and LeGeros, 1991; Lee-Thorp and van der Merwe, 1991; Michel et al., 1995; Sponheimer and Lee-Thorp, 1999b). For 13C/12C 2 and 18O/16O analysis, more soluble mineral phases (simple carbonates and soluble, diagenetic apatites) have been eliminated through various permutations of a weak acid pretreatment procedure (Sullivan and Krueger, 1981; Lee-Thorp, 1989; Koch et al., 1997; LeeThorp et al., 1997; Sponheimer, 1999) and reliability of the signals assessed by means of analysis of associated fauna with known browsing and grazing diets, and hence predictable isotopic values. The preferred sample material has been tooth enamel after it was shown to provide reliable δ13C signals for animals of known diets, even over very long periods of time (Lee-Thorp and van der Merwe, 1987; Morgan et al., 1994; Cerling et al., 1997). Tooth enamel, although resistant, is not immutable, and the presence of diagenetic fluoroapatites in some East

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African fossils (Kohn et al., 1999) is not amenable to acid washing. Damage to fossil tooth enamel has been minimized as a result of recently developed microsampling techniques (Sponheimer, 1999). δ18O data is produced simultaneously with δ13C analysis so the same pretreatment procedures have been used. Unlike phosphate, however, carbonate oxygen is known to be exchangeable with water, arguing for caution, and assessment of δ18O data is more difficult because faunal controls are not obvious. One approach has been to demonstrate maintenance of the seasonal variability δ18O signal, as shown in fossil equid enamel phosphate (Bryant et al., 1996) and more recently for enamel carbonate δ18O of a variety of Oligocene fauna in North America (Feranec and MacFadden, 2000). After observing that hippopotamus δ18O is always low compared to other fauna in a number of African mid-Pleistocene faunal assemblages, Bocherens et al. (1996) suggested their use as a check for diagenesis. Hippopotamus, however, are not always present. Sponheimer and LeeThorp (1999a) showed that predictable δ18O patterning, according to ecological expectations, was maintained for a wide variety of fauna in Pleistocene sites. One complication, of importance if patterned distribution of faunal δ18O data from enamel carbonate is used to assess reliability or to collect information, is that it seems the more vigorous pretreatment procedures used formerly (e.g., Lee-Thorp and van der Merwe, 1987) altered δ18O data in fossil enamel by up to 2‰, compared to gentler methods currently in use (Koch et al., 1997; Lee-Thorp et al., 1997). This means that δ18O data obtained by these two similar methods is not strictly comparable. Bone mineral remains the traditional sample material for trace element analyses, which have mostly focused on Sr/Ca. This is because most teeth (with the exception of the later erupting teeth, such as C and M3 in humans) develop early in life when discrimination against strontium in favor of calcium has not fully developed (Sillen, 1992). The recognition of strontium alteration in fossil bone (e.g., Boaz and Hampel, 1978; Sillen, 1981; Nelson et al., 1986) led to the development of rather more complex stratagems to address the problem and allow extraction of biologically meaningful Sr. The approach exploits the differing solubility characteristics of diagenetic apatites and minerals and biological apatite and measures [Sr], [Ba], and [Ca] only from those solution phases, or acid washes, showing the characteristics of biological mineral (Sillen, 1986; Sillen and LeGeros, 1991). Highly soluble phases not meeting these criteria, which include correct Ca/PO4 ratio, are not used in the subsequent evaluation. Sr/Ca patterns in associated fauna, mainly those demonstrating expected trophic level reduction in strontium, are used

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as controls. Strontium for the purpose of 87Sr/86Sr 3 analysis has been extracted in the same manner, using pooled solutions to produce measurable amounts of strontium (Sealy and Sillen, 1988; Sillen and Sealy, 1995). Largely because 87Sr/86Sr studies of the Swartkrans fossils developed out of the Sr/Ca work, the application described below also relied mainly on bone, but there are no principles preventing its application to enamel. To summarize, a number of studies have now shown that reliable, robust stable isotope signals can be obtained from enamel carbonate, and that in some fossil sites, but not all, biologically meaningful levels of Sr/Ca and 87Sr/86Sr can be extracted using appropriate pretreatment procedures. CARBON ISOTOPES IN THE ANCIENT SWARTKRANS ECOSYSTEM The foundation for reconstructing the diets of fossil taxa using stable carbon isotope (δ13C) analysis lies in isotopic discrimination during photosynthesis by plants at the base of the food web. In African savannas, trees, bushes, shrubs, and herbs (C3 plants) discriminate more markedly against 13C during CO2 fixation than do grasses and some sedges (C4 plants), resulting in distinctly lower δ13C in C3 plants than in C4 plants (O’Leary, 1981; Smith and Epstein, 1971). Modern C4 grasses have average values of –12.5‰ (Vogel et al., 1978; Ehleringer et al., 1997), while trees, shrubs, forbs and their edible parts (seeds, fruits, nuts, leaves, and corms) have average values of about –26. 5‰ (Smith and Epstein, 1971). δ13C in the tissues of herbivores reflect the relative contributions of carbon derived from C3 and C4 vegetation sources (Vogel, 1978; Cerling and Harris, 1999). Further fractionation occurs in animal tissue formation and metabolism, varying according to the tissue type analyzed. In predators, δ13C reflects the diets of their main prey; in fact, for bone and tooth mineral, the values for predator and prey are very similar (Figure 9.2) (Lee-Thorp, 1989). These carbon flow models have been developed from extensive observations of δ13C in modern fauna, but an adjustment to the modern data is necessary. Current atmospheric CO2 is about 1.5‰ lower than it would otherwise be, as a result of the “fossil fuel” effect (Friedli et al., 1986), and therefore, all modern ecosystems are anomalously depleted in 13C. After this adjustment, modern values for fauna with predictable diets, e.g., browsers, are very similar to those of their fossil counterparts, but there is usually a small remaining difference that is most likely associated with some degree of diagenesis. It is very small compared to the large distinctions

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Figure 9.2 A simple flow model of carbon isotope pathways in an African savanna ecosystem, using typical δ13C values for apatite in modern animals. All δ13C values shown have been adjusted by +1.5‰ to subtract the “fossil fuel” effect.

between C3- and C4-feeders, which are maintained, more or less intact, in the fossil record. These distinctions provide a way of establishing where an individual fits into the carbon isotopic spectrum in an ancient food web, relative to known C3- and C4-feeders, as well as providing information about the environment itself (Lee-Thorp et al., 1994; 2000; Koch, 1998; Cerling et al., 1997; Sponheimer and Lee-Thorp, 1999c). The δ13C results for a range of species from Member 1 are shown in Figure 9.3. Brain (1981) showed that the fauna in Members 1 and 2, including the hominids, were likely the prey of large predators, rather than the result of hominid hunting or scavenging activities, and various hypotheses have been advanced about which of the predators might have been responsible. Browsing and grazing herbivores show expected C3dominated (low δ13C) and C 4-dominated (higher δ13C) patterning, respectively, in both Members. Among the primates, Papio robinsoni and Papio (Dinopithecus) ingens (shown collectively as Papio sp.) clearly ate C3-based foods, while Theropithecus oswaldi relied somewhat variably on C4 foods. In Member 1, Procavia (Hyrax), Paranthropus, Homo, Panthera pardus (leopard), and Crocuta all reflect carbon of mainly C3

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Figure 9.3 Distribution of δ13C values shown as means and standard deviations for the faunal assemblages in Swartkrans Members 1 and 2, respectively. Values for Homo and Paranthropus are shown in Member 1, and for Paranthropus in Member 2. Data are from Lee-Thorp et al (1994), and Lee-Thorp et al. (2000).

origin but with some C4 input. Leopard diets shifted to concentrate more on C4 prey in Member 2 (not shown), lending support to Brain’s proposal that they shifted their predatory attentions from hominids to Antidorcas bondi, a small grazing antelope (included in the grazing class) (Brain, 1981; Lee-Thorp et al., 2000). Values for Homo and Paranthropus are almost identical, suggesting that both hominids had a similar mix of C3- and C4-based foods in their diets (~75% and 25%, respectively) (Lee-Thorp et al., 2000). The δ13C pattern can be explained only by direct consumption of enough grass (as blades, rhizomes, or seeds) to form 25% of dietary carbon, consumption of animals that ate grass, or both. The results do not demonstrate, however, that Paranthropus and Homo had the same diet. For

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Paranthropus, occlusal enamel microwear studies do not support eating of grass blades that have scratchy phytoliths (Grine, 1981), but Homo enamel microwear has not yet been subjected to similar analysis. Furthermore, C4 grass seeds are seasonally restricted and uneconomical packages that are difficult to collect without specialized tools. One unexplored possibility is consumption of C4 sedges inhabiting damp areas or pan edges, some of which may have had edible roots. This point is revisited later in this chapter. On present evidence, however, it seems reasonable to conclude that at least a good proportion of the 25% C4 carbon contribution is derived from animal foods. Animal foods may also have been incorporated in the C3 component, but it is impossible to assess the proportions. While hardly surprising for Homo, in the case of Paranthropus, this finding implies omnivory and runs counter to assessments that robust australopithecines were vegetarians specializing in one or another class of plant foods. OXYGEN ISOTOPES IN SWARTKRANS FOSSILS Current understanding of interspecies variability of 18O/16O in bones and teeth of fauna within an assemblage is incomplete, but this tool holds great promise as a source of information about water-related behaviors, thermophysiology, and, possibly, diets of extinct animals. Most research on δ18O in mammalian calcified tissues has been directed at oxygen extracted from the highly stable phosphate ions in the apatite structure, toward the derivation of continental paleotemperature proxies (Longinelli, 1984). It has been shown recently that reliable values can also be obtained from enamel carbonate in fossils in spite of concerns about the ready exchangeability of carbonate oxygen (Bocherens et al., 1996; Kohn et al., 1996; Cerling et al., 1997; Sponheimer and LeeThorp, 1999a; Feranec and MacFadden, 2000). δ18O composition of enamel carbonate and phosphate, which are highly correlated (Bryant et al., 1996a; Iacumin et al., 1996), is directly related to that of body water, which is in turn a function of δ18O of total oxygen entering and exiting the mammalian body (Luz et al., 1984; Bryant and Froelich, 1995). δ18O of meteoric water, and hence surface drinking water, varies according to temperature and latitude (Dansgard, 1964), but at any one location, the main variable inputs are liquid water in food and water and oxygen bound in food. Water in leaves is enriched in 18O due to preferential evapotranspiration of H216O (Gonfiantini et al., 1965; Yakir, 1992), and δ18O of oxygen bound in organic plant matter, such as cellulose, is tightly linked to leaf water composition with strong positive

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fractionation (Epstein et al., 1977; Sternberg, 1989). Values for bound oxygen in food sources, such as in proteins and fats, are less well known, but there is some evidence to suggest that they may be depleted in 18O. Major variations in outputs are due to relative amounts of water lost through liquid water (as urine and sweat) versus 18O-depleted vapor from mucous membranes. Thus, drinking behavior and thermophysiological adaptations—and diet—may affect δ18Obody water and hence δ18Oenamel. Several new studies have pointed to the existence of coherent intraspecific and interspecific patterning within an ecosystem (Kohn, 1996; Sponheimer and Lee-Thorp, 2000), including significantly lower values for faunivores. δ18O is shown plotted against δ13C for a subsample of the Swartkrans Member 1 fauna in Figure 9.4. Because the rigorous acid pretreatments used earlier (Lee-Thorp, 1989) seem to have shifted δ18O values by variable amounts, only data produced by the more recent methods (Koch et al., 1997; Lee-Thorp et al., 1997) are shown here. Unfortunately, this means that inadequate numbers of some classes (e.g., grazers) are available for comparison. (This constraint does not apply to δ13C values,

Figure 9.4 Distribution of δ18O and δ13C values for a subsample of fauna from Member 1, shown as means and standard deviation and as single points (filled circles). δ18O is reported relative to SMOW, and δ13C relative to PDB. Unless indicated otherwise, sample number for means calculations are n = 3. δ13C data were reported in LeeThorp et al. (2000); δ18O data are new.

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which are all comparable.) Highest δ18O values are observed for the giant baboon, P. (D.) ingens, the browsing kudu, Tragelaphus strepsiceros, and the single Connochaetes (a grazer). P. robinsoni, and to a more limited extent T. oswaldi, show relatively lower δ18O values than other herbivores in their respective δ13C “classes.” All faunivores are relatively low, but Crocuta, Megantereon, and Hyena brunnea are most depleted, and the leopards, P. pardus, less so. Both Paranthropus and Homo fit rather squarely in the middle and overlap with the leopards. A very small subsample of Paranthropus is shown (n = 2), and the apparent variability is due to inclusion of SK 876, which has markedly low δ18O (27.1‰) (it also falls toward the higher end of the Paranthropus δ13C range). Given the small sample size, no significant differences in either δ13C or δ18O are apparent for the two hominids. These intermediate to low δ18O results for the hominids are somewhat ambiguous and suggest a mixed signal with contributions from behaviors such as high water requirements and diets that include faunivory or root/underground storage organs. However, δ18O distinguishes the giant baboon clearly from P. robinsoni and implies a clear difference in ecology. One plausible explanation is that P. (D.) ingens obtained a high proportion of its water requirements from plant leaf water. STRONTIUM/CALCIUM RATIOS IN SWARTKRANS MEMBER 1 Calcium is a principle element in bone and tooth mineral, but chemically similar strontium may substitute to some extent for calcium in biological apatites. Mammals discriminate against Sr compared to Ca in the gut and preferentially excrete Sr, a phenomenon known as “biopurification of calcium” (Lengeman, 1963). The result is that very much lower proportions of Sr relative to Ca occur in calcified tissues compared to Sr/Ca in food, and Sr/Ca is reduced stepwise at higher trophic levels. This observation was recognized early on as a potential tool for detecting the trophic level or amount of animal food in the diet (Toots and Voorhies, 1965). It is now recognized, however, that considerable variability in Sr/Ca occurs within each trophic level, including variability within and between individual plants (Runia, 1987; Hall, 1995) and animals (Sealy and Sillen, 1988). Roots, rhizomes, and stems have elevated Sr/Ca, similar to available Sr and Ca in soils, compared to leaves. Hence, leaf-eating herbivores should have lower Sr/Ca in bone compared to herbivores that eat more stem material, and animals that eat underground parts should have higher Sr/Ca (Sillen et al., 1995). This variability complicates inferences about trophic levels, because a

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carnivore has reduced Sr/Ca compared to its particular prey species only. Identified predator–prey pairs follow the pattern of trophic reduction of Sr/Ca. Furthermore, a high level of variability—up to 30%—can exist for each species in a modern food web (Sillen, 1992). Measurements of Sr/Ca in fossil fauna and hominids from Swartkrans Member 1 (Figure 9.5) show that, although variability typical in modern food webs is reduced, patterns similar to those observed in modern African food webs can be observed (Sillen, 1992; Sillen et al., 1995). Highest Sr/Ca occurs in Procavia (hyrax) and Hystrix (porcupine), as is the case for a modern food web in the southwestern Cape (Sealy and Sillen, 1988). The two carnivores measured, Panthera pardus and Hyena, show reduced Sr/Ca compared to most of the other animals, including the primates, but very similar to the browsing kudu, T. strepsiceros. Sr/Ca for Paranthropus is relatively low, between the carnivores and most of the herbivores, a pattern that was considered to be inconsistent with that of a root-, rhizome-, or seed-eating herbivore, and most consistent with omnivory (Sillen, 1992). However, other possibilities include specialization for a wet microhabitat where Sr/Ca is typically low (an avenue discussed later in this chapter), while contributions of folivory or frugivory have not been addressed. Sr and Ca levels in fruit, and in frugivorous fauna, have not yet been adequately assessed. They could also impart lower Sr/Ca, given that leaf-eaters (kudu) are low, and fruit Sr/Ca should follow a similar pattern because intraplant variability is Figure 9.5 Distribution of Sr/Ca in solubility profile washes 11–15 from faunal bone in the Swartkrans Member 1 food web. Diagram is redrawn from Sillen (1992).

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related to transport phenomena (Runia, 1987). Sr/Ca in two Homo individuals are slightly but not significantly higher than Paranthropus. SK 27 falls at the upper end of the Paranthropus range, and SK 847 is slightly above the range (Sillen et al., 1995). Although admittedly a very small sample size, this result could be taken as a hint that Homo diets might have included more foods higher in Sr/Ca, for instance roots and underground storage organs. STRONTIUM ISOTOPES IN SWARTKRANS MEMBER 1 Unlike stable light isotopes, the mass difference between 87Sr and 86Sr is too small to cause fractionation during physical and chemical reactions; hence 87Sr/86Sr in calcified tissues is directly related to abundances in the biome, deriving ultimately from available strontium in local soils. 87 Sr/86Sr sourcing has been applied in archeology to reconstruction of the movements of people in prehistoric and historic times (e.g., Ericson, 1985; Ezzo et al., 1997; Sealy et al., 1995). Use of this tool at Swartkrans, to indicate preferred foraging locales of hominids (Sillen et al., 1998), represents the first application in paleoanthropology. Initially, 87 Sr/ 86Sr was determined to address questions arising out of the Swartkrans Sr/Ca data, including whether the unusually low coefficient of variation (CV) observed for Sr/Ca in the Paranthropus sample (n = 10) might relate to restricted foraging range, and/or whether their relatively low Sr/Ca might indicate a preference for wet, river-associated habitats (Sillen, 1992). At Swartkrans, 87Sr/86Sr in the Member 1 breccia closely resembles that in the present Blaaubank stream, and it is significantly lower than abundances in soils, plants, and animals in the surrounding veld (Figure 9.6), across the dolomite, and shale and quartzite, substrates further afield. Low values in stream water and breccia are likely due to differential leaching of a soluble, 87Sr-depleted carbonate phase in the dolomitic substrate. Low 87Sr/86Sr delimits a zone of influence for the stream on plants and animals in the riverine greenbelt (Figure 9.6). With the notable exception of the riverine rodent Mystromys, whose modern counterparts exclusively occupy riparian streamside vegetation and show low 87Sr/86Sr, all of the Member 1 fauna analyzed have relatively high 87Sr/86Sr values (Figure 9.6), suggesting that they ranged and fed in the veld away from the immediate river environs (Sillen et al., 1998). The Paranthropus and Homo individuals all fell into the “open veld” range (Figure 9.6), with one exception, SK 876, whose bone 87Sr/ 86Sr is significantly lower than that of the other hominids. 87Sr/86Sr was also measured in the M2 enamel as a test for diagenesis in the bone, and

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Figure 9.6 Distribution of strontium isotope values at Swartkrans. 87Sr/86Sr values for the modern ecosystem are shown alongside results for fossil bone and tooth enamel, and breccia, from Member 1. The figure is redrawn from Sillen et al. (1988).

it was shown to be even lower. If diagenesis was implicated in the low value, one would expect that the bone would have been more highly altered toward that of the breccia matrix than the enamel. Since enamel undergoes no turnover and M2 mineralization takes place at a young age (in humans, 2 to 8 years of age), Sillen et al. (1998) argued that the results suggested that this individual, an adult male, had arrived from another locale. The other explanation, that SK 876 only foraged in the riverine belt, was considered less likely. Apart from this outlier, results for the two hominid genera are very similar, suggesting that neither was reliant on riverine resources, but rather that they exploited open-country resources. SYNTHESIS Before attempting a synthesis of how these different lines of chemical evidence can be interpreted together, it should be pointed out that the

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analyses described above have been conducted on different specimens and sample materials. In cases where the same specimen has been sampled, the sample material differs. The preferred tissue for stable light isotope analysis is enamel, while that for Sr/Ca studies, and later strontium isotopes, has been bone, largely because of the development of the “solubility profile” technique. Although the methods for eliminating or circumventing diagenetically altered components are essentially similar in principle, the reliance on enamel on the one hand and bone on the other does mean that different life stages have been sampled. Teeth mineralizing at more mature stages were preferred, but not always available for sampling. The difference in sample material need not be a problem if juvenile and adult diets were essentially similar, but it does introduce another variable. Furthermore, in spite of the strengths of the “solubility profile” technique and the similarities in patterning to modern ecosystems, the 87Sr/86Sr and Sr/Ca data were obtained from bone, known to be susceptible to recrystallization, and the results have not been replicated elsewhere for similar age fossil materials. Therefore, the results must be treated cautiously, and this should be borne in mind in consideration of the following synthesis. The carbon isotope evidence shows clearly that both Paranthropus and Homo concentrated on C3-based foods, but also included roughly 25% contributions of C4-based foods in their diets. These may have been derived directly from grasses or from animal foods. However, pitting rather than scratches from grass phytoliths are evident on Paranthropus enamel surfaces (Grine, 1981). The lack of riverine foraging suggested by the 87 Sr/86Sr data militates against one class of (possibly) edible and less phytolith-rich C4 plants, namely sedges, which grow in damp areas. Intermediate to low Sr/Ca for Paranthropus are consistent with omnivory, although leaf- or fruit/seed-eating may also have contributed. Explanations for the intermediate to low δ18O for both hominids, as also observed for faunivores and other primates, include high daily drinking requirements, faunivory, and inclusion of roots and bulbs in the diet, or a combination of these. Taken together, the data suggest that Paranthropus subsisted on open veld food that, among other things, included animal foods such as small vertebrates and insects. Information for Homo is less complete because fewer individuals have been analyzed, but an equivalent scenario seems likely, since they share similar δ13C, δ18O, Sr/Ca, and 87Sr/86Sr. The slightly elevated Sr/Ca data for the very small Homo sample (n = 2) possibly hint that some class of food higher in Sr/Ca, such as roots and bulbs, may have been favored, as suggested elsewhere by O’Connell et al. (1999). Conversely, foods low in Sr/Ca, such as leaves or animals, were reduced.

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Although clear differences within any of these proxies would demonstrate a distinction in ecological niche, as is the case for significant δ18O differences between the two baboons, P. (D.) ingens and P. robinsoni, an overlap, as shown here for the two hominids, does not demonstrate the converse, i.e., that their dietary ecology was the same. Within various categories of food stuffs, for instance, aboveground C3 plants, dietary emphasis on different permutations such as leguminous pods versus fleshy fruits would yield similar δ13C, δ18O, Sr/Ca, and 87Sr/86Sr values. (Differences would be apparent only in δ15N, but fossil apatites contain no nitrogen.) Nevertheless, the overlap in all four dietary proxies for both hominids is surprising, and it suggests that there were no largescale dietary differences between them. Differences may have been rather those of emphasis or degree. The result underscores, again, that the hominids were generalists, and that rigid “pigeonholing” should be avoided. Paranthropus has often been assigned to a “tough/hard-objectvegetarian” dietary niche, at least partly because sympatric Homo has been consistently viewed as an omnivore and meat-eater, and a separation of this nature seemed necessary to satisfy the principle of competitive exclusion. Another reason is that a dietary analogy drawn from the great apes, with their overwhelming concentration on plant foods, is frequently applied to diets of early hominids, notably the australopithecines. While these models have been very useful, there may be some drawbacks. For one, according to observations of animals sharing a variety of modern habitats, considerable dietary overlap is common and niche separation may frequently only become apparent in the details or during periods of scarcity. For instance, substantial dietary overlaps were documented between modern hunter–gatherers, chimpanzees, and baboons in east and southern Africa (Peters and O’Brien, 1981), and dietary differences between western lowland gorillas (Gorilla g. gorilla) and chimpanzees (Pan troglodytes) in the Central African Republic were only apparent during periods of fruit scarcity (Remis, 1997). Second, hominid population density very likely remained low enough through the late Pliocene and early Pleistocene to minimize potential competition problems. The aptness of the hominoid/chimpanzee dietary analogy is supported by apelike trunk, and hence gut, proportions for Australopithecus afarensis, while lower-fiber diets containing more animal protein are suggested by early Homo body proportions (Aiello and Wheeler, 1995; Milton, 1999a). The state in between, however, is not so clear, and at least one important difference between australopithecines and chimpanzee-type dietary ecology had emerged by three million years ago. It is clear that A. africanus hominids at Makapansgat were regularly

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exploiting grassy patches for food (Sponheimer and Lee-Thorp, 1999c), a pattern that remained consistent for millions of years thereafter. Chimpanzees, however, do not exploit grassy areas for food, even though they may inhabit woodlands with significant open grass (Schoeninger et al., 1999). At some point, australopithecines took a major step into another foraging realm that was never taken by chimpanzees. The Swartkrans example illustrates that approaches based on chemical signals are useful tools for elucidating aspects of the diets and preferred foraging ranges for hominids, which are not readily addressed by other means. Combinations of these tools promise to be more powerful. One future direction of enquiry is likely to include relationships between Sr/Ca and δ18O in plants and animals and use of enamel as sample material rather than bone. With continuing miniaturization of required sample sizes, serial microsampling of teeth and tooth rows could provide information about seasonal variability in various fossil fauna and hominids—for all the variables. Developing these combinations could allow us to address more subtle questions about the dietary niches of hominids. ACKNOWLEDGMENTS I gratefully acknowledge contributions by my colleagues Bob Brain, Andrew Sillen, Matt Sponheimer, Francis Thackeray, and Nikolaas van der Merwe to this work. The South African National Research Foundation, the University of Cape Town, and the Harry Oppenheimer Institute for African Studies supported this work. NOTES 1. Crystallinity is a term that denotes both size and number of imperfections causing strain in crystal structures. 2. By convention, stable isotope ratios are expressed as δ in parts per mil relative to international standards, according to the expression: δ13C = (Rs/Rref – 1) × 1,000, or δ18O = (Rs/Rref – 1) × 1,000, where R = ratio of heavier to lighter isotopes. The standards used here are PDB (Peedee belemnite) for carbon and SMOW (standard mean ocean water) for oxygen. 3. Strontium isotopes are generally not reported in the δ notation, but as a ratio, that is, 87Sr/86Sr.

Chapter 10

Paleontological Evidence for the Diets of African Plio-Pleistocene Hominins with Special Reference to Early Homo Mark F. Teaford, Peter S. Ungar, and Frederick E. Grine

Many researchers have emphasized the importance of bipedality in scenarios of human origins (Lovejoy, 1975; Susman et al., 1984). The focus on bipedalism has spawned numerous analyses of australopith postcrania, whereas analyses of dietary differences have received relatively little attention. This is surprising because among early hominin taxa it is dietary differences and not necessarily locomotor differences that likely set them apart from each other. Witness the classic contrasts between robust and gracile australopiths (Robinson, 1956; Grine, 1981). Another general impression seems to be that all hominins earlier than the robust australopiths were simply generalized omnivores with little or no significant dietary differences between them. We have recently shown that this is unlikely to be true (Teaford and Ungar, 2000), since there appears to have been a gradual increase in dietary flexibility as one moves from Ardipithecus ramidus to Australopithecus africanus. This probably stands in stark contrast to the situation for the robust australopiths, who seem to become more specialized with time and yet may have had the capability to eat a wider range of foods than did the more gracile forms. Where do the earliest members of our genus fit into this dietary scheme? Recent publications have focused on the number of species of

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early Homo (Chamberlain and Wood, 1987; Grine et al., 1996; Lieberman et al., 1996; Wood, 1992; Wood and Collard, 1999a, b) and on possible dietary shifts in the origin of our genus (Aiello and Wheeler, 1995; Hill et al., 1992; Lee-Thorp et al., 2000; Milton, 1999a; Potts, 1988, 1996; Sillen et al., 1995). Yet there have been no recent surveys of the craniodental functional anatomy of early Homo. Perhaps this is not surprising. Members of our genus are usually dependent on tools (Oakley, 1963), and if that was the case for earliest Homo, and tools were used to acquire and process foods, it would be much more difficult to assess the adaptive significance of variation in craniodental morphology. Selective pressures on individuals with different morphologies might be difficult to ascertain. At a quick glance, such an argument might seem to make further analyses unnecessary. However, two basic points leave the door open for further morphological insights. First, we have no way of knowing how common and important tools were to early Homo. If the initial forms of tool use in early Homo were still like those in modern chimps, morphological differences from the earlier australopiths might be minimal. Second, we know extremely little about the earliest forms of tool use. Nonhuman primate tool-users generally use tools to aid in food acquisition and processing. Thus, for example, orangutans and chimps have been shown to modify sticks to probe for food (McGrew, 1994). One of the main differences between tools made by nonhuman primates and those made by later humans is that the former are often made of perishable materials. So the chances are good that the earliest forms of hominin tool use involved perishable tools. If so, they would be virtually impossible to detect in the fossil record (Mann, 1981). Similarly, even if the australopiths used tools made of stone or bone, they would probably be primitive enough to make functional interpretations difficult. This may well change as analyses become more sophisticated (Backwell and D’Errico, 2000), but no matter what form the first tools may have taken, crucial questions remain to be answered about them. Were they used for a variety of foods, or only a few? How were they used? Were they simply aids to ingestion—allowing foods like meat to be cut into small enough portions to be chewed? Or did they act as substitutes for mastication; i.e., cutting foods into small enough pieces to require little or no chewing? Recent work in a broad range of disciplines, such as paleoenvironmental studies (Potts, 1998; Vrba, 1995), behavioral ecology (O’Connell et al., 1999), primatology (Conklin-Brittain et al., 1998), nutritional studies (Aiello and Wheeler, 1995; Leonard and Robertson, 1997;

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Milton, 1999a), and isotope analyses (Sponheimer and Lee-Thorp, 1999c; Lee-Thorp et al., 2000), has rekindled interests in early hominin diets. More specifically, analyses of the earliest members of the genus Homo have brought back the idea that meat played a significant role in a dietary shift from the australopiths to the earliest members of our genus (Milton, 1999a). Can such a behavioral shift be documented through morphological analyses? This chapter attempts to answer these types of questions by looking at the craniodental morphology of early Homo in light of the morphology of its predecessors. Most of the evidence has come from analyses of tooth size, tooth shape, enamel structure, and jaw biomechanics. Taken together, they suggest a dietary shift moving from the early australopiths to the genus Homo, but they also suggest that the change took place after the initial appearance of fossils attributed to our genus. This may also have implications for early hominin taxonomy. TOOTH SIZE Incisor Size Jolly (1970) noted that australopiths had relatively small incisors compared with molars and speculated that this might be associated with terrestrial seed-eating, as seen in Theropithecus today. While this idea has been the subject of some controversy (Dunbar, 1976), Jolly’s ideas stimulated considerable research on the origins of hominin adaptations and on relative incisor size in a wide variety of living and fossil primates. Hylander (1975), for example, examined the relationship of incisor row length (relative to body size) in a range of living anthropoids and found that those species with larger incisors tend to consume larger, tougher fruits, whereas those with smaller front teeth tend to feed on smaller foods or those that require less extensive incisal preparation, such as berries or leaves. Since then, numerous workers have looked to incisor size in early hominins and other fossil primates for clues concerning diet. Incisor size might give us some clues to diet and tooth use for the early australopiths, and we have consistent weight estimates from independent studies for many of these taxa (Jungers, 1988; McHenry, 1992; McHenry and Coffing, 2000). A regression of maxillary central incisor breadth on body size for species representing a variety of catarrhine genera shows a separation of cercopithecines (with relatively larger incisors) above the line and colobines below (Figure 10.1). Further, more frugivorous chimpanzees and orangutans fall above the line, whereas gibbons and gorillas fall close to the line, with relatively smaller incisors.

Figure 10.1 Relative size of maxillary first incisors in catarrhines. Dashed lines indicate 95% confidence limits for the least squares regression plot. MD = mesiodistal. Data from are Coffing et al. (1994), Jungers (1988), Leakey et al. (1995), Ungar and Grine (1991), and Wood (1991).

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Indeed, values for the living frugivorous great apes fall above the 95% confidence limits of expected incisor size for modern catarrhines. The human values fall below the 95% confidence limits, indicating that we have very small incisors relative to body size. Relative incisor sizes for the three gracile australopiths are remarkably similar and fall very close to the regression line, much like the gorilla and gibbon. By contrast, the robust australopiths fall below the regression line and outside the 95% confidence limits. These results are similar to those reported by Kay (1984) and suggest that the robust and gracile australopiths used their incisors differently in ingestion, though they all probably used these teeth less than either the chimpanzee or orangutan. These data give us some idea of whether a taxon often eats foods that require incisal preparation. For instance, lar gibbons evidently have much smaller incisors than orangutans because they depend on smaller fruits that require little incisal preparation (Ungar, 1994b; Ungar, 1996; Ungar and Grine, 1991). From this perspective, the australopiths probably put less emphasis on foods that require substantial incisor use, such as those with thick husks and those with flesh adherent to large, hard seeds. Body weight estimates and incisor size data for A. ramidus, Australopithecus garhi, and Kenyanthropus platyops should offer even more insights. Early Homo provides an interesting contrast to the australopiths. The earliest members of the genus, those generally attributed to Homo habilis and Homo rudolfensis, had relatively larger maxillary central incisors than any of the australopiths. Granted, the sample sizes for early Homo are embarrassingly small (n = 2 for H. habilis and n = 1 for H. rudolfensis), but this evidence suggests that they used their incisors differently than the australopiths, perhaps by ingesting different foods or spending more time preparing or ingesting foods. When Homo ergaster is brought into the picture (again, with a sample of n = 2), another change in function is suggested—H. ergaster used its relatively small incisors differently than the earlier members of our genus. Molar Size One of the characteristic features of the australopiths is their large, relatively flat molars (Kay, 1985; McHenry, 1984; Robinson, 1956; Wolpoff, 1973; Wood and Abbott, 1983). There are certainly differences in the amount of occlusal relief between gracile and robust australopiths (Grine, 1981; see below), but by comparison with most other primates, all australopith molars are low-cusped and huge. This tendency for large molar size is evident even in the earliest australopiths. A plot of

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mandibular postcanine tooth area (MD × BL for P4 – M3) reveals that most of these early hominin taxa have teeth larger than those of the modern orangutan (Figure 10.2). As has been frequently noted in the literature, the robust australopiths reached extreme values for postcanine tooth area—in stark contrast to the members of the genus Homo, which show a steady decline in this measurement through time (Figure 10.2). Obviously, absolute values for tooth size tell only part of the story, as interpretations are affected by differences in body size. For some taxa, such as Ardipithecus, analyses can go no further because there are no reliable estimates of body size. However, those species for which we have body size estimates yield an intriguing picture of hominin dental changes through time. McHenry’s (1988, 1992) “megadontia quotient” is now a standard by which relative postcanine tooth size is measured. If it is computed for the earliest hominins (Australopithecus anamensis and A. afarensis), their molars appear relatively large for a hominoid, but smaller than those of A. africanus, or the robust australopiths (Figure 10.3). The same could be said about the teeth of the earliest members of our genus (H. habilis and H. rudolfensis). But with the transition to Homo ergaster, postcanine tooth size shrinks to about the level exhibited by modern H. sapiens. McHenry and Coffing (2000) have made note of the pattern of transition between the various australopiths and early species of the genus Homo. Basically, the australopiths show a gradual increase in cheek tooth size through time, while the members of our genus show a gradual decrease in cheek tooth size. This is generally true for absolute and relative tooth size. The one exception may be H. rudolfensis, which has cheek teeth that tend to be absolutely larger than those of most earlier gracile australopiths. Of course, the cheek teeth of H. rudolfensis may turn out to be relatively smaller when body size is taken into account, but body weight estimates for H. rudolfensis are tenuous at best because there are no associated craniodental and postcranial remains of this species, despite the implication that femora such as KNM-ER 1472 and KNM-ER 1481 should be assigned to it (Wood, 1992). It is equally possible that these bones could have belonged to H. ergaster. The association of postcranial elements with Paranthopus boisei is equally problematic. Even though individual postcranial bones and a partial skeleton have been linked to this species, the evidence for doing so is far from compelling (Wood, 1991). Thus, statements about relative tooth size in these taxa must be taken cautiously (Figures 10.2 and 10.3). To consider what all of these differences might mean, we need to remember a point raised by Lucas et al. (1986); namely, that variations in tooth size are a means of adapting to changes in the external charac-

Figure 10.2 Summed mandibular postcanine tooth areas (P4 - M3) in Miocene apes, hominins, and extant apes. Data are from Coffing et al. (1994), Leakey et al. (1995), White et al. (1994), and Wood (1991).

Figure 10.3 Megadontia quotients for hominins and extant primates. Data are from McHenry and Coffing (2000) and Wood (1991).

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teristics of foods, such as their size, shape, and abrasiveness. Clearly, some of these food characteristics underwent change during the evolution of the early hominins, as postcanine teeth became relatively larger in the australopiths and relatively smaller in early Homo. Tooth size, by itself, cannot pinpoint the initial change to a hominin diet, at least not with the samples at hand. However, the transition to early Homo suggests that (1) a major change may have accompanied the early evolution of our genus, but (2) that change may have occurred with the emergence of H. ergaster rather than the emergence of H. habilis and H. rudolfensis. Another way of examining postcanine tooth size is to look at the ratio of the areas of M1 and M3 (Figure 10.4). Lucas et al. (1986) showed that this ratio was inversely related to the percentage of leaves, flowers, and shoots in the diet. Thus, anthropoids with a high ratio of M1 to M3 area consume more fruit than those with a low M1-to-M3 ratio. When this ratio is computed for the earliest hominins and some Miocene hominoids, a clear separation is evident, with the earliest hominins, including Ardipithecus, showing higher ratios than the Miocene apes. Measurements for early Homo give mixed results. H. rudolfensis shows a value slightly less than that for the australopiths, whereas H. habilis shows a value slightly greater than those for the australopiths. Interestingly, H. ergaster shows a value within the range of modern great apes, and modern Homo sapiens shows a value only exceeded by modern Pan. Does this indicate progressively more fruit in the diet of the early hominins? To begin to answer that question, we must look at analyses of tooth shape. TOOTH SHAPE Variations in tooth shape are a means of adapting to changes in the internal characteristics of foods, such as their strength, toughness, and deformability (Lucas et al., 1986; Lucas and Teaford, 1994; Spears and Crompton, 1996; Strait, 1997; Yamashita, 1998). Because foods are complicated structures, it is impossible to describe all of the internal characteristics that might have confronted the teeth of the earliest hominins. However, another approach is to describe the capabilities of those teeth. For example, tough foods (i.e., those that are difficult to fracture) are generally sheared between the leading edges of sharp crests. By contrast, hard, brittle foods (i.e., those that are easy to fracture but difficult to penetrate) are crushed between planar surfaces. As such, reciprocally concave, highly crested teeth have the capability of efficiently processing tough items such as insect exoskeletons and leaves, whereas rounder

Figure 10.4 Ratios of M1 to M3 areas, defined as the products of maximal mesiodistal and buccolingual diameters. Data are from Alpagut et al. (1990, 1996), Andrews (1978), Begun and Güleç (1998), Coffing et al. (1994), de Bonis and Melentis (1984), Leakey et al. (1995, 1998), Mahler (1973), White et al. (1994), and Wood (1991).

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and flatter cusped teeth are best suited for a more frugivorous diet. Kay (1984) devised a “shearing quotient” (SQ) as a measure of the relative shear potential of molar teeth. More folivorous species have the highest shearing quotients, followed by those that prefer brittle, soft fruits, and hard-object feeders have the lowest shearing quotients (Kay, 1984; Meldrum and Kay, 1997). Among the early hominins, A. africanus had more occlusal relief than did Paranthropus robustus, suggesting a dietary difference between these species (Grine, 1981). Preliminary shearing quotient studies support this idea while reaffirming that the australopiths, as a group, had relatively flat, blunt molar teeth and lacked the long shearing crests seen in some extant hominoids (Ungar et al., 1999). Indeed, all P. robustus values fall below species averages for any extant ape, as does the A. africanus mean, though some individuals usually attributed to A. africanus have SQ values approximating the chimpanzee average (Figure 10.5). Of course, one of the main limitations to conventional shearing crest studies is that they depend on unworn teeth for analysis. This is a major problem because most fossil teeth are not unworn—quite the contrary. For example, Ungar and colleagues (1999) found less than ten unworn lower second molars (the tooth used in most shearing crest studies) in the entire South African Plio-Pleistocene australopith sample. The problem is even worse for early Homo, where fossil samples are much smaller. While it appears that H. habilis and H. rudolfensis had somewhat more occlusal relief than did the australopiths, this difference is difficult to assess given current methods for quantifying occlusal relief. By itself, the analysis of tooth shape indicates that the earliest hominins would have had difficulty breaking down tough, pliant foods, such as soft seed coats and the veins and stems of leaves—although they probably were capable of processing buds, flowers, and shoots. Would increased occlusal relief have allowed H. habilis and H. rudolfensis to process tougher foods? Probably not, unless the foods were only marginally tougher than those eaten by the australopiths. Interestingly, as suggested by Lucas and Peters (2000), another tough pliant food the hominins would have had difficulty in processing is meat. In other words, the early hominins were not dentally preadapted to eat meat—they simply did not have the sharp, reciprocally concave shearing blades necessary to retain and cut such foods. Of course, this assumes that all meat has the same degree of toughness. This may not be the case. Studies of the physical properties of foods have thus far focused on plant remains, with only brief mention of the toughness of materials like skin (Lucas and Peters, 2000; Lucas and Teaford, 1994). Variation in toughness between animal tissues might well exist due to

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Figure 10.5 South African early hominin shearing quotients (SQs) compared with extant ape averages. Data are from Ungar et al. (1999). Detailed description of methods used to compute SQs can be found elsewhere (Ungar and Kay, 1995; Kay and Ungar, 1997).

variations in the arrangement and density of collagen matrix. Also, the physical effects of cooking or decomposition might render meat less tough and more readily processed by hominins. If so, it could mean that the australopiths were capable of processing meat, on occasion, as part of a variable diet. This could be further support of the idea that scavenging played a role in early hominin life. However, given the flat, blunt teeth of the australopiths, chances are good that they spent far more time processing hard, brittle objects. Processing of soft fruits would certainly be possible, depending on the toughness of those fruits. If they were tough, they would also need to be precisely retained and sliced between the teeth. Again, early hominins, including early Homo, would be very

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inefficient at this. If those foods were not tough, then the hominins could certainly process them. H. ergaster and H. erectus were even more poorly equipped to handle tough foods. With their smaller molars and thinner enamel, even hard objects would present problems. So, through scavenging, hunting, or some combination thereof, H. ergaster was probably forced to use tools to aid in the consumption of meat. In sum, Miocene apes show a range of adaptations, including folivory, soft-fruit eating, and hard-object feeding. This range of specializations exceeds that of living hominoids, and especially the early hominins. While shearing crest length studies have only been conducted on some of the early hominins, the evidence indicates that the australopiths had relatively flat molar teeth compared with many living and fossil apes. Members of the genus Homo may have had slightly more occlusal relief on their molars. These teeth were well-suited for breaking down hard, brittle foods, including some fruits and nuts, and soft, weak foods, such as flowers and buds; but again, as a group, the Plio-Pleistocene hominins were not well-suited to breaking down tough pliant foods like stems, soft seed pods, and meat. ENAMEL STRUCTURE Another area of interest regarding the functional anatomy of the masticatory system is enamel thickness. Notwithstanding methodological differences between studies (Beynon et al., 1991; Beynon and Wood, 1986; Grine and Martin, 1988; Macho, 1994; Macho and Thackeray, 1992; Martin, 1985; Spoor et al., 1993), there is a general consensus that the australopiths had relatively thick enamel compared with living primates, and that many of the Miocene apes also had thick enamel (Andrews and Martin, 1991; Beynon and Wood, 1986; Gantt, 1986; Grine and Martin, 1988; Kay, 1985; Macho and Thackeray, 1992; Robinson, 1956; Schwartz et al., 1998). This perspective is gradually being refined as we get glimpses of more taxa and larger samples. For instance, Conroy et al. (1992) have noted that Otavipithecus had thin enamel, and White et al. (1994) have made the same observation for Ardipithecus. In the first case, however, we lack reliable measurements (Grine et al., in press), and in the second we lack any meaningful assessment of relative enamel thickness. Still, the figures quoted for Ardipithecus (1.1–1.2 mm) are far smaller than those reported for australopiths (2–3 mm). Despite the complication of body size, the point remains that, in direct comparisons between gracile and robust australopiths, the robust australopiths generally have thicker enamel (Grine and Martin, 1988; Macho and Thackeray, 1992; Schwartz et al., 1998). Unfortunately, the

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earliest members of our own genus are harder to fit into this picture. Isolated measures of enamel thickness from various sources (RamirezRozzi, 1998; Tobias, 1991) are hard to separate from values for the australopiths, but attempts at quantification (Beynon and Wood, 1986) have indicated that early Homo has thinner enamel than that of the robust australopiths. Moreover, examination of Beynon and Wood’s results shows that specimens traditionally assigned to H. ergaster or H. erectus generally show the thinnest enamel of any of the molar specimens studied by them. When the larger body size of these species is taken into account, differences in relative enamel thickness would probably be all the more pronounced. This suggests that a change from relatively thicker to thinner enamel was certainly manifest by H. ergaster. So what might be the functional significance of enamel thickness? The most frequently cited correlations are between the consumption of hard food items, or abrasive food items, and thick molar enamel (Dumont, 1995; Kay, 1981). There are many potential complicating factors (Dumont, 1995; Macho and Thackeray, 1992; Macho and Berner, 1993; Martin, 1983), thus, it is perhaps not surprising that the correlation between enamel thickness and diet is not a perfect one (Maas and Dumont, 1999). Moreover, thick enamel by itself does not necessarily provide protection against hard objects, which commonly cause fracture of enamel (Teaford et al., 1996). The best protection against that is prism or crystallite decussation or interweaving. Maas (1993, 1994), Rensberger (1997, 2000) and others (Dumont, 1995; Strait, 1997) have shown that prism and crystallite orientations can give clues to intricate details of dental function and that decussation can be an effective crack-stopping mechanism in many animals. Only anecdotal references to this phenomenon in Miocene apes and early hominins have been made thus far, largely because more detailed work generally requires the sectioning and etching of teeth. Still, after some discussion and debate (Beynon and Wood, 1986; Gantt, 1986; Grine and Martin, 1988), the consensus now seems to be that they did have a significant degree of prism decussation. This, plus their thick enamel, probably left them with an efficient means of resisting tooth breakage during the consumption of hard objects. MANDIBULAR BIOMECHANICS Finally, there are other lines of evidence that we can examine to look for evidence of diet. Mandibular fragments are among the most common bony remains found at hominin fossils sites, and the architecture of this bone has been adapted to withstand stresses and strains associated with oral food processing. Thus, its morphology must reflect some

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aspect of diet. Analyses of australopith mandibular biomechanics have focused on corpus size and shape. Comparisons with extant hominoids have shown that A. afarensis and A. africanus have relatively broad mandibular corpora, as did P. boisei and P. robustus (Hylander, 1988; Daegling and Grine, 1991). Figure 10.6 shows mandibular robusticity index values for extant great apes, some Miocene apes, and the australopiths. The early hominins show relatively thicker mandibular corpora than extant great apes and Miocene catarrhines, which suggests a trophic shift in the former. Interestingly, the earliest members of the genus Homo also show robusticity values greater than those for the same modern and Miocene apes (Figure 10.6). They even show values greater than those for some of the australopiths. Both functional and nonfunctional interpretations have been offered to explain these types of differences. For example, it may simply be that a broad mandibular corpus is an effect of large cheek teeth or a reduced canine (Chamberlain and Wood, 1985; Wood, 1978). This is not a likely explanation, however, as australopiths still have relatively broad mandibles even when considered relative to molar size, and there appears to be no relationship between mandibular robusticity and relative canine size among the australopiths (Daegling and Grine, 1991). It seems more likely that the shape of australopith mandibular corpora relates to the functional demands of mastication. Thickened mandibles can act to resist extreme stresses associated with transverse bending (that is, “wishboning”) and torsion of the corpora around their long axes. Wishboning stresses are concentrated at the symphysis (Hylander, 1984). Thus, torsion is likely a more important explanation of mandibular thickening. As corpus torsion results from bite force and muscle activity during mastication, australopith mandibular morphology probably reflects elevated stresses associated with unusual mechanical demands. Daegling and Grine (1991) suggest that australopiths may have eaten fibrous, coarse foods that required repetitive loading. While this fails to explain why colobines do not have thick corpora, it does suggest a fundamental difference between australopiths and living great apes that may reflect a shift in diet in the early hominins. Studies of corpus shape in Ardipithecus will likely provide further clues regarding differences in mandibular architecture between great apes and later australopiths. However, corpus robusticity values for A. anamensis (measured below M1) average 53.5 (M. Leakey, unpublished data). These values fall at the upper range for extant hominoids (Pan = 39.2–57.8; Gorilla = 43.5–59.7; Pongo = 35.7–52.0) and at the lower end of the range for subsequent fossil hominins (e.g., A. afarensis = 48.4–68.9;

Figure 10.6 Mandibular corpus shape for Miocene hominoids, hominins, and extant apes. Data from Daegling and Grine (1991), Smith (1980), Wood (1991), and Wood and Collard (1999).

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A. africanus = 54.8–79.0) (Figure 10.6) (Daegling and Grine, 1991; Lockwood et al., 2000; Wood, 1991; Wood and Collard, 1999). Based on similar data, Wood and Aiello (1998) have recognized four groups of early hominins: (1) a “generalized simian” group (A. afarensis and A. africanus), scaling like modern anthropoids, (2) a “supersimian” group (P. robustus and P. boisei), with mandibles far larger than simians of the same body mass, (3) an “early Homo” group (H. habilis and H. rudolfensis), scaling between modern simians and anthropoids, and (4) a hominoid group (H. ergaster and H. erectus), scaling like modern hominoids. While the data on mandibular robusticity yield similar groups, two additional points are worth mentioning. First, A. anamensis would fall below the generalized simian regression. Thus, it might form a transition between the Miocene apes and hominins, assuming the patterns hold true with larger samples and reliable estimates of body mass for the Miocene apes. Second, H. habilis, H. rudolfensis, H. erectus, and H. ergaster all retain relatively high values of mandibular robusticity, although H. erectus and H. ergaster may show the beginning of the decline that continues through H. neanderthalensis and H. sapiens (Fig. 10.6). In sum, the architecture of the mandibular corpus suggests that the australopiths differed from living apes in their ability to dissipate masticatory stresses. This would, in turn, suggest dietary differences between these taxa, with the australopiths consuming tougher foods. Among australopiths, the range of mandibular robusticity is also noteworthy. Australopithecus anamensis is intermediate between the African apes and later australopiths, while the other early australopiths exhibit a temporal and phylogenetic progression of increasing mandibular robusticity, culminating in Paranthropus robustus P. aethiopicus, and P. boisei. Interestingly, H. habilis, H. rudolfensis, and H. ergaster exhibit levels of mandibular robusticity greater than A. afarensis and similar to those of A. africanus. By contrast, the low levels in H. sapiens have long been thought to stem from a diet that puts relatively little mechanical demands on the masticatory apparatus (Wood and Aiello, 1998; Wood and Collard, 1999a,b). DISCUSSION The earliest hominins, the australopiths, exhibited a unique mosaic of craniodental features as compared with living hominoids and Miocene apes. They had small-to-moderate sized incisors; large, flat molars with little shear potential; a ratio of first to third molar area that is low compared with extant apes, but generally higher than those of Miocene apes;

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thick tooth enamel; and broad mandibular corpora. This distinctive suite of traits suggests a dietary shift at or near the stem of the hominin clade. The comparatively small incisors of the australopiths probably prevented them from specializing on large, husked fruits or those requiring extensive incisal preparation. Thick-enameled, flattened molars would have had great difficulty propagating cracks through tough foods, suggesting that the hominins were not well-suited for eating tough fruits, leaves, or meat. However, the same molars would have served well for crushing, and their thick enamel would have withstood abrasion and fracture. Not surprisingly, their mandibular corpora would probably have conferred an advantage for resisting failure given high occlusal loads. For much of their history, however, the australopiths underwent a change in diet (discussed later in this chapter) (Teaford and Ungar, 2000), the net effect of which was an adaptive package in later forms that allowed ready access to hard objects, plus soft foods that were not particularly tough. The early hominins could also have eaten both abrasive and nonabrasive foods. These abilities would have left them particularly wellsuited for life in a variety of habitats, ranging from gallery forest to open savanna. Analyses of early Homo are hampered by small sample sizes, but if we could rely on the evidence we have, what might it tell us? Does craniodental morphology indicate that there was an abrupt dietary shift between the australopiths and the earliest members of our genus? In all probability, there was not. What the evidence does show is that there was a mosaic of craniodental changes in our genus spread over at least a million years. Each carried with it certain advantages, or changes in capabilities, but all of those changes did not occur simultaneously. Thus, the appearance of the genus Homo was not marked by a dramatic change in the entire masticatory apparatus. Instead, some traits changed while others stayed the same. The changes that did occur are subtle enough that Wood and Collard (1999a) have suggested that H. habilis and H. rudolfensis are virtually indistinguishable from the australopiths and might best be treated as such. From that perspective, the idea of a characteristic “australopith” dietary pattern contrasted with a dietary pattern for early Homo is probably naive. So what can be said about the evolution of diet during the period from approximately 4.5 to 1 million years ago? Much of the evidence for A. ramidus is not yet available, but despite its thin molar enamel and absolutely smaller teeth compared with those of later hominins, it shows molar size proportions that may hint at dietary changes to come. A. anamensis shows the first indications of thicker molar enamel in a hominin, and its molar teeth were intermediate

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in size between those of modern great apes and later hominins. Similarly, its mandibular corpus is intermediate in robusticity between those of living great apes and later australopiths. This combination of features suggests that A. anamensis might have been the first hominin to effectively withstand the functional demands of hard and perhaps abrasive objects in its diet, whether or not such items were frequently eaten or only an important occasional food source. Australopithecus afarensis was probably similar to A. anamensis in enamel thickness, yet it did evidently show an increase in relative molar size and mandibular robusticity. Thus, hard and perhaps abrasive foods may have become even more important components of its diet. Australopithecus africanus shows yet another increase in postcanine tooth size and mandibular robusticity, which by itself would suggest an increase in the size and abrasiveness of foods. Its molar microwear, however, does not show the degree of pitting one might expect from a classic hard-object feeder (Grine, 1981, 1986). Thus, even A. africanus evidently did not specialize on hard objects, but rather has emphasized dietary breadth. In contrast, the robust australopiths, P. robustus, P. boisei, and P. aethiopicus, show a unique combination of craniodental specializations, including small incisors, massive molars, thick enamel, and a robust mandible. All indicate a diet emphasizing hard and abrasive objects requiring little incisal preparation (but, see later in this chapter). Interestingly, the robust australopiths do show the pronounced pitting on their molars characteristic of classic hard-object feeders (Grine, 1981, 1986). The appearance of Homo may have been accompanied by a slight reduction in enamel thickness—especially when compared to the “hyperthick” levels found in the contemporaneous robust australopiths—and a possible increase in relative incisor size. This is coupled with the maintenance of mandibular robusticity at levels seen in A. africanus and moderate molar tooth sizes approximating those of A. afarensis. The possible decrease in enamel thickness may indicate a smaller proportion of hard objects in the diet of early Homo as compared with the robust australopiths. Of course, a change in the proportion of hard foods is not necessarily the sole cause of changes in mandibular robusticity. Thus, maintenance of mandibular robusticity levels in early Homo might merely mean that peak loads in processing hard food items remained the same or that there may have been an increase in the proportion of tough foods (i.e., those requiring repetitive loading). The slight increase in molar occlusal relief displayed by early Homo (as compared with the australopiths) might have yielded a slight improvement in the ability to process such tough foods. The larger incisors might also have aided in this task by cutting tough foods into small enough pieces to allow

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sufficient mastication for swallowing. Obviously, the only way this strategy would succeed is if the food in question was readily digestible. The other intangible variable in this reconstruction is tool use, however, which might also have aided in the processing of tough foods. The same might also be said for H. ergaster, where there are still more changes toward H. sapiens-like craniodental features. Specifically, molar size decreased compared with the australopiths, and incisor size and relative enamel thickness may also have declined. The ratio of M1 to M3 size also begins to climb toward the levels exhibited by H. sapiens and is quite similar to the value for modern Pongo. But, as in the earlier members of our genus, mandibular robusticity remains at the level exhibited by A. africanus This suite of morphological changes accompanying the origin of H. ergaster may have been aided by a growing dependence on tools, which would have facilitated an important transition in diet from H. habilis/H. rudolfensis to H. ergaster. In sum, diet was probably an important factor in the origin and early evolution of our family. The earliest australopiths show a unique suite of diet-related features unlike those of Miocene apes or living hominoids. Such features suggest that the earliest hominins may have begun to experiment with harder, more brittle foods at the expense of softer, tougher ones early on. This does not mean that all of the australopiths were specialized hard-object feeders. It merely means that, through time, they acquired the ability to feed on hard objects. Many modern primates need to consume critical fallback foods at certain times of the year (ConklinBrittain et al., 1998), and it may well be that the earliest australopiths only resorted to the consumption of hard objects in such situations, whereas the robust australopiths relied on them far more regularly. This is not to say that robust australopiths ate only hard objects (Sillen, 1992; Lee-Thorp et al., 1994), but morphological and microwear analyses suggest that these were not simply fallback foods needed in only certain situations. Instead, they were probably an everyday fact of life, a staple of their diet. Diet also played a crucial role in the early evolution of our genus, although perhaps not in the way traditionally presented. The earliest members of Homo resembled the australopiths in many ways, but at least some began the trend of decreasing molar size that continued on through H. ergaster and H. sapiens. As this happened, their ability to cope with a variety of foods may also have declined, unless, as suggested above, their diminishing dental capabilities were countered by an increasing dependence on tools. In fact, the craniodental evidence indicates that, during this period, H. habilis and/or H. rudolfensis must have reached a critical threshold where they had to turn to tools in order to

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survive. That turning point may well have been a two-step process, rather than one giant leap for humankind. The initial step was probably taken by H. habilis and/or H. rudolfensis with the use of tools for a variety of tasks. Crude Oldowan flakes and perishable tools could have been used for procuring and processing some plants, such as underground storage organs. They also could have aided the incisors in cutting tough foods, including meat, into manageable pieces. In essence, tools would have allowed early Homo to maintain a variable diet despite the changes to the masticatory apparatus. Tools may have facilitated a relaxation of selective pressures for larger molars, thicker enamel, and other hard-object specializations. The need for tools became even more pressing for H. ergaster as molar size and perhaps even relative enamel thickness and incisor size decreased. This was probably accentuated by increased nutritional requirements for the development of a larger brain (Aiello and Wheeler, 1995). The only way to meet those requirements, with the craniodental equipment of H. ergaster, was through a greater reliance on high-quality, easily digestible foods, such as meat (Milton, 1987, 1999a; Milton and Demment, 1988; Speth, 1989). The only way to do that was through the use of tools (e.g., Blumenschine and Cavallo, 1992; de Heinzelin et al., 1999). Thus, there is an interesting contrast between the dietary shift from Miocene apes to the earliest hominins and the dietary shift from the australopiths to Homo. The former did not involve an increase in the consumption of tough foods (i.e., those that are difficult to fracture), because the australopiths were not anatomically preadapted for eating meat. Instead, they were well equipped to process a fairly wide range of foods, to the point where they were probably not dependent on tools. By contrast, the earliest members of our genus began a trend that continued through H. sapiens. This involved diminishing craniodental capabilities. Normally, this trend might have gone hand in hand with decreased dietary flexibility. The earliest members of our genus, however, avoided that outcome by using tools for many tasks, thus maintaining dietary breadth. Obviously, it takes more than just tools to perform some of these tasks. For instance, in hunting, social and cognitive skills would need to be finely honed (Milton, 1987). As those behavior patterns are fairly far removed from evolutionary changes in craniodental anatomy, we have left them for other workers. At first glance, the possibility of interspecific differences in diet among the early hominins might seem to run counter to recent isotope work suggesting that A. africanus, P. robustus, and early Homo all had similar proportions of C3 and C4 plants underlying their diets (Sponheimer and

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Lee-Thorp, 1999c; Lee-Thorp et al., 1994, 2000). Closer examination, however, reveals that both perspectives may be adding to our understanding of the complexity of this problem. The craniodental evidence has shown that there were significant differences in dietary capabilities among the early hominins. This would easily allow niche partitioning among the species, and it would also make possible the coexistence of multiple species. Two lines of evidence from the isotope work echo these findings. First, all of the isotopic analyses to date have suggested that C3 plants formed the foundation of early hominin diets. Those plants are much more diverse than C4 plants and thus would reiterate the possibility of subtle niche partitioning among hominin species. Second, the C3 emphasis in the hominin diet could be the result of either feeding on C3 plants, or feeding on animals that ate C3 plants (Lee-Thorp et al., 2000). The craniodental evidence suggests that the robust australopiths retained the ability to feed directly on plants, to the extent that even hard nuts and abrasive roots could be a significant portion of their diet. By contrast, Homo would seem to have two different options—either use tools to significantly aid in the procurement and processing of C3 plants or place heavier emphasis on the consumption of C3 feeders. Thus, as Lee-Thorp et al. (2000) have noted, the isotope data does not necessarily mean that the early hominins had identical diets. It merely means that “their diets contained an isotopically similar mix of foods” (Lee-Thorp et al., 2000). There are innumerable ways to obtain such a mix and still retain the degree of diet differences suggested by the craniodental evidence. Finally, investigators have tried to relate patterns of hominin evolution to patterns of climatic change for some time (see Foley, 1987; Potts, 1996, 1998; Stanley, 1992; Vrba, 1995, for reviews). The focus of much of the recent work has admittedly been on the origin of the genus Homo. But first, can the dietary shifts in the earliest hominins also be tied to such changes? While there is some evidence of large-scale climatic changes around the Mediterranean (Bernor, 1983) and unusual faunal turnover in parts of western Asia (Barry, 1995), there are no large-scale changes evident in sub-Saharan Africa until after the earliest hominins have arrived on the scene (i.e., not until 1.5–2.5 Ma). There is the slow and inexorable cooling and drying of the Miocene, but perhaps the crucial result of that was an increase in microhabitat variability. Certainly, there are limits to our paleoecological evidence from this period (White, 1995), but as Potts (1998) has noted, “in general, the oldest hominins were associated with a diverse range of habitats.” These included lake and river margins, woodland, bushland, and savanna. Thus climatic and habitat variability seem to be the most obvious correlates with the origin of the hominins.

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As for the origin of our genus, there seems to be no doubt that a major episode of global cooling occurred at about 2.5 Ma (Shackleton et al., 1984; Vrba, 1988). However, the impact of that climatic change on the flora and fauna of Africa has been the subject of discussion and debate. By some accounts, the cooling and drying of that period translated into major faunal changes in Africa, as the appearance and disappearance of taxa could be readily correlated with the climatic changes (Brain, 1981; Vrba, 1988; Vrba et al., 1995). By other accounts, the period of faunal turnover was not that uniform or fast (Behrensmeyer et al., 1997; Cerling, 1992; Hill, 1995; McKee, 1996; Turner, 1995; White, 1995). Because the time period from 2.5 to 1.6 Ma is crucial for the origin of our genus and the disappearance of Paranthropus, one might legitimately ask, “if both creatures were omnivores, why would one genus appear and the other disappear during the same time period?” The answer probably lies in the fact that what is good for one omnivore is not necessarily good for another. In this case, Paranthropus was capable of eating many different foods, but if a critical item in its diet, such as something hard or abrasive, disappeared in the face of climatic change, then extinction could still occur. For example, during this time period, C4 grasslands were spreading across east Africa (Cerling, 1992), despite periodic fluctuations in climate. If the critical food items for Paranthropus were found in more closed habitats, then there would be no escaping extinction. By contrast, one of the hallmarks of early Homo was its adaptability. Initially, its biological adaptations (most notably its craniodental features) would allow it to cope with all contingencies. But as its craniodental tool kit changed, culture began to take over, in the first steps toward the unprecedented adaptability we have come to rely upon. Potts (1998) has emphasized that locomotor versatility was a crucial adaptation of the early hominins in the face of varied environmental conditions. We feel that this perspective needs to be extended to the dietary adaptations of the early hominins as well. In such a land of variable opportunities, the generalized craniodental tool kit of the earliest hominins, and the biological and cultural tool kits of early Homo, may have had distinct advantages, allowing our forebears the flexibility to cope with short- and long-term climatic variations and the resultant changes in resource availability. ACKNOWLEDGMENTS We are grateful to the governments of Ethiopia, Kenya, and Tanzania, and especially to the National Museums of Ethiopia, Kenya, and Tanzania, for permission to study early hominin specimens in their care.

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We also thank the curators at the University of the Witswatersrand and the Transvaal Museum for permission to study early hominin materials from South Africa. This work was supported by National Science Foundation grants SBR 9804882, 9727175, and 9601766.

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Index

Ache, 38–48 passim Agriculture, advent of. See Neolithic revolution, diet change and Aka, 38 Alouatta palliata. See Howling monkeys Anemia, 25 Ardipithecus ramidus, 147–48, 155, 157, 160 Australian aborigines, 112 Australopithecines, 62, 72–76. See also under names of specific Australopithecus genus; names of specific Paranthropus genus Australopithecus aethiopicus. See Paranthropus aethiopicus Australopithecus afarensis, 140, 148, 157–59, 161 Australopithecus africanus, 124, 140, 148, 153, 157–59, 161–63 Australopithecus anamensis, 148, 157–61

Australopithecus boisei. See Paranthropus boisei Australopithecus gahri, 75, 147 Australopithecus robustus. See Paranthropus robustus Baboons, 59, 131, 140 Bioarcheology, 19–35 Blood pressure, 13 Bonobos, 79–108 passim Brain size and expansion, 9–10, 75– 76, 113, 120, 163 Breast feeding, 47 Cancer, 13 Carbohydrates, consumption of, 64, 73, 115 Carbon isotope analysis, 131–33. See also Stable isotope analysis Carbon isotope discrimination in C3 and C4 plants, 130–31 Caries, 22–23

202

Index

Cercopithecoids. See Old World monkeys Cercopithecus ascanius, 62–63 Cercopithecus mitis, 62–63 Cereal grains, consumption of, 11, 13, 25 CHD. See Coronary heart disease Children, health status of, 37–48 Chimpanzees, 59, 61–76 passim, 78– 108 passim, 140, 157 Chumash, 29 Climatic change, 57–58, 164–65 Cooking, 59, 118 Coronary heart disease, 15 Cribra orbitalia, 25–26 Degenerative joint disease. See Osteoarthritis Dental: caries, 22–23; crowding, 28; microwear analysis, 75, 124, 133, 163. See also Tooth Depression, 16 Diabetes, 14 Diagenesis, and calcified tissues, 127–30 Diarrheal disease, 40 Digestive anatomy, 59, 114, 121 Digging sticks. See Tools, and food procurement Domestic foods, chemical composition, 65–66, 74, 114–20 Early Homo. See Homo habilis; Homo rudolfensis Electrolytes, 13 Enamel: hypoplasia, 27; structure, 156; thickness, 75, 155–56, 160–63 Encephalization quotient. See Brain size and expansion EQ. See Brain size and expansion Eskimo, 112 Fallback foods, 63–64, 74, 162 Fat, consumption of, 9, 12, 15–16, 63, 70–71, 117–18

Fatty acids, consumption of. See Fat, consumption of Fiber, consumption of, 62, 64–72, 115, 118–19 Fire. See Cooking FLK Zinjanthropus site, 51–52 Food: external and internal characteristics, 151–55, 159–62; texture, 28 Foraging, 52–53 Fossilization, bone and tooth, 127–28 Fruit: chemical composition of, 114– 15; consumption of, 63 Gibbons, 108 Gorillas, 78–108 passim, 140, 157 Gorilla gorilla. See Gorillas Grandmothers, 54–56 Growth and development, 24–27, 40– 48; early Homo, 56–57 Hadza, 43, 50–56, 74 Hiwi, 43 Homo erectus, 10, 50, 56–60, 67, 75, 125, 131–33, 137–40 passim, 147–53, 155–56, 159–65 Homo ergaster. See Homo erectus Homo habilis, 10, 15, 56–57, 147–53, 159–65 Homo neandertalensis, 159 Homo rudolfensis, 147–53, 159–65 Howling monkeys, 117, 119 Human diet: modern hunter-gatherer, 70, 121; modern non-western, 58– 59, 70–72, 120–21; modern western, 12, 111–12, 121–22 Hunting: archeological evidence for, 50–52; by chimpanzees, 50 Hunting-scavenging hypothesis, 49–52 Hylobates. See Gibbons Immune response, 40 Incisor size, 145–47 Industrial era, 12 Infectious diseases, 29

Index Insulin, resistance, 14 Inuit, 43 Isotope analysis. See Stable isotope analysis Jaw biomechanics. See Mandibular biomechanics Kenyanthropus platyops, 147 Kibale, 61–65, 69–70, 73 !Kung, Dobe, 38–48 passim Last common ancestor, nutritional needs of, 7–8, 72 Lifespan, hominoid, 53–54 Lophocebus albigena, 62 Malnourisment, 40–48 Malocclusion, 28 Mandibular biomechanics, 156–62 Meat: carcass processing rates, 51, 120; consumption of, 120; fatty acid content, 9 (see also Fat, consumption of) Megadontia, 148 Menopause, 57 Mesolithic, 34 Micronutrients, consumption of, 11, 116–17 Minerals, consumption of. See Micronutrients Molar size, 147–51 Mortality: adult, 54; infant and child, 38–40 Neandertals. See Homo neandertalensis Neolithic revolution, diet change and, 10–11, 19–35 Nitrogen isotope analysis. See Stable isotope analysis Nursing. See Breast feeding Old World monkeys, 107 Optimal foraging, 12, 54

203

Orangutans, 78–108 passim, 157, 162 Osteoarthritis, 30 Otavipithecus, 155 Oxygen Isotope Analysis, 133–35. See also Stable isotope analysis Paleolithic diet, the discordance hypothesis, 7–17, 67–68, 112–13 Paleopathology, 19–35 Pan paniscus. See Bonobos Pan troglogytes. See Chimpanzees Papio. See Baboons Paranthropus aethiopicus, 159, 161 Paranthropus boisei, 157–59, 161, 165 Paranthropus robustus, 124–25, 131– 40 passim, 153, 157–59, 161, 163, 165 Periodontal disease, 24 Plants: distinction of parts, 81; diversity of and ape diets, 87–91; geographic variation of, 103–5; overlap in ape consumption of, 91–98 passim; taxonomy of, 80– 81, 86–87 Polyunsaturated Fatty Acids. See Fat, consumption of Pongo pygmaeus. See Orangutans Porotic hyperostosis, 25–26 Protein, consumption of, 8, 50, 63–64, 68, 70–71, 115, 119–20 Provisioning, 49–50, 53 PUFAs. See Fat, consumption of Sarcopenia, 14 Savanna resources, 73, 138, 164–65 Scavenging, archeological evidence for, 50 Sedentism, infectious diseases and, 28–30 Shearing quotient, 153–54 Skeletal: biomechanics, 32; robusticity, 30 Stable isotope analysis, 21–22, 57, 124, 127–35, 137–41, 163–64 Strontium analysis, 135–38

204

Index

Swartkrans, 125–27, 130–41 passim; excavation of, 125–127; location of, 125–26 Taxonomy. See Plants: taxonomy of Teeth. See Dental; Tooth Tools, and food procurement, 59, 144, 163 Tooth: loss, antemortem, 27; shape, 151, 153–55; size, 28, 75, 145–51, 160–62. See also Dental Trace element analysis, 129–30, 135– 38

Tubers. See Underground Storage Organs, consumption of Underground Storage Organs, consumption of, 52–60, 67, 72– 76 Undernourishment, 40–48 U.S. college women, 70 USOs. See Underground Storage Organs, consumption of Vitamins, consumption of. See Micronutrients, consumption of

About the Editors and Contributors

Nicholas Blurton Jones, Departments of Psychiatry and Anthropology, University of California, Los Angeles, California Nancy Lou Conklin-Brittain, Peabody Museum, Harvard University, Cambridge, Massachusetts Loren Cordain, Department of Health and Exercise Science, Colorado State University, Fort Collins, Colorado S. Boyd Eaton, Departments of Anthropology and Radiology, Emory University, Atlanta, Georgia Stanley B. Eaton III, Science Department, Charlotte Lockhart Academy, Kennesaw, Georgia Frederick E. Grine, Departments of Anthropology and Anatomical Sciences, SUNY Stony Brook, Stony Brook, New York Kristen Hawkes, Department of Anthropology, University of Utah, Salt Lake City, Utah

206

About the Editors and Contributors

Clark Spencer Larsen, Department of Anthropology, Ohio State University, Columbus, Ohio Julia Lee-Thorp, Department of Archaeology, University of Cape Town, Cape Town, South Africa Katharine Milton, Department of Environmental Science, Policy, and Management, University of California, Berkeley, California James O’Connell, Department of Anthropology, University of Utah, Salt Lake City, Utah Peter S. Rodman, Department of Anthropology, University of California, Davis, California Catherine C. Smith, Peabody Museum, Harvard University, Cambridge, Massachusetts Sara Stinson, Department of Anthropology, Queens College, Flushing, New York Mark F. Teaford, Department of Cell Biology and Anatomy, Johns Hopkins University, Baltimore, Maryland Peter S. Ungar, Department of Anthropology, University of Arkansas, Fayetteville, Arkansas Richard W. Wrangham, Department of Anthropology, Harvard University, Cambridge, Massachusetts