Powered by Plants V2.3.1 Hard Copy

Don Matesz, M.A., M.S., L.Ac.

INTEGRITY PRESS 2013 Powered By Plants How Natural Selection Adapted Humans To A Whole Foods Plant-Based Diet

Second Edition

ISBN-13: 978-1494367961

ISBN-10: 1494367963

Front cover photo © Chatrawee Wiratgasem/Shutterstock License

No part of this book may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or by any information storage and retrieval system, without written permission from the copyright holder. Contents

Acknowledgements vi Note To The Reader vii Introduction viii Part I: Natural Selection & Nutrition 1 1: Human Evolution & Nutrition 3 The Stone Age Red Herring 3 Reproductive Fitness vs. Health 4 Fossil Diet Records? 4 Meat Made Us Human? 5 Going Underground 11 Control of Fire 12 Hunting a Learned Behavior 14 Accelerated Evolution 15 Summary 15 2: The Nature of Nutritional Adaptations 17 The Carnivore Ideology 18 Plants vs Animals and Plant-eaters vs Carnivores 19 Omnivore Or Not? 20 Two Kinds of Omnivores 20 Natural Selection of Nutritional Adaptations 22 Biological Versus Behavioral Adaptations 25 Primates 27 Frugivores 29 Summary 30 Part II: Human Nutritional Physiology 33 3: Sensation and Nutrition 35 Vision 36 Hearing 38 Olfaction 39 Taste 40 Fat Taste 45 The Taste For Liver 47 Behavioral Adaptations 48 Summary 48 4: Locomotion 51 Stance 51 Human Stance 52 Bipedalism Not Optimal for Hunting 53 Bipedalism Originated In Forest-Dwelling Frugivores 53 Locomotion, Speed, and Endurance 55 Energy Cost of Locomotion 56 Persistence Hunting 56

i Behavioral and Technological Circumvention of Our Locomotive Limits 64 Summary 66 5: Manual Endowments 67 Manual Dexterity and Tactile Sense 67 Hand and Brain 68 Manual Dexterity and Manufacture of Hunting Tools 69 Claws Versus Nails 71 6: Face, Mouth, and Throat 73 Facial Musculature, Jaws, and Throat 73 Teeth 74 Human Dentition In Comparison To Other Extant Apes 75 Canine Teeth 76 Dental Shearing Quotient 78 Dental Carbon Isotope Studies 82 Tropical Grasses, Tools, and Teeth 84 Megadontia Quotient 85 Another Kluge? 86 Comparative Oral Anatomy 87 A Mastication Experiment 87 Saliva 88 Salivary Proline-Rich Proteins 90 Summary 91 7: Stomach 93 Stomach Volume 93 Stomach Acidity 95 Scavenging 97 Summary 98 8: Small Intestine 99 Comparative Intestinal Length 100 Intestinal Immunity 102 The Expensive Tissue Hypothesis 103 A Plant Food Ceiling? Pandas, and Fiber in Wild Versus Cultivated Plants 105 Plant Food Ceiling Part 2: Modern Raw Dieters 113 Plant-Food Ceiling Part 3: Simian Diet Trials 119 Small Intestine Length and Obesity 121 9: Cecum and Appendix 125 The Cecum 125 The Appendix 126 Summary 127 10: Colon 129 Comparing Colons 129 Intestinal Ecology 130 Flora, Fiber, and Fats 132 Colon Health 134 Summary 135

ii 11: Reproductive System 137 Seminal Vesicles 137 Placenta 137 Morning Sickness 137 Fertility 139 Animal Flesh and Female Infertility 140 High Protein Diets Potentially Toxic To Fetus 142 Meat and Male Infertility 143 Summary 147 12: Protein Requirements 149 Natural Selection of Protein Requirements 149 Human Protein Requirements 150 Plant-Based Protein 152 Plant-Based Protein For Athletes 154 Wild Plants Could Satisfy Human Protein Needs 159 Methionine and Cystine 160 Summary 163 13: Vitamin C, Uricase, and Uric Acid 165 Gout In Traditional Meat-Based Cultures 167 Contemporary Diet-Gout Research 169 Summary 175 14: Complexion Preference 177 Complexion, Vascularization, Oxygenation, and Diet in Humans 177 Summary 179 15: Vitamins A & B-12 181 Comparing Human Carotenoid Metabolism To Flesh-Eating Animals 181 Comparing Human Retinol Metabolism To Flesh-Eating Animals 183 Human Vitamin B12 Metabolism Compared to Flesh-Eating Animals 185 Humans Absorption of Animal-Based B12 Appears Limited 186 Non-animal B12 Sources 187 Is a B12 Supplement ‘Artiﬁcial’? 190 Summary 190 16: Carbohydrate & Lipid Metabolism 191 Carbohydrate and Fat Oxidation 191 Metabolism of Saturated and Unsaturated Fats 193 Obesity and Meat-Rich Diets 197 Obesity Among Mongols and Inuit 198 Cholesterol 200 Hyperlipidemia 201 Spontaneous Atherosclerosis 203 Simian Diet Effect On Human Blood Lipids 206 Summary 207 17: Brain Size & Metabolism 209 Encephalization Quotient 209 Is Seafood Superior Brain Food? 210

iii Cerebral Neuron Count 211 The Favored Frugivores 212 The Capuchin Catch 214 Flesh Does Not Provide Ready Brain Fuel 215 Neural Fatty Acids 215 Dietary DHA Potentially Harmful to Embryos 221 Plants Provide The Only Required Omega-3 Fat 221 Brain-Speciﬁc Minerals 222 Factors Correlating With Primate Encephalization 229 Plant-based Intelligence 230 Meat-eating Mentality 234 Animal Cruelty and Social Violence 235 Animal-Based Diets and Brain Damage 236 Does Meat-Eating Make People Warlike? 240 18: Meat-Adaptive Genes? 243 ApoE3: Meat-Adaptive, or Agriculture-Adaptive? 244 CMAH and Neu5Gc Sialic Acid 250 Summary 251 19: Science or Science Fiction? 253 Moving Beyond Carnism 254 Part III: Appendices & Bibliography 257 Appendix A: Essential Nutrients 259 Appendix B: A Whole Foods Plant-Based Diet 261 Supplements 263 Appendix C: Proposed Human Ancestors 269 Was The Alleged Last Common Ancestor Chimpanzee-like? 269 Orrorin tugenensis 273 Australopithecus 275 Homo habilis and rudolfensis 279 Erectus species 282 Homo heidelbergensis 285 Neanderthals 286 Homo sapiens 287 The Limits of Archaeology 289 Appendix D: Chimpanzees 291 Quantity 291 Measuring Wild Chimpanzee Diets 292 Chimpanzee Insectivory 292 Do Chimpanzees Scavenge? 294 Chimpanzee Hunting 295 Remarkable Variations In Chimpanzee Hunting 297 Chimps Probably Do Not Hunt To Obtain Macronutrients 300 How Well Do Chimpanzees Digest Animal Flesh? 301 Bibliography 305

iv v Acknowledgements

I thank the following people for helping me to complete this project.

My wife, Tracy Minton, for her love, support, and considerable assistance in completion of this project, including cover design.

My mentor Jim Lehrman (jimlehrman.com) for helping me to understand the way the mind gets trapped by beliefs, and the way to free oneself from the limits they impose.

Milton Mills, M.D., for his lecture discussing comparative digestive anatomy and physiology, which led me on a quest for thorough documentation.

John McDougall, M.D., for producing The McDougall Plan and The Starch Solution, two of the best documented books on plant-based diets and health.

T. Colin Campbell, Ph.D. for his books The China Study and Whole, which contributed to my wholistic understanding of nutrition research.

Travis, blogger at healthylongevity.blogspot.com, for performing reviews of the manuscript and encouraging me to completion, as well as helping me obtain some of the literature I used.

Plant Positive (www.plantpositive.com), for producing the very informative Primitive Nutrition video series from which I gained considerable knowledge that inspired and helped me to complete this project.

Michael Greger, M.D., for providing on NutritionFacts.org many leads to research reports I found valuable in completion of this project.

John D. Speth, Ph.D., for providing in his book The Paleoanthropology and Archaeology of Big-Game Hunting many leads to research I have included in this work.

Daniel Choleva, for bringing to my attention to some key scientific papers I refer to in this work, particularly Katherine Milton’s papers describing the gastrointestinal tract of the spider monkey.

Katherine Milton, Ph.D., for her several papers on primate evolution and diets, which I found extremely valuable for this work.

Melanie Joy, Ph.D., for her identification of carnism, the ideology that states that eating animals is normal, natural, and necessary.

I assume full responsibility for any errors or defects remaining in what follows.

vi Note To The Reader

Diet has a powerful effect on health and fitness. If you are seriously ill or on medications, consult a health care provider knowledgable about nutrition and its health effects and about your medications before you make any changes to your diet or exercise program. You remain always responsible for your choices, actions, and their consequences. This book serves as educational information only and does not substitute for the guidance of a health care professional familiar with your unique situation. Nothing herein is to be construed as a diagnosis or treatment plan for any individual’s unique physical condition.

vii Introduction

Before there is truth there must be a true human.

Chuang Tzu

My parents raised me on the typical American diet rich in red meat, poultry, fish, eggs, and milk products. From an early age, they taught me to eat these foods to maintain health and strength. We have probably all heard parents uttering phrases like “If you want to grow big and strong, you have to eat your meat.” You might have said this to your own children.

Using such phrases, most parents eventually overcome any natural resistance to eating flesh the child may have. Children live in complete dependence upon parents, and quickly learn what to do to receive parental approval and love and survive under their authority. When parents advise the child that dire consequences will descend upon anyone who refuses to eat flesh, the immature mind naturally associates disease and dysfunction with a flesh-free diet.

Teachers in my grade school reinforced the message with class materials provided by the USDA describing the four food groups that make up a balanced diet: meat, milk, cereals and bread, and fruits and vegetables. The child’s mind absorbs culture like a sponge, without having the ability to critically evaluate its claims.

By route of this cultural conditioning, many people develop a deep-seated belief that humans “are” omnivores who must eat the flesh, eggs, and milk of other creatures to maintain a “balanced” diet and support health and fitness.

Think about this: If you have ever believed that humans “are” obligate omnivores, for whom flesh- eating constitutes natural and necessary behavior, how did you come to hold this belief? Did you consciously adopt this belief only after considering all available scientific evidence, or did you just find yourself holding this belief despite never even encountering or conducting a thorough, evidence-based evaluation of human anatomy, physiology, and metabolism?

The cognitive conditioning provided by our parents and culture during our childhood strongly binds our minds in tangles of erroneous beliefs. When your parents and mentors all eat flesh and approve of you when you do it, your mind associates approval, acceptance, love, and safety with eating what your caretakers and everyone else around you eats. Rejection of flesh-eating will in the recesses of your mind amount to rejection of your mother, your father, and so on, leading ultimately to fatal social isolation. Moreover, your family and friends may indeed mock or reject you if you do stop eating flesh.

viii

Even if in adulthood you become conscious that the beliefs instilled in you in childhood by your parents and mentors do not have a sound evidence basis, you may find it very difficult to free yourself from the insidious way in which those beliefs condition your perception, because of the deep feelings associated with the beliefs. When you act contrary to your cultural conditioning, you will feel the same feelings you felt whenever your parents disapproved of your childhood behavior: most likely, anxiety, fear, and the like.

Beliefs you acquire in childhood profoundly condition your perception and cognition. Even if you consciously reject a belief on an evidence basis, if any age-regressed part of your mind remains bound to that belief, it will continue seeking and interpreting evidence to support its belief. If you do not have a conscious relationship with this part, it can foil your best intentions.

By the time I reached 22 years of age, I had consciously chosen to follow a low-fat lacto-ovo vegetarian diet, and within a few years of that, I had the aspiration to avoid eating any animal products. For roughly the next 15 years, I mostly pursued a vegan path, but during that time I for several time periods (ranging from roughly 3 to 12 months) lapsed back into eating eggs, milk, or flesh. All of these lapses arose because a culturally conditioned part of my mind still believed that humans need to eat animal flesh1 to maintain health and strength.

A mind conditioned by a belief tends to seek confirmation for that belief. For example, if a someone bound by the belief that humans must eat flesh encounters a meat-eater feeling fatigued or getting frequent viruses, s/he may conclude that excessive activity, insufficient sleep, stress, or contact with virus carriers may have caused the problem; but if the same person encounters someone eating a flesh- free diet with the same issues, s/he will likely conclude that the flesh-free diet makes a body weak. The concerned “someone” may include a parent, a spouse, a health care professional, a friend, an acquaintance, or even the individual him/her self.

In short, anyone raised on an omnivorous diet who attempts to live without eating flesh in the midst of a flesh-eating culture constantly receives the message that his/her choice is abnormal, unnatural, and nutritionally deficient, not only from others but even from entranced parts of his own mind. No surprise then that many people who attempt a plant-based diet eventually give it up and adopt the dominant view that eating meat is normal, natural, and necessary.

This does not prove that humans need to eat flesh. It only proves that most people will follow and justify the dominant ideology, even if it involves inflicting suffering on others, when they don't understand the process by which culture, ideology, and social pressure shapes their perceptions and actions.

After having experienced living on flesh-free diets, whenever I decided that I “needed” to eat flesh, I based and buttressed my “feelings” and “decision” on (myth-) information I found in popular and

1 Throughout this book, I will use the term “animal flesh” to refer to any and all tissues taken from the living or dead bodies of animals, including eggs and milk products.

INTRODUCTION – ix

scientific literature claiming that we “are” biologically obligate omnivores. These sources claimed that 1) meat-eating “made us human” in the course of evolution; 2) we “probably” require some nutrients claimed to be scarce or absent from plants, including essential amino acids, essential fats, vitamin A, and vitamin B12; 3) we have an omnivore-bordering-on-carnivore gut that can’t process or even tolerate plant foods very well; and 4) flesh-eating people have better health, strength, and intelligence than people who eat plant-based diets.

In other words, I had read literature that seemed to give a scientific cloak to the belief that people must eat meat to grow up big and strong. To someone indoctrinated in carnism2 and fed meat from an early age, any supposedly scientific claim advocating the importance of flesh-eating to human evolution, nutrition, health, and fitness “just makes sense” and any evidence to the contrary might not even seem plausible.

If you believe that humans must eat meat to maintain health you will almost certainly have great difficulty accepting the abundant contrary evidence presented in this book. Your mind may think, “Well, if this was true, my (insert authority, such as parents or doctor) would have told me long ago.” Not so. Ideologies often function to hide the truth. The authorities you rely upon grew up in the same culture that indoctrinated them with the same ideology. In fact, the highest authorities in the culture (e.g. physicians) receive the most thorough indoctrination; after all, they achieve their status as authorities by demonstrating mastery of the doctrine, and very few of them realize the truth. The ideology becomes so much a part of the fabric of the mind of all members of the culture that almost no-one can see it as just an ideology, the prerequisite to questioning and testing it. It becomes the ground upon which everyone in the culture stands. Only people who find an alternative stand point (i.e. from outside of the culture) can question it.

In 2004, my first wife Rachel Albert and I published The Garden of Eating: A Produce-Dominated Diet and Cookbook, a book promoting a so-called Paleolithic diet. When I wrote my portion of that book I blindly accepted carnism. We published this book after spending about 6 years eating a diet supplying more than half of its energy from flesh and fat, supplemented by fresh vegetables and fruits.

However, during the ensuing years during which I ate a flesh-rich diet, I gradually developed adverse signs and symptoms. For some time, I avoided recognizing them as consequences of my diet. In what I now call my “paleo daze,” often aided and abetted by others in the same daze, I found ways to manage, rationalize, or minimize the significance or impact of these issues on my own health, in order to protect a belief in my “need” to eat meat.

By 2007, my total and LDL cholesterol had risen to 231 mg/dL and 138 mg/dL, respectively, and my blood urea nitrogen (BUN), creatinine, and uric acid measured on the high side of the normal range. Following the lead of advocates of meat-based diets, some of whom claim that elevated cholesterol is harmless or even beneficial, I rationalized that my high HDL and low triglycerides protected me from

2 Carnism consists of the belief that consumption of animal products is normal, natural, and necessary for human health and fitness. See: Joy M. Why We Love Dogs, Eat Pigs, and Wear Cows. Conari Press, 2011. www.carnism.org x – POWERED BY PLANTS

the excess cholesterol and saturated fat in my food and my blood. My high meat intake produced the elevated BUN and uric acid. I rationalized that they were “normal,” ignoring that the normal range is not necessarily a healthy range, since it is merely what occurs in our largely diseased population.

The body ignores rationalizations and responds to reality. On the meat-based diet, I developed small lipomas, a persistent rosacea near the root of my nose, and skin tags. The latter surprised me because three leading advocates of a ‘paleo diet’ had published a paper in which they implied that a meat-based diet low in carbohydrates (i.e. plants) would prevent skin tags.3

More worrisome, after some years on the meat-rich regime, I started having intermittent bouts of difficult, painful urination consistent with prostate hypertrophy. Since the advocates of meat-based ‘paleo’ and low-carbohydrate diets laid all illness at the door of dietary plants, I reasoned that I was not faithful enough to the ‘insight’ that humans are carnivores. Following the ‘Paleolithic diet’ theory to its logical conclusion, I tried to correct the problems by greater restriction of plant-foods and an increased intake of flesh and fat. My low-fiber, fatty feasting resulted in intermittent bouts of severe post-meal bloating and nausea, and constipation lasting 5 to 7 days, frequent complaints among followers of meat- based diets.

During these years, I served as an adjunct professor of nutrition at Southwest College of Naturopathic Medicine and director of the nutrition program at Southwest Institute of Healing Arts (SWIHA). I knew that a very large body of research had linked the things I experienced with flesh- and fat-rich diets. Despite my growing concerns and cognitive dissonance, Rachel remained committed to the “Paleolithic” diet.

In 2010, two years after the end of my first marriage, I met my current wife, Tracy Minton, who began eating “paleo” with me. Soon she had sharp intestinal pains almost daily, and her bowels would not move more than a couple of times a week. Within a few months she felt almost constantly stiff and achy throughout her body, and had a dull pressure in between her eyebrows. Within 6 months, she added about 20 pounds of fat to her 4’11” frame. Most alarming, she developed painful cystic changes in her breasts.

I had seen this happen before. I also knew of scientific evidence indicating that such diets promote both benign and malignant breast disease and low-fat plant-based diets prevent or reverse these disorders. Tracy and I together decided to return to a whole foods plant-based diet (very high in carbohydrates and low in fat). Within a month (one menstrual cycle) her breast signs and symptoms significantly improved, and within three cycles they had resolved entirely.

By about 18 months after the change, my total and LDL cholesterol dropped to 178 and 97 mg/dL, respectively. My BUN and creatinine dropped to the low normal. I no longer suffered bouts of

3 Cordain L, Eades MR, Eades MD. Hyperinsulinemic diseases of civilization: more than just Syndrome X. Comparative Biochemistry and Physiology Part A, 2003;136:94-112.

INTRODUCTION – xi

indigestion and constipation, had no skin tags, and the lipomas had receded. The rosacea that began during the ‘paleo daze’ and had plagued me for at least 10 years had disappeared.

To know truth, one must awaken from the trances produced by false ideologies that pervert perception and condition cognition. While I had found ways to rationalize my lipid profile and skin issues and the discrepancies between my “paleo diet” beliefs and the bulk of scientific evidence, witnessing Tracy develop breast disease while eating a flesh-based diet provided a wake-up alarm.

Hypnotized by the idea that we must eat flesh, eggs, or milk to maintain health and fitness because we “are” omnivores, we imprison, torture, kill and eat millions of animals annually; suffer obesity, premature aging and degenerative diseases; waste agricultural resources; pollute water; contribute to global climate change; and degrade the natural beauty of rural regions. Carnism also causes many to deny that eating animals has any of the aforementioned effects, since many people find it hard to believe that a “normal, natural, and necessary” behavior, endorsed first by our parents and finally by our medical professionals, can inflict any such widespread damage on our world.

In this book I question the idea that humans have a physiology specially adapted to consumption of animal flesh, and attempt to awaken something in you. If you eat flesh, you might not find it possible to read this book without reacting very emotionally. You may find your mind defending yourself, your parents, and your culture from the revelation that you base your diet on a fallacy. Few people react with ease when told that a cherished belief holds no water. You may find yourself choosing between feeling angry at the message and messenger, or painfully acknowledging that you accepted a falsehood on faith. I know from experience: escaping this trance will require you to reject one pillar of your culture and your very identity.

Although subtle, trances both blind and bind. Breaking free demands a commitment to truth and growth, but the effort pays you an immeasurable reward. Beyond the illusion you will find both your humanity and the truth.

xii – POWERED BY PLANTS

INTRODUCTION – xiii

Part I: Natural Selection & Nutrition 2 1: Human Evolution & Nutrition

The Stone Age Red Herring

In the late 20th and early 21st centuries, several authors have proposed that the paleoarchaeology and paleoanthropology serve as the best sciences to guide us to an understanding of the optimal diet for modern humans. These authors have stated that the best diet for support of health in modern humans consists primarily of animal flesh. They claim that human ancestors ate animal-based diets and consequently, evolution by natural selection has made the human species into an obligate carnivore, the correct appellation for any animal that must eat a meat-based high-protein or high-fat diet to maintain health and fitness.

When one party to an argument introduces irrelevant issues into the discussion, in an attempt to lead the other party to consider these irrelevant issues rather than the evidence at hand, logicians call that a red herring. This tactic got its name from the use of smoked herring (red in color) to distract hounds from the trail of a fox in the “sport” of fox hunting, which of course I consider barbaric and do not endorse in any way.

I believe that reference to stone age species and diets in discussions of modern human nutrition qualifies as a type of red herring. We don’t need to know what prehistoric hominins or isolated hunter-gatherer tribes ate, or even the general outline, let alone the details, of any alleged human evolution, to experimentally determine modern human nutritional requirements. If we want to learn what type of food best supports modern human health, we can and should restrict ourselves to studying modern humans, both in the natural experiments produced in free-living humans following significantly different diets in large populations, and in controlled clinical trials. Introducing speculations about prehistoric species and diets and the proposed evolution of humans from non-human species into this discussion only serves to distract us from the large body of evidence already available from studies of modern humans, which clearly indicates that plant-based diets best support human health, fitness, and athletic performance. I believe that advocates of ‘low carb’ and ‘paleo’ diets have used this red herring because they lack quality evidence derived from studies of modern humans to support their claims, so they have to resort to logical fallacies to mislead people into adopting their miserable menus.

Since the ‘prehistory/evolution’ argument for ‘low carb’ and ‘paleo' diets just distracts us from the large body of recent historical, epidemiological, experimental, and clinical data, accumulated over the past 200 years, we could ignore it altogether without losing any vital information. However, advocates of these diets have dressed up this red herring to make it look legitimate. Consequently, someone has to show that the carnivorous caveman has no clothes.

As I will show in this book, an abundance of data gathered by modern nutritional research suggests strongly that human evolution was primarily powered by a plant-based diet, and that the pursuit of meat was possible only after humans had established a highly efficient plant-based subsistence coupled with control of fire. Unlike ‘paleo’ diet proponents who attempt to determine the optimal modern human diet

by examining the weak evidence provided by the fossil record and the ecologically constrained and socially and politically motivated choices of contemporary hunter-gatherers, I will use well-established human nutritional research to shed light on the evolutionary diet of the human lineage.

Reproductive Fitness vs. Health

From a Darwinian perspective, fitness consists of the ability to survive and reproduce. We have no reason to assume that any diet that enables a species to reproduce adequately to survive for millennia will also promote optimal overall health or athletic fitness or prevent chronic degenerative diseases.

Simply put, we know that humans can grow to adulthood on a wide range of diets, and can reproduce while simultaneously suffering from various chronic maladies, such as obesity, allergies, asthma, skin rashes, and constipation. Moreover, many chronic progressive degenerative diseases, such as coronary artery disease, cancer, arthritis, or type 2 diabetes, manifest symptomatically only after 40 or 50 years of age.

None of these disorders increases mortality during reproductive years or severely impairs reproductive ability. An individual can have seven to ten children before starting to have symptoms related to any of these diet-related diseases. Therefore, Darwinian natural selection could not have removed from the human population any individuals or lineages who developed any of these disorders as a result of consuming an animal-based diet.

If for the moment we grant that the prehistoric ancestors of modern humans did in some or even all circumstances consume an animal-based diet, this diet could have helped a majority of those ancestors survive to reproductive age, and produce numerous children, without having any effect on any natural selection processes that influence human nutritional physiology.

Fossil Diet Records?

Archaeological remains suffer from preservational bias. Organic materials, such as remains of plants or feces, generally do not survive for millennia simply because organic processes quickly recycle such materials. Bones can survive for millions of years, although frequently in a more or less disintegrated condition. Stone tools survive the passage of time in many environmental conditions, but tools made of organic materials only survive under unusual conditions.

Consequently, the fossil record preserves far more evidence of animal bones than of plants. This preservational bias inevitably gives us more evidence of meat-eating than of plant-eating. Furthermore, we have incredibly small amounts of fragmentary fossil evidence available to us. In the words of the paleontologist Stephen Jay Gould, “Most hominid fossils, even though they serve as a basis for endless speculations and elaborate storytelling, are fragments of jaws and scraps of skulls.”4 Although we have a few more complete specimens, and they do provide good quality evidence for an evolution of

4 Gould SJ. The Panda’s Thumb. WW Norton and Company, 2010. 126.

4 – NATURAL SELECTION & NUTRITION

hominins over time, they do not provide us with a complete history of prehistory, let alone a journal of daily food intake for representatives of each species over the previous 6 million or more years since the alleged last common ancestor of humans and modern ape.

People have tried to circumvent this by reference to isotope studies. However, isotope studies have their own weakness. We can surmise, for example, that bones containing a high proportion of specific carbon isotopes indicate that the individual from whom the bone came ate either plants that use C4 carbon fixation–grasses, grass seeds, or grass sap (e.g. sorghum)–or flesh from animals that ate grasses. These studies however can not at this point distinguish between these alternatives.

In contrast, we have presently on Earth about 6 billion living modern humans, and we have historical records of human food consumption extending back several thousand years. Contemporary and recent historical human populations have eaten and continue to eat widely different diets, ranging from 100% or very near 100% animal-based (e.g. arctic Inuit and low-carbohydrate diet adherents) to 100% plant- based (e.g. Seventh-Day Adventist and Chinese Buddhist vegans). We have studied the anatomy, physiology, and metabolism of modern people in great detail, and accumulated knowledge of the effects of various diets on human health, disease, mental and physical performance, and fertility for nearly 200 years with modern scientific methods.

In short, the fossil record is not a detailed diet record. It can never tell us exactly what ancient hominid species consumed on a daily basis, so it is severely limited as a tool for enabling us to understand modern human nutritional physiology, and also for retrodicting the probable habitual diets of early human ancestors. The sparse and biased fossil evidence we have of stone age hominid dietary practices can not provide us with more information about modern nutritional requirements than the direct study of modern humans. No fossil evidence can refute modern medical and nutritional research. At most, it could provide us with an hypothesis, which we then would have to test on modern humans.

In fact, whereas the fossil record can’t provide us with much information about modern human biology, if modern human biology was molded by natural selection, then the huge body of indisputable information we have gathered in the study of modern human nutrition can help us retrodict the probable habitual diets of stone age hominids. That is the approach that I adopt in this book.

Meat Made Us Human?

As of 2013, the dominant hypothesis of human origins among paleoanthropologists and paleontologists proposes the following:

1. The hominin lineage descended from the last common ancestor (LCA) of apes and hominins, which resembled a chimpanzee (long face, enlarged canines in males, large molars, both knuckle-walking and arboreal locomotion, small brain),5 probably used natural materials (including stones) as tools, and ate a plant-based diet;

5 Although some authors suggest the LCA was more like an orangutan than a chimpanzee; see Appendix C.

HUMAN EVOLUTION & NUTRITION – 5

2. The Australopithecines descended from the LCA and gave rise to the human lineage; they had adaptations for both bipedal and arboreal locomotion, small brains and large teeth, used natural materials for tools but lacked artificially flaked stone tools, and ate plant-based diets; 3. Early Homo species6 had in comparison to the Australopithecines similar molar teeth and similar or somewhat larger brains, ate a plant-based diet, and (unlike earlier Australopiths) manufactured flaked stone tools and cut-marked animal bones; 4. By 1.6 million years ago, Homo erectus7 had emerged, sporting brain twice as large as that of Australopiths; a body size similar to modern humans; markedly smaller teeth, jaw, and face than Australopiths; and often making flaked stone tools; 5. Modern humans emerged about 200, 000 years ago, equipped with smaller teeth, a more gracile body, and a larger brain than erectus.

For those interested, in Appendix C I have provided more details about proposed human ancestors.

Some authors (including Darwin himself) have ventured the hypothesis that “meat made us human,”8 i.e. that hunting and meat-eating combined with a reduction in consumption of plant foods drove the transformation from a quadrupedal chimp-like ancestor through the above stages and made it both necessary and possible for modern humans to have large brains. As noted by Wrangham et al.:

“These ideas involve a range of hypothesized relationships between hunting and hominization, including the need to follow migratory herds, the benefits of cooperative hunting, the importance of group size in defense against the large predators of the savanna, and the large (and therefore sharable) package size of meat.”9

Some authors have also hypothesized that the increases in body and brain mass required the consumption of meat to supply adequate energy, essential fats, or minerals. At this time, the idea that hunting and meat-eating uniquely drove human evolution remains a disputed hypothesis, and one that has serious shortcomings that I will discuss in detail, partly in this chapter, and throughout this book.

According to the neo-Darwinian theory of evolution by natural selection, genetic evolution sufficient to produce novel species requires as its basis genetic mutations. In other words, according to neo- Darwinism, mutations made us human, and meat-eating can only contribute to a species transformation by either causing genetic mutations, or favoring the survival and procreation of specific mutants in an environment where every member of the species depends on meat-eating for survival to reproduction.

6 At present, early Homo may include late Australopiths, Homo habilis, or Homo rudolfensis, although these details may change; see Appendix C.

7 Including Homo ergaster; see Appendix C.

8 Bunn HT. Meat Made Us Human. In Evolution of the Human Diet: The Known, the Unknown, and the Unknowable, edited by Peter S. Ungar. Oxford University Press, 2007.

9 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 568.

6 – NATURAL SELECTION & NUTRITION

As discussed above, the most dramatic alleged transformation appears in the transition from the bipedal apes to erectus/ergaster. By 1.6 mya, erectus/ergaster had a markedly larger body and brain and consequently larger food energy requirement than the earlier bipedal apes. The hunting hypothesis proposes that early Homo satisfied this increased energy requirement primarily by consuming animal flesh. However, this proposal faces six major problems it can not solve.

As noted by Wrangham et al., the first problem for the hunting hypothesis lies in the fact that, within non-human species, populations eating more meat-rich diets don’t appear to have markedly larger bodies (or brains) than those eating more plant-based diets:

“For example, a highly carnivorous population of chimpanzees (at Gombe) also has the smallest known body weight among chimpanzees…and polar bears, which are much more carnivorous than brown bears, have only 7% more female body mass (which itself may be less than expected simply because of latitudinal differences between the two taxa) and smaller neonates.”10

Consequently, we lack evidence for the idea that pursuit of an animal-based diet reliably increases energy intakes and favors individuals having larger lean body mass or brain sizes.

A second problem lies in the fact that early human ancestors had neither natural nor artificial weaponry, nor the speed and muscular power suitable for making hunting a primary method for food acquisition. Lieberman et al. state:

“If early humans were carnivores, then how did they manage to kill their prey and/or compete with other carnivores over access to prey? This was not a trivial problem for early Homo, because hominins lack the natural weaponry of cursorial predators, such as claws and fangs, and cannot sprint fast enough to capture most prey. The fastest human sprinters can run approximately 10/m/sec for only about 20-30 seconds; in contrast, most African mammals that were apparently hunted by Homo can run at least twice as fast for several minutes…”11

Although “Most scenarios of early human hunting and scavenging assume that early Homo, like modern humans, managed to hunt and compete with other carnivores by relying heavily on technology,” neither early Homo, nor H. erectus/ergaster had the weapons used by modern hunter-gatherers – bow and arrow, tipped spears, and others. Although we have evidence that by about 400, 000 years ago erectus did manufacture clubs and untipped wooden spears, “Thrown, untipped spears have a lower, possibly negligible, probability of mortally wounding or disabling an animal,” and clubbing is not a likely stand- alone technique because “getting within a few meters of any medium- to large-sized animal is seriously risky because such animals can kick or butt with great force. Rodeo athletes, who regularly interact at

10 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 571.

11 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 7.

HUMAN EVOLUTION & NUTRITION – 7

close quarters with large mammals, frequently incur injuries such as broken legs that would have killed or disabled early humans.”12

Leiberman et al. suggest that “evidence that ESA [early stone age] hunters were able to hunt mammals such as zebra, wildebeest, and various other antelopes suggests an ability to get close enough to prey to kill them with crude, nonprojectile weapons without serious risk of injury.”13 They suggest that erectus used persistence hunting to exhaust prey. Although I will discuss the relative importance of persistence hunting in natural selection of human traits in greater detail in Chapter 4, one immediate problem with posing this as a method of hunting that enabled the transition from bipedal ape to Homo is that in order to succeed at persistence hunting, you need a body adapted to endurance running; but according to the fossil evidence, neither Australopithecus nor early Homo had the long-legs, shoulder girdle, or cylindrical rib cage necessary to make this a consistently successful endeavor.

Thus, during the time that the hominins already adapted to a plant-based diet allegedly evolved some ability to succeed at persistence hunting, the species involved would have remained dependent on a predominantly plant-based diet as the fallback, primary support for health, physical fitness, and reproduction. Under such conditions, natural selection would strongly favor retention of the ability to thrive on a plant-based diet, by favoring those individuals who were most capable of both reproduction and endurance running– healthiest, strongest, and fastest– when eating the basic plant-based diet.

This hypothesis is testable in that it predicts that modern humans have superior fertility and endurance running performance when eating a plant-based–i.e. carbohydrate-rich–diet. If modern humans have superior athletic performance when eating a plant-based diet, this serves as evidence that during evolution, natural selection favored the reproduction of humans who depended upon a plant-based diet to support their physical activities. Conversely, if modern humans have their best endurance running performance when eating meat-based diets low in carbohydrate, this would serve as evidence that human ancestors depended upon a low-carbohydrate diet to fuel their activities. In Chapter 4 I will show that humans require a plant-based diet for high performance in endurance running, a fact that supports the hypothesis that human evolution was powered by a plant-based diet, and undermines the meat hypothesis.

Further: If modern humans are more fertile when eating plant-based diets than when eating animal-based diets, this would confirm that prehistoric humans did not have consistent access to or nutritional dependence upon meat as a support for basic fertility. On the other hand, if modern humans are more fertile when eating an animal-based diet, this would serve as evidence that during human evolution, the people who had the most access to meat, particularly in times of general food shortage, had the most reproductive success. In Chapter 11 I will discuss the extensive evidence supporting the plant-based hypothesis.

12 Ibid., 8.

13 Ibid., 8.

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The third problem with positing hunting as the subsistence strategy driving human evolution lies in the fact that, although modern African hunters have sophisticated weapons invented within the last 200,000 years, they fail to bring home food from about 75% of the hunts they devote to chasing ungulates, the targets of persistence hunting (see Chapter 4). Further, studies of the modern Hadza hunters have shown that despite their possession of equipment superior to ancient humans, and the absence of the very large, probably social carnivores with which ancient human species would have had to compete for almost any carcass, they have a lower food productivity than they would if they gathered plant foods at rates similar to children:

“The household share is a rough estimate of the hunter's contribution to family consumption when he hunts big game. The overall average acquisition rate for hunters is 4.89 kg/day (live weight; Hawkes et al. 1991). If we assume that the hunter's household keeps 10%, then his "take- home" rate is 0.49 kg/ day.3 Hadza men spend 4.13 hrs/day hunting on average, making their average take-home rate 0.12 kg/hr....

“The rates for large game can also be compared with gathering plant foods by converting kilograms of meat to calories. If large animals are estimated at 1500 Cal/kg live weight (following Lee 1979), a rate of 0.12 kg/hr (live weight) gives 180 Cal/hr. This rate is lower than all but the very youngest children earn gathering (Blurton Jones et al. 1989; Hawkes, O'Connell, and Blurton Jones 1995). In the long run, big-game hunting is inferior to available alternative strategies for provisioning families.”14

Consequently, rather than go hungry, contemporary African foragers eat largely plant-based diets.

“Nevertheless, on days when a hunter returns to camp without having been able to feed himself, he depends on food gathered by females and/or other more successful hunters.”15

H. erectus lacked modern weapons, and had a brain only 2/3 the size of a modern human; it is unlikely that H. erectus had greater hunting success than modern humans, except outside Africa where the prey were “sitting ducks” due to unfamiliarity with human predation. As support for hunting, the proposed ancestor of the first H. sapiens, African erectus/ergaster (see Appendix C) most likely would have required the ongoing support of a plant-based diet.

Wrangham et al. note that, since human hunters frequently fail to bring home food, “increased hunting requires efficiency in other forms of foraging,” so evidence for intensified hunting by H. erectus probably provides evidence that these hominids had already achieved highly efficient plant-based subsistence:

14 Hawkes K. Hunting and the Evolution of Egalitarian Societies: Lessons from the Hadza. In: Diehl, M. W. (Ed.), Hierarchies in Action: Cui Bono? Occasional Paper 27. Southern Illinois University, Center for Archaeological Investigations, Carbondale, IL. 59–83. 65.

15 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 11.

HUMAN EVOLUTION & NUTRITION – 9

“By this argument, meat is not an important source of food but, rather, hunting itself is an important behavior, less efficient than foraging for plants and thus possible only if supported by gains in efficiency in other areas of foraging.”16

The fourth problem with the hunting hypothesis stems from the fact that, for ecological reasons, human meat intake would most likely have varied considerably over evolutionary time, as it has in historical populations. During phases when game animal populations and therefore meat availability declined, natural selection would strongly favor individuals who could fallback on whole plant foods and thrive. Again, we can test this hypothesis by examining the reproductive performance of modern humans subjected to plant-based or animal-based diets; if modern humans are more fertile on plant-based than animal-based diets, this supports the hypothesis that human ancestors relied on plant-based diets for basic health, and that meat was a luxury food; whereas if modern humans require dietary animal flesh for maximum fertility, this supports the hypothesis that “meat made us human.”

Wrangham et al. point out that the variability of meat availability to a lineage already preadapted to plants would make it unlikely that meat consumption would markedly favor any consistent, progressive skeletal or soft tissue evolution, such as the doubling of brain size mentioned above.17 For example, if brain size was highly dependent on access to meat, a decline in meat supplies would lead to a loss of brain size, leaving a trail of fossil craniums showing growth spurts during meat feasts and shrinkage during meat scarcity. Such a trail does not exist.

The fifth problem lies in the fact that wild animal flesh has a low energy value during periods of climatic stress, when prey are starved and lean, making it an unlikely fallback food for a hominin species that has a constant high energy demand due to having a large brain.18 As Wrangham et al. note:

“When plant food is scarce, hunters are probably less willing to risk energy and time in a failed search for meat. In addition, wild meat is a low-fat food which may have low nutritional quality during lean periods…We therefore suggest that early humans, including H. erectus, continued to rely on plant foods most of the time and especially during the periods of food shortage in which natural selection would have been intense.”19

Since natural selection is most intense when food is scarce, it will always favor those who can thrive and reproduce on the population’s fallback diet as opposed to the luxury diet available in good times. In the alleged human evolution, when game was short or too lean to support health, anyone who required

16 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 571.

17 Ibid., 571.

18 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 571.

19 Ibid., 570.

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animal flesh for survival would have been impaired or perished, while those who could continue to live on plants would have thrived. This would lead to the seemingly paradoxical outcome that the individuals who could achieve maximum physical and reproductive performance on a strictly plant- based diet would generate the lineage most capable of developing improved hunting abilities; in the end, the best hunters would be those who didn’t need to hunt for any nutritional purpose!

A sixth problem for the hunting hypothesis lies in the dangers involved in giving up arboreal adaptations for full-time terrestrial existence. So long as hominins had the ape-like shoulder girdle and powerful arms, they could retreat to arboreal nests at night or when threatened, to avoid predators. The alleged evolution of the lineage involved the loss of this climbing ability concurrent with gaining the ability to run, but the latter does not keep a hominin safe from the swifter, more powerful carnivores, particularly at night or in the early stages of bipedal efficiency. Artificial weapons are also useless for protection when surprised by a predator like a leopard during your sleep. Therefore, before the lineage could fully commit to leaving the trees, and really develop the ability to run, it had to have some passive defense against predators, particularly at night. For living humans, the camp fire provides the most primitive primary passive defense against nocturnal predators. Therefore, I suggest that hominins most likely developed control of fire concurrently with developing a physiology committed to living in a savannah habitat.

In sum, H. erectus, like modern humans, lacked the natural weapons (teeth, claws) found in carnivores like canines and felines; consequently, in most circumstances, it seems most likely that those erectus who did hunt did so while supported by a predominantly plant-based diet and aided by technology, including control of fire.

Going Underground

Lieberman et al. and Wrangham et al. believe that late australopithecines and early Homo depended upon starchy underground storage organs (USOs).20 In Africa, tubers are a much more stable and abundant food resource, virtually constantly available, in comparison to meat. In the 50 km2 forest area inhabited by the African Aka tribes “there is a permanent amount of biomass larger than five tons of tubers;” these are edible, some without cooking; most belong to the Dioscorea family; and toxic species “grow exclusively outside of the forest.”21 Sixty-six percent of 48 USOs consumed by African foragers require no cooking, yet cooking increases the number of edible species.22 Five African savannah sites have 101 species with edible USOs, compared to only 14 species in four forest sites.23 The major plant families providing these 101 USOs were Asclepiadaceae, Leguminoseae, Curcurbitaceae, and Liliaceae,

20Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 6-7.

21 Hladik CM, Bahuchet S, Garine I de, eds. Food and Nutrition in the African Rain Forest. Unesco/MAB, 1990. 14-15.

22 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 573.

23 Ibid., 569.

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accounting for 59% of species consumed. The Leguminoseae and Curcurbitaceae families also produce edible starchy fruits (legumes and edible squashes).

Wrangham et al. have estimated that increasing the proportion of the diet consisting of cooked starches raises energy intake substantially more than substituting meat for plant foods. Cooking dramatically improves the digestibility of starches, and Wrangham et al. have estimated that H. erectus/ergaster would have obtained a 19% higher energy intake from a diet based primarily (~60%) on cooked tubers than from one based primarily (60%) on animal flesh (Table 1.1).24

Table 1.1: Effects on Daily Energy Intake of a Hypothetical Early Homo Diet of Adding Different Proportions of Meat versus Cooking Cooked Tubers, Early Homo diet 20% Meat 40% Meat 60% Meat No Meat Food % of Cal/ g/day Cal/ g/day Cal/ g/day Cal/ g/day Cal/ g/day Type Diet day day day day day Fruit 20 400 140 320 112 240 84 160 56 400 140

Seeds 20 400 189 320 151 240 113 160 75 491 189

USOs 60 1200 638 960 511 720 383 480 255 1966 638

Meat 0 0 0 534 194 1067 387 1601 580 0 0

Total 100 2000 967 2134 967 2267 967 2401 967 2857 967

% 7 13 20 43 Change NOTE: Cooking was assumed to double the energy value from carbohydrate in underground storage organs and increase it by 60% in seeds. Source: Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec;40(5):567-594. 573.

Control of Fire

Currently, the earliest evidence for some controlled use of fire comes from Koobi Fora and Swartkrans, both dating to about 1.6 mya, the time of H. erectus. According to Wrangham et al.:

“Thermal and paleomagnetic data suggest that the reddened patches at Koobi Fora (from around 1.6 million years ago) represent repeatedly used hearths (Bellomo 1994). At Swartkrans, burned bone are associated with hominid artifacts at around this time as well (Brain 1993). This suggests that control of fire arose with H. erectus.”25

24 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 573.

25Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 572.

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Early humans probably would have had frequent exposure to natural fires. In the lower Pliocene, the African climate became increasing dry, facilitating wild fires caused by lightening strikes, volcanic activity, spontaneous combustion, and percussion sparks from rockfalls.26 Wild fires would have produced cooked plants and animals, giving early humans experience of the merits of cooking. They may have discovered somewhat cooked tubers by digging for roots in areas recently burned by wild fire. They could have captured wild fire, kept it burning in hearths, and carried embers with them to restart fires; or learned to start fires themselves with stones.

Early hominins inhabited forests that provided high-energy but difficult-to-access foods such as palm nuts. They also had the natural resources, strength, manual dexterity, and intelligence necessary to make simple stone tools (hammer and anvil). Since modern great apes, particularly chimpanzees, use stones as hammers to crack open nuts, most likely the alleged last common ancestor of apes and humans did the same. Panger et al. note that “Because stone hammer use can unintentionally create sharp-edged stones, it is possible that this type of stone-tool use preceded the intentional production of stone flakes.”27 I would say this is not only possible, but probable. Upon discovery of uses for these sharp- edged stones, an intelligent creature would attempt to reproduce the tool.

Australopithecus garhi, dated to 2.5 mya, apparently used stone tools, and fossils of A. afarensis have hands indicating human-like adaptations for the manual dexterity necessary for use of stone tools dating to 3.2 mya.28 By 1.6 mya hominids had been working with stones as hammers and anvils for at least 1.0 million years; during this time they likely would have noticed that they could generate sparks by percussion of particular stones (pyrites).29

Erectus/ergaster certainly had the ability to use stones to pound starchy plant foods to a pulp to improve their digestibility; and we have clear evidence that ergaster (African erectus) had sufficient control of fire to cook foods 1.0 million years ago.30

Early humans would have noticed that most animals keep a safe distance from wild fires. Control of fire would have given early hominins the passive defense against predation necessary to allow them to safely inhabit, at least for periods of time, open grasslands. This would have relaxed the selection for the ape- like shoulder girdle and arms adapted to tree-climbing (as a retreat from predation).

26 Ibid.

27 Panger MA, Brooks AS, Richmond BG, Wood B. Older than Oldowan? Rethinking the Emergence of Hominin Tool Use. Evolutionary Anthropology 2002;11:235-45.

28 Ibid.

29 For a video demonstration of generation of fire using stones: https://www.youtube.com/watch?v=G5vnLg9uZwc

30 Miller K. Archaeologists Find Earliest Evidence of Humans Cooking With Fire. Discover 2013 April 12. Retrieved Nov. 6, 2013 from http://discovermagazine.com/2013/may/09-archaeologists-find-earliest-evidence-of-humans-cooking-with- fire#.UnqziRkbr4g .

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Controlling fire for cooking would have increased food energy intake from plant foods, particularly USOs, making it possible for males to live off the food gathering efforts of women when, as is often the case, they failed to succeed at hunting As explained by Wrangham et al.:

“Why do women gather? They are forced to do so because they won’t acquire food otherwise and access to resources is critical for their reproductive success. Why don’t men gather (much)? They don’t need to because they can scrounge plant foods from women [in exchange for protection and sex]. Why do men hunt? They can afford a high-risk, high-gain activity because they are supported by women’s foraging and food preparation effort.”31

I also suggest that control of fire may have contributed to selection for reduction of body hair. Hair is relatively more combustible than skin, so hairy individuals are more likely to catch fire than those without hair. If women did more cooking than men, as typical in modern human groups, their greater exposure to fire might explain in part a selection for much less body hair in women than in men; women’s sexual selection (preference for less hairy mates) may reinforce reduction of body hair in males. In addition, use of fire may in both sexes relax selection for hair as insulation to protect against cold temperatures at night.

Hunting a Learned Behavior

Humans are not born hunters. As already noted, we lack the anatomical equipment of natural carnivores (specialized senses, claws and teeth), therefore we have to use technology and skills to learn to hunt successfully. In contemporary hunter-gatherer tribes, males train for many years before they become proficient at bringing home any dead animals of size large enough to contribute to the family economy (and even then, as discussed above, their contribution is often less than it would be if they dedicated the same time to gathering with the proficiency of a child).

This means that hunting and meat-eating was a learned behavior for human ancestors as well. Learned behaviors are not ‘written in our genes’ – hunting is like using a computer in this respect. In fact, humans generally invent technology precisely because they do not have the biology required to achieve a specific task.

To illustrate, scuba gear, airplanes, heated shelters, and insulated clothing all enable us to accomplish things that our native biology does not permit. No one suggests that by using heated shelters and insulated clothing to inhabit cold climates, we become biologically better adapted to those climates. In fact, we all recognize that by using technology to adapt to cold climates, we eliminate any natural selection for genetic mutations that would improve biological adaptation to cold, such as by increasing thermogenesis, or growing thick fur coats. But when it comes to diet, for some reason some people persist in believing that the use of technology and culture to enable us to hunt, eat meat, and combat the diseases arising from this practice (via medicinal practices) creates some natural selection favoring

31Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594. 574.

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humans having not only some specific biological adaptation to, but an absolute requirement for, dietary animal flesh.

Accelerated Evolution

Regardless of hypotheses about prehistoric human diets, evolutionary biologists believe that human genetic evolution has accelerated since prehistory:

“Human evolution is speeding up. Around 40,000 years ago our genes began to evolve much faster. By 5000 years ago they were evolving 30 to 40 times faster than ever before and it seems highly likely that we continue to evolve at this super speed today.”32

Since modern humans exist as a distinct species, and genetic evolution has occurred in modern humans since the stone age, during which time many human groups have lived largely on plant-based diets, we should study modern humans, ourselves, not ancient fossils, to discover our nutritional adaptations and requirements.

Summary

First, references to the alleged dietary practices of prehistoric stone age humans in discussions of modern human nutrition constitute a red herring that distracts many people from going directly to the large body of laboratory, clinical, epidemiological, and historical evidence we have accumulated over the past 200 years that constitutes the modern science of nutrition. We don’t need to know anything about the dietary practices of prehistoric hominids in order to know the nutritional needs of modern humans. In contrast, we absolutely must understand the nutritional needs of modern humans to come close to understanding the circumstances under which these needs evolved.

Second, although some of our ancestors did in some circumstances consume an animal-based diet to survive and reproduce in the climatic conditions of some ecosystems, this could not have selected out of the population individuals who became obese, or developed any chronic, age-related disease from the animal-based diet, because reproduction can occur while these diseases are progressing, and an individual affected with these diseases can leave plenty of descendants before dying from diabetes, atherosclerosis, auto-immune disease, cancer, or any other such disease.

Third, the fossil record provides biased and limited evidence of ancient dietary practices. The preservational bias inherent in fossil records favors evidence of meat-eating. We can’t rely on this evidence for a clear view of prehistoric dietary habits.

Fourth, we currently have two competing hypotheses concerning the role of food in the alleged human evolution. The first, oldest, and most widely believed, asserts that “meat made us human” and is taken

32 Holzman D. Modern times causing human evolution to accelerate. New Scientist 14 December 2007. Retrieved September 16, 2013, from www.newscientist.com/article/mg19626343.900-modern-times-causing-human-evolution-to-accelerate.html .

HUMAN EVOLUTION & NUTRITION – 15

by some to imply that humans are obligate carnivores (animals that must eat meat). The hypothesis that the alleged macroevolution of humans was powered by a fat-rich, animal-based diet predicts that modern humans will have specific genetic, anatomical, physiological, and metabolic adaptations and dependence upon animal fats and proteins to sustain peak reproduction and mental and physical performance. This hypothesis also suggests inversely that humans eating plant-based diets will have poor health, mental and physical performance, sexual function, and fertility.

The second hypothesis suggests that early control of fire allowed early human ancestors to consistently and efficiently obtain high energy intakes from cooked starchy foods, which allowed but did not require some of them (primarily males) to invest in risky hunting. The hypothesis that the alleged macroevolution and development of hunting skills within the human lineage was powered by a starch- rich plant-based diet predicts that modern humans will have anatomical, physiological, and metabolic adaptations to a plant-based, starch-rich, low-fat diet, and require a plant-based diet for sustained health, peak mental and physical performance and maximum fertility. It also predicts that modern humans will have little or no metabolic adaptation to an animal-based diet, and will likely develop numerous diseases when consuming an animal-based diet.

Due to the preservational bias inherent in the fossil record, archaeological research does not have the power to help us decide between these hypotheses. However, as I will show throughout this book, only the latter one makes sense in light of what we know about modern human nutritional anatomy, physiology and metabolism, as well as the influence of plant and animal foods on human health.

16 – NATURAL SELECTION & NUTRITION 2: The Nature of Nutritional Adaptations

We are omnivores; therefore, we need to eat animal flesh.33

That sentence expresses what I call the Omnivore Myth. Adherents believe that the fact that many humans do eat flesh, eggs, and milk provides adequate evidence for two conclusions:

1. Humans have specific biological adaptations to consumption of flesh, eggs, or milk, and 2. Humans must eat flesh, eggs, or milk to sustain health.

This ideology may originally arise from the structural defects present in the English language and Aristotelian logic perhaps first noted by Alfred Korzybski, founder of general semantics.34 The phrase “Humans are omnivores” has the form “X is Y.” Korzybski noticed that this type of sentence tends to mislead us into thinking that Y constitutes the fixed essence or identity of X.

General semantics recommends tailoring our descriptions to the phenomenon as closely as possible, without using any form of the verb to be whenever possible. The following sentence more closely represents the phenomenon in question:

Some humans sometimes eat animal flesh as well as plant foods.

This sentence differs markedly from “Humans are omnivores” in that it 1) more closely represents the facts, and 2) does not in any way imply that human behavior provides evidence that all humans have a fixed biological identity (“omnivore”) dictating consumption of animal flesh as well as foods derived from plants. These sentences differ in the same way that “Jack is a murderer” and “Jack once killed a man” differ; the former attributes a fixed identity to Jack, whereas the latter only reports an action that Jack once performed.

The fact that some humans did or do eat flesh can’t in and of itself support the conclusion that flesh- eating constitutes an essential part of the biological identity of humans, any more that the fact that Jack once killed a man supports the conclusion that Jack has always been and will always be a murderer by nature.

Modern humans often engage in behaviors for which they lack specific biological adaptation. For example, humans smoke cigars, live in large cities, travel to the moon, scuba dive, engage in war, and ingest pharmaceutical drugs. We have no a priori reason to believe that all stone age or modern human behaviors arose from or reflected biological requirements or adaptations.

33 Throughout this book, I will use the term “animal flesh” to refer to any and all tissues taken from the living or dead bodies of animals, including eggs and milk products.

34 Korzybski A. Science and Sanity: An Introduction to Non-Aristotelian Systems and General Semantics. Institute of GS, 1958.

Although many animals––e.g. canines, bears, pigs, and chimpanzees––do in fact eat both plant and animal tissues, the simple fact that some individuals of some species consume both plant and animal foods does not tell us what dietary plant-animal ratio promotes the best possible health in that species or individual. To discover how well any species tolerates plant or animal nutrients, or whether any species actually requires any specific nutrients found only in animal flesh, we need to conduct careful scientific research on the living animals, not archaeology or descriptive nutritional anthropology (which only tells us what people do, not what they require).

The Carnivore Ideology

By definition, an omnivore eats both animal flesh and plants. Although laypeople generally reserve the word “carnivore” for species that they think depend largely or completely on animal flesh for their nutrient requirements, since the word “carnivore,” derived from the Latin words for “flesh/meat” (caro) and “to devour” (vorare), means “flesh-eater” or “meat-eater,” all omnivores are carnivores. Moreover, anyone who claims that humans must eat both meat and plants clearly believes that humans “are” obligate carnivores.

Advocates of low carbohydrate diets believe that the best diet for humans consists primarily of animal flesh and fat, and the leading author of scientific papers on contemporary application of putatively animal-based paleolithic diets, Loren Cordain, Ph.D., appears to believe that humans are biologically (genetically) adapted to and may require for best health a diet providing 55 to 65 percent of energy from animal flesh.35, 36 These authors describe humans as an animal that pursues, consumes, and requires a diet consisting primarily of animal flesh. Biologists call such animals facultative carnivores; for example, Finch and Stanford refer to “fossil evidence that early humans were facultative carnivores.”37 No one has identified a specific animal:plant ratio that clearly distinguishes a facultative carnivore from an omnivore.

Further, biologists have also classified carnivores (in the order Carnivora) by their relative dependence upon animal flesh. A hypercarnivore (e.g. lion) consumes a diet consisting of more than 70 percent flesh, a mesocarnivore (e.g. coyote) 50 to 70 percent, and a hypocarnivore (e.g. black bear) less than 30 percent.38 No one can give any logical reason that we should apply these categories only to members of the Carnivora order, since members of that order have diets ranging from virtually zero flesh (pandas) to virtually 100 percent flesh (lions), the same range found outside that order. Indeed, we can find that same range within the human species alone.

35 Cordain L. The Nutritional Characteristics of a Contemporary Diet Based Upon Paleolithic Food Groups. JANA 2002 Summer; 5(3): 15-24.

36 Cordain L. The Paleo Diet. Houghton Mifflin Harcourt, 2010.

37 Finch CE and Stanford CB. Meat-Adaptive Genes and the Evolution of Slower Aging in Humans. The Quarterly Review of Biology 2004 Mar;79(1): 3-50. 19.

38 Van Valkenburgh B. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47(1): 147-163.

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Applying these three categories of carnivore, Cordain believes that humans have genetically adapted to and require a mesocarnivorous diet (55 to 65 percent of energy from flesh), a similar dietary plant:animal ratio as coyotes, foxes, civets, martens, ring-tailed cats, and skunks, all of which belong to the Carnivora order but also get classified as dietary omnivores. Of interest, biologists believe that the earliest members of the order Carnivora had mesocarnivorous diets.39

Thus, from a scientific perspective, the Omnivore Myth describes humans as obligate carnivores. In other words, people who strongly adhere to the belief that humans “are” omnivores usually covertly believe that humans are obligate carnivores.

Plants vs Animals and Plant-eaters vs Carnivores

Among possible foods for animal life, we find two basic types, namely plants and animals. As a consequence of the significant differences between plants and animals, in appearance, behavior, structure, and chemical makeup (Table 2.1), natural selection has favored significant physiological differences between animals that have specialized in eating plants compared to animals that have specialized in eating animals.

Table 2.1: Contrasting Characteristics of Plants and Animals Characteristic Plants Animals Colors Primarily green leaves with brightly colored Primarily brown, black, grey, white, or yellow flowers and fruits. Vary with stages of and frequently camouflaged. Do not vary much development of flowers and fruits; colors throughout life stages, do not indicate stages of indicate stage of ripeness / edibility of parts ripeness or edibility. rich in nutrients.

Sounds Primarily relatively quiet. Relatively noisy due to breathing, movement and vocalizations.

Odors Subtle and variable with stages of life cycle. Stronger and consistent. Flavors Primarily derived from carbohydrates. Primarily derived from protein and fat.

Mobility Primarily immobile, with small range of slow Primarily mobile and elusive, capable of wide motion. ranges and rapid motion.

Composition Primarily sugars. Primarily proteins (amino acids) and fats.

An animal that specializes in eating particular types of plant foods needs organs and metabolic systems that increase its success at identifying and gathering those types of plant foods, and digesting and metabolizing carbohydrates and carbohydrate-derivatives, while an animal that specializes in eating other animals needs organs and metabolic systems that increase its ability to detect, track, chase, and capture elusive animals, then digest and metabolize animal fats and proteins and their breakdown products. For example, a primarily frugivorous animal may need equipment to help it determine when

39 Ibid.

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to gather a fruit or leave it alone, while a flesh-eating animal needs equipment to help it move very quickly and powerfully to capture, hold, and subdue a rapidly moving, struggling animal.

Omnivore Or Not?

Among non-human animals, we can find some species that as a matter of fact consume animal flesh, yet do not have any dietary requirement, specific adaptation to, or even significant metabolic tolerance for it.

To illustrate, the wild rhesus monkey primarily consumes fruit supplemented by seeds, buds, and barks, and observers have also seen them eat insects and small game, making the rhesus a behavioral omnivore. When scientists fed rhesus monkeys a high-fat (40% energy) diet containing very small amounts of cholesterol (found only in animal tissues), the lowest amount (43 mcg/kcal) equivalent to less than one egg yolk for a 3000 kcal diet, for 18 months, they developed pathological arterial intimal thickening and increased aortic cholesterol compared to controls not receiving the cholesterol, despite maintaining plasma total cholesterol in the range found in monkeys fed cholesterol-free diets (130-170 mg/dl).40

Hence, although rhesus monkeys occasionally eat animal flesh, they have little tolerance for sustained exposure to dietary cholesterol, which occurs only in animal foods. This shows that a wild species can engage in a behavior that, if sustained on a daily basis for a long period of time, would cause it harm.

Two Kinds of Omnivores

Since the equipment required for successful acquisition, digestion, and metabolism of plants and their major components differs so markedly from the equipment required to capture, digest, and metabolize animals, it should not surprise anyone if we found that very few if any species have native physical equipment equally well-suited to processing plant foods and animals.

Based on behavior, people have classified pigs, chimps, dogs, and bears as omnivores, yet the wild feeding behavior, anatomy, and physiology of the former two differs markedly, and in a similar fashion, from the latter two. Classifying bears, dogs, and pigs all as omnivores obscures very important physical and behavioral differences between them.

Although they will eat some animal flesh, wild pigs primarily consume roots, fruits, leaves, grasses, and flowers, and they have specialized dentition and guts clearly adapted to a plant-based diet, including a hindgut specialized for fermentation of plant fibers. Wild pigs innately forage for plant foods, and only consume animal flesh opportunistically. Commercially raised pigs develop and grow very well on diets composed entirely of plants, indicating that pigs do not require animal food.

40 Armstrong ML, Megan MB, Warner ED. Intimal Thickening in Normocholesterolemic Rhesus Monkeys Fed Low Supplements of Dietary Cholesterol. Circ Res 1974;34:447-454.

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Table 2.2: Some behavioral omnivores, their gut features and primary foods Species Order Gut features Diet Badgers Carnivora Shearing teeth, short simple Mainly animals, some roots and gut botanical fruits1 Bears Carnivora Sharp pointed incisors and Animal-based when possible; mainly large shearing canines, short botanical fruits1 (acorns, nuts, berries, simple gut drupes) when plant-based Coatis Carnivora Shearing teeth, short simple Mainly animals, some fruits gut Canines (wolves, Carnivora Shearing teeth, short simple Mainly (~80%) animals, some fruits dogs) gut Raccoons Carnivora Shearing teeth, short simple Mainly animals, some fruits and nuts gut Skunk Carnivora Shearing teeth, short simple Mainly animals, some fruits, nuts, gut fungi, leaves Opossums Didelphimorph Shearing teeth, short simple Mainly animals, supplemented by (marsupial) gut fruits Hedgehogs Erinaceomorpha Shearing teeth, short simple Mainly animals, some fruits, roots, (previously Insectivora) gut fungi Sloth Pilosa (Folivora) Grinding teeth, long complex Mainly buds, shoots, and leaves gut Chimpanzees Primates Grinding teeth, long complex Mainly botanical fruits1 and leaves gut Spider monkey Primates Grinding teeth, long complex Mainly (up to 90%) botanical fruits1 gut Chipmunks Rodentia Grinding teeth, long complex Mainly botanical fruits1 (seeds and gut grains) Mice Rodentia Grinding teeth, long complex Mainly botanical fruits1 gut Rats Rodentia Grinding teeth, long complex Mainly botanical fruits1 (seeds and gut grains) Pigs Artiodactyla Grinding teeth, long complex Mainly fruits, roots, and leaves gut Squirrels Rodentia Grinding teeth, long complex Mainly botanical fruits1 (nuts and gut seeds) 1. Botanical fruits include sweet fruits, nuts, grains, legumes, and berries, all characterized by a relatively low fiber content coupled with high contents of enzymatically digestible sugars, starches, proteins, or fats.

In contrast to pigs, bears and wolves clearly have innate behavioral and physiological adaptations to a meat-based diet (claws, teeth, guts, predatory behavior), neither one having any gut features specialized for processing plant foods, although wolves sometimes get 40% of their food from fruits (such as wolfberry, Lycium barbarum), and when without prey options, bears may eat large amounts of botanical fruits.

As we can see from Table 2.2, many and possibly all mammalian, terrestrial “omnivores” fall into one of two groups:

1. Animals such as the bear, wolf, coatis, raccoon, etc., which have the shearing teeth and short, simple gut typical of a physiology adapted to hunting and meat-eating, and whenever possible eat flesh-based

THE NATURE OF NUTRITIONAL ADAPTATIONS – 21

diets, but will eat variable amounts of fruits or nuts, or nutritionally similar plant parts when possible or necessary. Most of these belong to the order Carnivora. 2. Animals such as rodents, primates, and pigs, which have the grinding molars and long, complex guts typical of evolved herbivores, and whenever possible primarily consume diets rich in botanical fruits or roots, but will consume animal flesh opportunistically or out of necessity (e.g. starvation).

Another way to put this: One group consists of opportunistically frugivorous carnivores, and the other group consists mainly of opportunistically carnivorous frugivores.

Since the ancestors of extant carnivores always pursued meat as their primary food, natural selection favored among them the survival of individuals having a high tolerance for and nutritional dependence upon certain substances present only in flesh. However, they have no nutritional dependence on direct consumption of plants; they can live their entire lives in excellent health without ever consuming plant foods.

Frugivores have the ability to enzymatically digest botanical fruits and their seeds, some of which (e.g. peas, coconuts, avocados, almonds, sunflower seeds) contain large amounts of protein or fat. Therefore, the carnivore and frugivore gut physiologies display some similarities (exemplifying convergent evolution), and the frugivore’s digestive physiology allows it to digest animal flesh. However, since frugivores descended from a lineage specializing in acquisition, digestion, and metabolism of fruit and vegetables, natural selection favored among them the reproduction of individuals having a nutritional dependence, not on flesh, but on fruits and vegetables. For example, the de facto omnivorous primates have physiologies primarily adapted to folifrugivory, not to carnivory.

Animals that, in the absence of human intervention, must eat flesh to maintain health– obligate carnivores–have a dietary requirement for ingestion of substances uniquely provided by animal flesh. Although not commonly acknowledged, some animals must eat certain plant foods to maintain health. These obligate plant-eaters have as a consequence of natural selection a dietary requirement for specific substances or nutrient profiles provided by plant-based diets.

Natural Selection of Nutritional Adaptations

If an animal evolves for millions of years in dependence on a diet that has a shortage of or depletes a specific nutrient, natural selection will favor those individuals who have mechanisms that will minimize the need for that nutrient and avidly conserve it to minimize losses and prevent deficiency. If an animal evolves in an environment and on a diet that supplies an excess of a specific nutrient, natural selection will favor the reproduction of mutants who have mechanisms that will minimize absorption of that nutrient and rapidly dispose of the excess to prevent toxicity.

To illustrate, among plants, cacti evolved in arid environments, which favored the reproduction of individuals having mechanisms for maximizing absorption, storage, and conservation of water. Consequently, they have succulent tissues and you can quickly kill a cactus by giving it too much water too often, because all of its evolved mechanisms will cause it to over-hydrate and rot. In contrast, water

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lilies evolved in water, so natural selection favored the reproduction of lilies that have mechanisms for eliminating excess water, and have a high water requirement; they will die quickly if not immersed in water.

These differences in plants form the basis for classical Chinese herbal medicine. Plants adapted to arid environments, such as aloe vera, have moisturizing properties because their tissues have naturally selected molecules that retain moisture. On the other hand, plants adapted to wet environments, such as water lilies, have drying properties, because these species produce naturally selected molecules that help them expel excess fluids.

Table 2.3: Some qualities denoted by the terms “yin” and “yang” in Chinese scientific discourse.

Quality Yin Yang

Color Black-Blue-Green White-Yellow-Red

Sounds Quieter Louder

Temperature Cooler Warmer

Luminescence Darker Brighter

Humidity Moister Drier

Texture Smoother, softer Rougher, harder

Flavor Sweeter Saltier

Activity More inertial More mobile

Traditional Chinese scientists developed the yin-yang theory as a result of observing that all natural processes involve a play of complementary opposites. The terms “yin” and “yang” simply serve as a shorthand method for referring to a constellation of intrinsically related sensible qualities (Table 2.3). By intrinsically related, I mean that in each of the yin (or yang) qualities we detect all other yin (or yang) qualities. For example, in the more yin colors we sense coolness, quietude, softness, and wetness; while in the more yang colors we sense warmth, loudness, roughness, and dryness. We sense a darkness in quietude, a quietude in darkness, a coolness in soft, a softness in cool, a softness in wetness, and a wetness in softness, and so on. On the other hand, we detect a hardness in loud, a loudness in hard (compare the sound of tapping a pillow to tapping a table), a dryness in roughness, a roughness in dryness, and so on.

Once you consciously integrate your ability to detect yin-yang relationships of complementary opposition in natural systems, you will have adopted a new, wholistic perspective on how these systems operate. I have implemented this perspective throughout this book in describing how present human physiology ‘mirrors’ the conditions under which it evolved. Let me illustrate how it can help us understand nutritional adaptations in animals, both carnivores and plant-eaters.

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As shown in Table 2.1, plants and animals have complementarily opposite features. In general, plants have more yin features: cool, quiet, moist, soft, sweet, and coloration dominated by the green-blue spectrum; while animals have more yang features: warm, noisy, dry, rough, salty, and colors primarily in the white-red spectrum. These sensible characteristics arise from the composition and structure of the organism, which in turn arose as an adaptation to its native habitat.

Plants live by photosynthesis. Their leaves absorb hot, red, oxidizing, drying sunlight and reflect cool, green light. To survive the long hours in sunlight, they must have mechanisms for retaining moisture and counteracting coagulation, inflammation, and oxidation; consequently, they have large amounts of hydrating, antioxidant, anticoagulant, and anti-inflammatory molecules in their tissues. An animal that specializes in feeding on specific types of plants will have continuous exposure to these molecules, and natural selection will favor those individuals that capitalize on the constituents of those plants.

For example, in an animal that feeds on plants containing anticoagulants, natural selection will favor those individuals that have a coagulation system adapted to the presence of those dietary anticoagulants. Probably the favored individuals will produce more procoagulant factors than it would need if its natural diet did not contain the anticoagulant-rich plants. If we take that animal off of its natural diet rich in anticoagulants, its blood will now lean toward excess viscosity, coagulation and thromboses. We can say that this animal requires dietary anticoagulants to maintain balance in its coagulation system. If you have wondered why humans eating conventional diets seem to “need” aspirin (derived from the anticoagulant phytochemical salicylic acid, abundant in fruits in vegetables) to ward off thromboses, this provides you with a clue.

In contrast to plants, animals live by oxidation of organic molecules obtained by consumption of plants or animals. Consequently, animal tissues absolutely must have a molecular soup containing many pro- oxidant molecules. Animal tissues also have pro-coagulant and pro-inflammatory molecules, produced to maintain structural integrity, regulate circulation and control injuries, and if the animal eats a plant- based diet containing large amounts of antioxidant, anticoagulant, and anti-inflammatory molecules, it will naturally produce enough pro-oxidant, pro-coagulant, and pro-inflammatory molecules to counter the phytochemicals to which its species has adapted.

Consequently, among animals biologically adapted to living on animal flesh natural selection will have favored natural mechanisms for countering the effects of regular ingestion of pro-oxidant, pro- inflammatory, pro-coagulant molecules found in meat. For example, these carnivorous species may have a lower endogenous production of pro-oxidant, pro-inflammatory, and pro-coagulant molecules than herbivorous species; or a higher endogenous production of anti-oxidant, anti-inflammatory, and anti-coagulant molecules. These species will have the ability to eat animal flesh day in and day out without incurring an increased risk of thrombosis, excess oxidation, or inflammatory diseases.

In contrast, a species adapted to a herbivorous diet containing plenty of anticoagulant, anti- inflammatory, and anti-oxidant phytochemicals probably has a much higher endogenous production of pro-coagulants, etc., than a biological omnivore/carnivore. If such a species consumes animal flesh,

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thereby ingesting more pro-coagulants, etc., it will incur an increased risk of diseases involving thrombosis, excess oxidation, and inflammation.

For another example, animal foods provide large doses of sodium and relatively low doses of potassium, and plant foods, the opposite. Consequently, animals biologically adapted to plant-based diets have physiologies that conserve sodium and rapidly excrete potassium. Therefore, if an animal adapted to eating plant foods adopts a diet of flesh, it will probably get an overdose of sodium and a deficiency of potassium. The degree of the imbalance might be great enough to cause chronic disease in individuals without significantly impairing their reproductive ability and ability to pass on their genes.

For a last example, plants provide virtually no cholesterol, and contain substances (e.g. fiber and phytosterols) that bind with cholesterol released (as part of bile) into the gut during digestion. Therefore, in animals eating a plant-based diet, natural selection will favor individuals having very efficient recycling of bile and endogenous production of cholesterol high enough to counter the cholesterol-depleting effects of its diet. If such an animal adopts flesh-eating, it has less intake of cholesterol-depleting substances (because the flesh displaces plants) while ingesting significant amounts of cholesterol from the flesh. This may lead to an increase in blood cholesterol. Again, and depending on context, this might not have a strong enough impact on reproductive ability to exert a significant selective pressure in favor of mutants who have more efficient cholesterol excretion or less efficient absorption. Instead, it will probably lead to chronic hypercholesterolemia and age-related cardiovascular diseases.

In contrast, since animal flesh contains plenty of cholesterol, among carnivorous species, natural selection will favor those individuals who have compensatory mechanisms to reduce cholesterol accumulation. These might include reduced endogenous production of cholesterol (which possibly would create a dependence on dietary cholesterol), increased cholesterol excretion (e.g. through modification of bile acid composition, as found in bears; see below), or reduced absorption of dietary cholesterol. Among such animals, exposure to high levels of dietary cholesterol will either be essential or very well tolerated with no adverse effects.

To summarize, animals naturally adapted to plant-based diets have a dietary requirement or high tolerance for the spectrum of phytochemicals or nutritional profile found in their native diets, while animals naturally adapted to meat-based diets have a dietary requirement or high tolerance for the compounds or nutritional profile uniquely supplied by animal flesh.

Biological Versus Behavioral Adaptations

In some cases, changes in behavior, including culture or technology, can enable a species to continuously consume foods largely incompatible with its basic physiology, but not without a price.

The curious case of the panda illustrates the issue well. The pandas belong to the order Carnivora, and like other bears their anatomical and physiological features clearly indicate a primary adaptation to

THE NATURE OF NUTRITIONAL ADAPTATIONS – 25

consuming animal flesh.41 They retain all the genetic requirements for maintaining a purely carnivorous diet.42 However, due to loss of prey in their native habitat, pandas have turned to subsist on a diet consisting primarily of bamboo.

Despite the panda lineage living on bamboo for an estimated three million years, they have few heritable physiological adaptations to this lifestyle. Like other bears, natural selection has favored pandas having some dental adaptations to eating plants (discussed in Chapter 5), but their digestive system still has the short, simple structure found in carnivores. This short and simple gut lacking fermentation chambers severely limits the panda’s ability to extract nutrients from very fibrous bamboo, so pandas have adapted primarily by reducing their energy expenditure in physical activity to a minimum and sleeping a lot, which allows them to maintain a layer of body fat to minimize energy loss.43

Although some people classify all bears as omnivores, when we look at their anatomy and physiology, we find clear heritable biological adaptations that serve to facilitate flesh-eating, such as preference and appetite for flesh and blood, acute sense of smell (up to seven times more powerful than dogs), shearing teeth, a short and simple gut, and a production of bile exceptionally high in ursodeoxycholic acid, which improves fat digestion, reduces cholesterol absorption, and prevents formation of cholesterol gallstones.44 The polar bears utilize this physiology to its fullest. Like pandas, other bears that consume plant-based rather than flesh-based diets have adapted to more plant-based diets largely by behavioral changes to minimize energy expenditure, such as reducing physical activity to maintain a thick layer of body fat, and denning or hibernating.

In short, bears have a carnivore physiology primarily adapted to eating flesh, but some bear species happen to have found a way to get along well enough to sustain their lineage on diets composed largely of fruits, or, in the case of the panda, highly fibrous bamboo, despite their lack of adequate physiological equipment for the job.

However, this “adaptation” comes at a distinct biological price. For example, pandas have an extraordinarily difficult time with reproduction. Simply, their gut physiology limits their ability to extract nutrients from their bamboo-based diet, which in turn limits their rate of reproduction:

“Their poor, low-energy bamboo diet prevents giant pandas from devoting much energy to gestation or lactation. As a result, giant pandas are the smallest newborn of any nonmarsupial mammal and they grow very slowly. Giant panda infants weigh just four to six ounces at birth

41 Buchen L. Could Pandas Be an Evolutionary Mistake—or Proof of an Intelligent Designer? Discover Magazine Online, August 8, 2005. Retrieved September 18, 2013 from http://discovermagazine.com/2008/aug/05-could-pandas-be-an- evolutionary-mistake2014or-proof-of-an-intelligent-designer

42 Li R, Fan W, Tian G, et al.. The sequence and de novo assembly of the giant panda genome. Nature 2010 Jan 21;463:311-17.

43 Buchen L, op. cit..

44 Lanzini A, Northfield TC. Effect of ursodeoxycholic acid on biliary lipid coupling and on cholesterol absorption during fasting and eating in subjects with cholesterol gallstones. Gastroenterology. 1988 Aug;95(2):408-16. Abstract.

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and young are a year old before they reach 75 pounds, which is about one-third of adult weight. And this growth rate is based on giant pandas in zoos, where mothers are fed rich diets, with fruits, vegetables, meat, vitamins, and minerals supplementing their daily ration of bamboo; growth of cubs in the wild is likely to be slower still.”45

This illustrates one of the ways we can determine the primary nutritional adaptation of a species. Animals primarily adapted to meat-based diets produce more offspring when fed meat-based diets than when fed plant-based diets; and animals primarily adapted to plant-based diets produce more offspring when fed plant-based diets than when fed animal-based diets. I devote Chapter 11 to discussing this topic in relation to humans.

I would like to note that we can’t rationally label foods as “low energy” or “high energy” without reference to the consumer, because the energy content of the food remains relative to the digestive physiology of the individual eating it. The bamboo diet is “low energy” for the panda, but it wouldn’t be so for an animal biologically adapted to extracting energy from cellulose.

For example, rabbits and cattle live largely on fibrous foods like leaves of grasses, yet they do not have trouble extracting enough energy from those foods to support efficient gestation or lactation. A cow fed only grass can give birth to a calf that weighs about 84 pounds, and produces large amounts of very rich milk that will allow her calf to gain about two pounds of body mass daily. The calf will weigh 550 to 600 pounds by time of weaning (nine months), a gain of 500 pounds in nine months, compared to the 75 pounds per year gain found in pandas.

The bears eating largely plant-based diets, particularly the panda, provide examples of species having very definite physiological adaptations to a flesh-based diet that have adapted behaviorally and culturally to eating plants while substantially retaining their original constitution. They illustrate clearly that the feeding behavior of a species does not tell us whether the species has a physiology well-suited to that behavior. The fact that the panda eats a diet of bamboo doesn’t justify classifying the panda as a physiological herbivore.

Yet the panda also shows that a species with a Carnivoran genetic, anatomical, and physiological constitution can find ways to adapt to a 100% plant-based diet, without human assistance. Keep this in mind the next time you hear someone say that we humans, who have a genetic constitution more than 95% similar to the plant-eating great apes, are poorly adapted to plant-based diets.

Primates

Zoologists classify humans as primates. Many primates eat both plants and animals, making them de facto behavioral omnivores. Most primates have heritable physiological specializations adapted to one of three different primary feeding strategies.

45 Kleiman DG. Giant panda reproduction. Retrieved September 18, 2013 from http://www.4panda.com/panda/pandatips/ reproduction.htm

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Faunivorous primates (mainly insect eaters) primarily consume animal flesh46 and have simple, globular stomachs; convoluted small intestines; a short, conical caecum; and a simple, smooth-walled colon.47 Most primate species that rely primarily or largely on insects have relatively small bodies (smaller than chimpanzees).48 Small-bodied primates weighing less than 500 grams (1.1 pounds) can capture enough insects to supply a majority portion of their energy requirements, but large-bodied primates weighing more than 500 grams can not and must rely primarily on fruits or leaves.49

Folifrugivorous primates, such as the chimpanzee and the gorilla, specialize in eating fruits and fibrous vegetation, with a heavy dependence on leaves. For example, the chimpanzee diet consists of about 48% fruit, 25% leaves, and 27% a mixture of seeds, blossoms, stems, pith, bark and resin. Folivorous- frugivorous primates have simple stomachs, a relatively reduced small intestine, a large caecum, and a capacious haustrated colon.50 Their colons comprise a greater proportion of their total gut volume than their small intestines.

Table 2.4: Types of Botanical Fruits (Fleshy and Dry)

Type Example Type Example

Achene Strawberry Hesperidium Citrus

Berry Currant, tomato Legume Pea, peanut, lentil, bean

Capsule Brazil nut Nut Almond, chestnut

Caryopsis Corn, wheat, rice Pepo Melons, squashes

Drupe Cherry, plum, olive Pome Apple, pear, rosehips

Drupe, fibrous Coconut, walnut Syconium Fig

Primarily frugivorous (or frugifolivorous) primates feed very heavily on fleshy or dry botanical fruits (Table 2.4), including primarily sweet fruits, but also legumes, nuts, and seeds, with lesser amounts of various fibrous plant parts, primarily leaves. Examples include the spider monkey, described as “extremely frugivorous,”51 whose diet averages about 75 percent fruit and at times consists of 90 percent

46 Invertebrate (e.g. insects) or vertebrate.

47 McNab B. The Physiological Ecology of Vertebrates: A View from Energetics. Cornell University Press, 2002. 399.

48 Fleagle JG. Primate Adaptation and Evolution. Academic Press, 1998. 286-288.

49 Ibid.

50 McNab, op. cit., 399.

51 Milton K. Food choice and digestive strategies of two sympatric primate species. The American Naturalist, April 1981; 117 (4): 496-505.

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fruit and nuts. Primarily frugivorous primates have simple stomachs; long, convoluted small intestines; a reduced caecum; and a relatively compact, but haustrated (pouch-walled) colon.52

As we shall discuss in detail in several chapters below, the human gut fits the frugifolivorous pattern.

Frugivores

Fleshy and dry botanical fruits (Table 2.4) differ from leaves and stems of plants by having a higher concentration of digestible sugars, proteins, or fats, and a lower concentration of insoluble fibers such as cellulose. Consequently, the digestive physiology of animals biologically adapted to a fruit-based diet (frugivore or frugifolivore) differs significantly from that of an animal biologically adapted to significant feeding on leaves, grasses, or herbage (folivore or folifrugivore).

The herbivore/folivore depends very heavily upon symbiotic microbes for digestion of fiber. Some of these animals, such as ruminants like goats and cattle, house the symbionts in the foregut, in capacious multi-chambered stomachs, while others, such as pigs, horses, gorillas, and chimpanzees, house them in the hindgut, including a capacious cecum and colon. We call these two types, respectively, foregut fermenters and hindgut fermenters.

As already noted, we know of two types of frugivorous primates. One type, the folifrugivore, pursues a diet consisting largely of botanical fruits, while also consuming substantial supplementary amounts of leaves and other fibrous plant materials. Chimps, gorillas, orangutans, and other primates of this type have large hindguts53 and derive a large portion of their energy from hindgut fermentation of fiber.

The second type, the frugifolivore, pursues a more highly fruit-based diet and much less fibrous vegetation. The spider monkey and other primates of this type have relatively smaller hindguts54 and derive less of their energy from hindgut fermentation of fiber.

More frugivorous primates have midguts (small intestine) equipped primarily for enzymatic digestion of the relatively abundant sugars, starches, proteins, and fats found in the various types of botanical fruits (or similar foods, such as starchy tubers and roots). Since botanical fruits and similar foods have a high proportion of enzymatically digestible carbohydrates, proteins, or fats, very highly frugivorous species such as the spider monkey neither need nor have the capacious multi-chambered stomachs found in foregut fermenters, nor the capacious cecums found in hindgut fermenters.

In its high reliance upon enzymatic digestion rather than cellulose fermentation, the gut of a primarily frugivorous animal somewhat resembles the gut of a primarily carnivorous species. The frugivore’s ability to pursue and digest animal flesh arises not from a specific adaptation to consumption of animal

52 McNab, op. cit., 399.

53 Ibid., 399.

54 Ibid., 399.

THE NATURE OF NUTRITIONAL ADAPTATIONS – 29

matter, but from the fact that some of the requirements for successful adaptation to a highly frugivorous diet resemble in some respects the requirements for successful adaptation to a carnivorous diet, resulting in somewhat convergent evolution.

Summary

If you believe that humans need to eat meat to maintain health or reproduction, you believe that humans “are” obligate carnivores.

Among terrestrial mammals, many and possibly all behavioral omnivores appear to fall into one of two groups:

1. Primarily carnivorous animals having a suite of heritable physiological characteristics clearly adapted to flesh-eating, who will under some circumstances (e.g. stress, necessity, or opportunity) eat plants, primarily botanical fruits, as needed, or, as in the case of some bears, particularly the panda, have behaviorally adapted to eating plant-based diets by adopting energy-conserving habits that have become part of their culture.

2. Primarily frugivorous animals having a suite of heritable physiological characteristics clearly adapted to eating plant foods, who naturally prefer plant foods (i.e. carbohydrates) and generally eat predominantly plant-based diets, but will under some circumstances (e.g. stress, necessity, opportunity, or for sport) eat some insects, animal flesh, or eggs.

As explained in this chapter, although animals having heritable adaptations to a plant-based diet may have no heritable characteristics unequivocally and specifically originated to facilitate acquisition, consumption, digestion, and metabolism of animal flesh, heritable adaptation to a specific kind of plant- based diet––frugivory––may confer a limited ability to acquire, consume, digest, and metabolize animal flesh as a result of somewhat convergent evolution.

Further, due to the wide range of significant differences between plants and animals, natural selection will favor in an obligate plant-eater such as a frugivore heritable anatomical, physiological and metabolic characteristics specifically adapted to plant foods. The interaction of these characteristics with dietary animal flesh may result in the plant-eater or frugivore having a tendency to develop chronic metabolic disorders when habitually consuming animal flesh.

So, regardless of whether you classify humans as omnivores or carnivores, either classification raises the following three questions:

1. Do humans have any specific heritable characteristics, acquired by mutation and natural selection, that unequivocally and specifically originated and function primarily to facilitate acquisition, consumption, digestion, and metabolism of plants?

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2. Do humans have any specific heritable characteristics, acquired by mutation and natural selection, that unequivocally and specifically originated and function primarily to facilitate acquisition, consumption, digestion, and metabolism of animal flesh?

3. Do humans have any proven dietary requirement for at least one substance available only by consumption of animal flesh?

The remaining chapters answer these questions, and provide evidence that humans have a physiology highly adapted to a plant-based diet, with no currently known requirement and little to no metabolic tolerance for habitual consumption of animal flesh. This evidence supports the hypothesis that human evolution was powered by plants.

THE NATURE OF NUTRITIONAL ADAPTATIONS – 31

Part II: Human Nutritional Physiology

3: Sensation and Nutrition

The sensory system (sight, hearing, olfaction, taste, touch) guides an animal to select appropriate foods. Since plants and animals differ significantly in sensible characteristics (Table 3.1), animals biologically adapted to a primarily plant-based diet generally have sensory systems that differ markedly from those found in animals that have biologically adapted to consumption of animal flesh.

Table 3.1: Sensible Characteristics of Plants and Animals Characteristic Plants Animals Colors Very colorful flowers and fruits that attract Commonly camouflaged to reduce visibility; pollinators and seed dispersers; vary with stages do not vary much throughout life stages, do of development of flowers and fruits; colors not indicate stages of ripeness or edibility indicate stage of ripeness / edibility of parts rich in nutrients Sounds Relatively quiet. Relatively noisy due to breathing, movement and vocalizations. Odors Subtle and variable with stages of life cycle Stronger and consistent Flavor sources Primarily sugars and starches, organic acids Primarily proteins (amino acids) and fats, secondarily mineral salts

Plants typically have little odor, little motion, and make little sound, but have vibrant colors, particularly of flowers and fruits. In contrast, animals emit stronger odors, engage in lots of motion, make distinct noises (both as a result of motion and as vocalizations), and typically have coloration that makes them hard to detect visually (i.e. camouflage).

A plant-eater needs to be able to discern ripeness of fruits or vegetation before tasting (otherwise s/he wastes an unripe fruit), which is very often signified by color. Since prey typically have camouflage coloration making visual identification of prey unreliable, a carnivore needs to reliably detect the motions, sounds, and odors of prey. Thus a plant-eater obtains more benefits from color vision and visual acuity than from acute olfaction or hearing, whereas a flesh-eater benefits more from keen senses of hearing and smell than from color vision.

Plant tissues primarily consist of carbohydrates (sugars); while animal tissues primarily consist of proteins composed of amino acids, along with fats. Thus, a plant eater benefits most from an ability to taste and enjoy sugars and starches. In contrast, an animal will have most success at obtaining animal flesh if it has an ability to taste and enjoy the flavor of straight raw animal flesh.

Our sensory system differs very markedly from that of an animal specifically adapted to eating animal flesh. We have sensory abilities consistent with the hypothesis that human evolution was powered by plants.

Vision

Emphasis on vision supports gathering plants, which have little odor but distinct shapes and colors (particularly in flowers and fruits), whereas emphasis on smell supports hunting animals, which have distinct odors but camouflage coloration. The visual cortex dominates the human brain, but the olfactory cortex dominates the brain of dogs and cats.

According to Stanley Coren, a professor of psychology and expert on human-dog interactions, humans have a visual system very specifically adapted to a diet based on gathering various types of botanical fruits; whereas the dog has a sensory system naturally, primarily, and very specifically adapted to hunting animals:

“Because humans evolved from tree-dwelling primates, we needed eyes that could see colors (to pick out ripe fruit and nuts from among the leaves of trees), good visual acuity (to see small nuts and berries), and good depth perception (so that we would not misjudge the distance between branches and fall to the ground). The ancestors of dogs were primarily hunters and meat eaters that were adapted to run swiftly on the ground to pursue prey that might be distant but still within chasing range. Canines are also ‘crepuscular,’ meaning they are usually active at dusk and dawn and are more comfortable than humans when operating in dim light. The type of eye needed for twilight and nighttime activity requires sensitivity to low levels of brightness, but perception of color is really not very important.”55

An animal adapted primarily to hunting needs a good ability to discriminate moving objects (prey). Cats and dogs have relatively poor visual acuity compared to humans, but a greater ability to discriminate moving objects.

“One study of fourteen police dogs found that the dogs could recognize an object when it was moving even at distances of over half a mile (900 meters), but if that same object was stationary and much closer (just over 600 yards or 585 meters), they could not discriminate it.”56

Experiments have shown that dogs can resolve flickers at 75 Hz whereas humans can only resolve flickers at 55 Hz.57 Therefore, dogs detect things in motion much more efficiently than humans, but humans detect stationary objects more efficiently than dogs. This indicates that the survival of ancestral humans depended primarily on visually detecting stationary or relatively slowly moving things (e.g. plants), whereas the survival of ancestral canines depended primarily on visual detection of quickly moving things (animals).

55 Coren S. How Dogs Think: Understanding the Canine Mind. New York, Free Press, 2004. 17.

56 Ibid., 26.

57 Ibid., 29.

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Humans finely discriminate colors, whereas cats and dogs have poor color discrimination. For example, dogs see the colors of the world as yellow and blue; they see green, yellow, and orange as yellowish, they see violet and blue as blue; and they see red as a very dark gray or perhaps even as black.58 Our polychromatic vision with high resolution of stationary objects supports the identification of fine distinctions between stationary objects, such as identifying the subtle differences between two very similar leaves or fruits, one of which presents danger (toxins) or ripe nutrients and the other not.

Polychromatic vision has limited usefulness to an animal that hunts due to the camouflage of prey. Also, most predators hunt primarily at dawn or dusk, when dim lighting serves as cover for the predator, and also reduces colors to shades of black and white. Consequently, predators generally have excellent vision in dim light. Paul Miller, clinical professor of comparative ophthalmology at University of Wisconsin-Madison, explains:

“‘Dogs have evolved to see well in both bright and dim light, whereas humans do best in bright light. No one is quite sure how much better a dog sees in dim light, but I would suspect that dogs are not quite as good as cats,’ which can see in light that’s six times dimmer than our lower limit. Dogs, he says, ‘can probably see in light five times dimmer than a human can see in.’”59

Dogs and cats have eyes with heritable characteristics naturally selected for dim-light vision, including:

• A greater ability to enlarge the pupil to let in more light. • A greater retinal concentration of the most light-sensitive cells (rods), whereas humans have a greater concentration of the color-detecting cells (cones). • The light-sensitive compounds in their retinas respond to lower light levels. • A lens located closer to the retina, producing a brighter image on the retina. • The tapetum, a mirror-like structure that reflects light, giving the retina a second chance to register light that has entered the eye, which makes their eyes glow in the dark.

In short, humans have a visual system naturally and specifically adapted to gathering fruits, vegetables, nuts, and seeds, and not well adapted to hunting animals. Note also that these systems don’t overlap very much, meaning that the canine visual capacities will not make dogs very successful at gathering fruits and vegetables, and the human’s visual system does not have the powers that increase success at hunting. In other words, canines (and felines) have a visual system relatively maladapted to living on fruits, while humans have a visual system relatively maladapted to living by hunting.

58 Ibid., 33.

59 University of Wisconsin - Madison (2007, November 9). How Well Do Dogs See At Night?. ScienceDaily. Retrieved September 16, 2013, from http://www.sciencedaily.com/releases/2007/11/071108140336.htm

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Hearing

Cats and dogs, like many other animals, have in comparison to humans, relative to body size, larger and more mobile ears to enable greater sound reception. Dogs and cats have a much greater hearing range than humans, which facilitates stalking camouflaged or hidden prey.

Dogs can detect sounds with frequencies between 47,000 and 65,000 Hz, whereas a young human can detect only sounds with frequencies less than 20,000 Hz. Also, dogs have a higher sensitivity to low intensity sounds having frequencies above 3,000 Hz. Up to 12,000 Hz, dogs can detect noises that humans cannot detect (between –5 and –15 decibels), and above 12,000 Hz the dog’s ability to detect sounds exceeds human ability so greatly that numerical comparison doesn’t make sense.60

Coren thinks that this difference in ability to detect high frequency sounds probably arose as a result of natural selection:

“Dogs can hear sounds in the very-high-frequency range because of the evolutionary history of their wild ancestors. Wolves, jackals, and foxes often prey on small animals like mice, voles, and rats, which make high-pitched squeaks, and their scrabbling around in the leaves and grass produces high-frequency rustling and scraping sounds. Although some wild canine species like the wolf can and will hunt larger prey like deer, wild sheep, or antelope, field studies show that the summer diet of many wolves is mainly composed of small rodents like rats and mice, supplemented with an occasional rabbit. The ability to hear the high-frequency sounds that these little creatures make is therefore a matter of survival, and it is likely that only those canines that developed high-frequency hearing abilities actually endured and prospered. Cats, whose entire sustenance may depend upon small rodents, can hear sounds that are 5,000 to 10,000 Hz higher than dogs.”61

Cats can detect a range of sound frequencies two to three times greater than humans.62 Dogs can hear sounds four times farther away than humans,63 which equips them for detecting and tracking mobile prey.

Thus, natural selection equipped canines and felines with very sensitive hearing that enables them to detect the movements of prey regardless of visibility, thus increasing their success at hunting. In contrast, humans have hearing poorly adapted to hunting.

60 Coren, op. cit., 40.

61 Ibid., p. 41.

62 Strain GM. How well do dogs and other animals hear? Professor of Neuroscience, School of Veterinary Medicine, Louisiana State University. http://www.lsu.edu/deafness/HearingRange.html

63 Animal Physiology Class. General Physiology of Dogs. Davidson College. http://www.bio.davidson.edu/Courses/anphys/ 2000/Hatfield/Hatfield2.htm

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Olfaction

The olfactory cortex dominates the dog’s brain, and is forty times larger than that of the human relative to brain size.64 The dog’s sense of smell is somewhere between one thousand and ten thousand times more sensitive than that of humans.65 According to Darwinian theory, natural selection favored canines with this acute sense of smell because it improves their efficiency at hunting:

“The dog’s nose initially evolved to help him hunt. As a hunter he requires two things of his nose. First, he has to be able to detect scents. He must also be able to recognize the species of the animal that left the scent and also the scent unique to the particular individual that he is tracking. Discriminating the scent of an individual is important because wild canines often work by chasing their prey until it becomes too exhausted to run any farther or to put up a struggle. Of course this means that they have to stay with that specific animal.

“Consider a pack of wolves that has isolated a caribou and begins to chase it. If the animal simply stayed out on the plain and kept away from the other members of its herd, there would only be the task of pursing [sic] it until it was weak enough to be attacked. Like many of the animals that wild canines hunt, however, caribou are herd animals. When they are threatened they will seek the safety (and the anonymity) of the herd. Thus the animal that is singled out by the pack will often attempt to evade pursuit by dashing back into the herd. The wolves may have invested twenty minutes in chasing the caribou. After such a long chase, the caribou should be beginning to tire and to slow, but once it’s back in the herd, the wolves must keep track of this individual or their quarry will have time to rest and all of their efforts will have been in vain. Since canines have less than perfect vision, and individual animals in a herd look very similar to one another, they must resort to their sense of smell to identify and continue the pursuit of this already weakened animal.”66

We employ the canines’ excellent ability to hunt by scent in police activities, such as hunting drugs and people. If we had the equipment of a hunter/carnivore, we wouldn’t need to train canines to do this job for us.

Some people have practiced the same type of persistence hunting used by canines, but humans do not attempt to pursue individual animals if they merge with a herd. Due to our upright stance and genital exposure making us easy targets for kicking and charging bulls, a stone age human on foot would not likely survive an encounter with a herd of large, fast moving mammals such as caribou without sustaining serious injury. In any case, a human would not likely succeed in following the specifically exhausted individual if it entered the herd, because neither our weak flicker resolution vision nor our

64 Coren, op.cit., 37.

65 Ibid., 51.

66 Ibid., 63.

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olfaction can adequately distinguish between two different but very quickly moving large mammals. I will have more to say about persistence hunting in the next chapter on locomotion.

A cat has about 40 times more olfactory receptors than a human, giving her a sense of smell about fourteen times stronger than had by humans. Cats rely primarily on the sense of smell to identify individuals or objects they encounter. Felines and canines have highly developed olfactory sensation to guide them in their search for prey, as this allows them to track prey even if the prey has camouflaged coloration or has hidden.

Taste

Fruits, vegetables, nuts, and seeds have a wide variety of flavors reflecting various stages of ripeness and spoilage as well as presence of toxins. In contrast, animal flesh consisting primarily of protein and fat varies little in composition and therefore flavor from species to species. Consider for example the subtle differences in flavors between the various fruits such as bananas, mangos, apples, peaches, grapes, and oranges, to name only a few, compared to the relative uniformity of beef, bison, pork, chicken, frog, and rabbit (assuming no seasonings or condiments). How many times have you heard someone say that some flesh food “tastes like chicken”?

To successfully navigate the large number and variety of flavors present in plant tissues, an animal primarily adapted to eating a variety of plants must have a relatively high taste sensitivity. In contrast, an animal that eats a flesh-based diet has little need for fine taste distinctions.

Taste sensitivity depends upon the number of taste buds in the tongue. Humans markedly differ from dogs (omnivorous) and cats (purely carnivorous) in this respect:

“Humans win the sensitivity contest for taste, with around 9,000 taste buds compared to a dog’s 1,700. Dogs have considerably more taste buds than cats, which average only about 470.”67

Thus, humans have more than five times as many taste buds than a dog, and more than nineteen times as many taste buds as a cat. Although about 80 percent of a wild canine’s diet will consist of flesh, s/he will also eat fruits when necessary or opportunity present. However, wild cats only eat flesh. This suggests a gradation in taste bud endowment, with pure carnivores having the fewest, omnivores having an intermediate number, and animals adapted to a plant-based diet having the largest number. It seems likely that our high endowment of taste buds indicates a physiology very highly adapted to a plant-based diet.

All great apes, including humans, have taste receptors uniquely adapted to detecting glucose, fructose and sucrose, carbohydrates found only in plants, particularly botanical fruits, tubers, and roots. These receptors emerged in the hominoid primate lineage more than thirty-five million years ago, and this ability may have played a critical role in support of brain evolution in primates including humans:

67 Coren, op.cit., 82.

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“Finally, we think that the appearance >35 million years ago (Gingerich, 1984, 1986), in the ancestral stock of the Old World simians, of an innovative sweetness receptor that was remarkably adapted to the specific detection of fructose and sucrose must have been a major transition in the catarrhine evolution, by improving food search efficiency and dietary choice of these primates for highly energetic nutriments, especially fruit, which could have favoured, as stated previously (Glaser et al., 1995a), their mental development, and, later, the emergence of humans.”68

Of interest, in the wild fruits consumed by extant primates most (50-65%) of the detectible sugar consists of glucose, while sucrose and fructose occur in small quantities. In contrast, humans have artificially selected modern fruits to have higher amounts of fructose and sucrose and lower levels of fiber. Wild fruits also have more protein and fiber than cultivated fruits.69

This suggests the possibility that our taste receptors, digestive physiology, and metabolism may be best adapted to foods that have high levels of glucose and low levels of sucrose and fructose. Among modern foods, dry, starchy fruits like chestnuts, legumes, and grains, and starchy roots and tubers (e.g., sweet potatoes and potatoes) have high amounts of glucose (in the form of starch), but low amounts of fructose and sucrose. Of these, legumes have the highest levels of protein and fiber. Of interest, Darmadi- Blackberry et al. studied the dietary predictors of longevity among long-lived elderly people from Japan, Sweden, Greece, and Australia, and found that only legume intake consistently predicted longevity.70

Investigators at the Monell Chemical Senses have reported that carnivores have a general loss of taste receptor function, particularly sweet-taste receptor function, compared to herbivorous species.71

“Scientists from the Monell Center report that seven of 12 related mammalian species have lost the sense of sweet taste. As each of the sweet-blind species eats only meat, the findings demonstrate that a liking for sweets is frequently lost during the evolution of diet specialization.”72

Humans not only have not lost the taste for sweets, but we have a strong drive for sweets, indicating an evolved dietary specialization in plant foods rich in sugars.

68 Nofre C, Tinti JM, and D. Glaser D. Evolution of the Sweetness Receptor in Primates. II. Gustatory Responses of Non- human Primates to Nine Compounds Known to be Sweet in Man. Chem. Senses 21: 747-762, 1996.

69 Milton K. Nutritional characteristics of wild primate foods. Nutrition 1999;15:488-498.

70 Darmadi-Blackberry I, Wahlqvist ML, Kouris-Blazos A, et al.. Legumes: the most important dietary predictor of survival in older people of different ethnicities. Asia Pac J Clin Nutr 2004;13(2):217-220.

71 Jiang P, Josue J, Li X, et al.. Major taste loss in carnivorous animals. PNAS USA 2012 Mar 27;109(13):4956-61.

72 Monell Chemical Senses Center (2012, March 12). Extensive taste loss found in mammals: Feeding preferences shaped by taste receptors. ScienceDaily. Retrieved September 16, 2013, from http://www.sciencedaily.com/releases/ 2012/03/120312152639.htm

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Animals well adapted to flesh-eating, such as cats and dogs have taste buds primarily attuned to the taste of flesh. Cats have taste receptors specifically adapted to detecting the flavors of amino acids, salts, sour, and bitter.73 Most essential amino acids have a bitter flavor, blood has a salty and bitter flavor, and spoiled flesh has sour and bitter flavors. The cat has a sense of taste specifically adapted to guide it to eat flesh74 (and to avoid spoiled flesh). While dogs can sense sweet, salty, sour, and bitter, and come from an omnivorous lineage, they too have their tastes tuned to flesh.

“Cats are true carnivores…their taste buds evolved to react to certain chemicals found in flesh (nucleotides) and the cat will tend to reject virtually anything that does not cause a response from these ‘meat detectors’…dogs also have some specific taste receptors that are tuned for meats, fats, and meat-related chemicals. Dogs will tend to seek out and clearly prefer the taste of things that contain meat or flavors extracted from meat.”75

While carnivores have the taste buds required to relish raw flesh, humans typically describe unseasoned raw flesh as virtually flavorless or blood-like.76

“If the high-quality protein that meat yields up to the successful hunter or scavenger were the ‘nutrient among nutrients’ in our evolutionary climb to modernity, one might reasonably assume that we should have developed some clear-cut, hardwired taste for it. Curious, then, that study after study characterizes uncooked fresh meat as essentially tasteless.”77

The characteristic flavors people usually attribute to flesh come from the many complex and toxic chemicals produced when people cook flesh, such as heterocyclic amines and lipid peroxides.

“Meat flavor is thermally derived, as uncooked meat has little or no aroma and only a bloodlike taste. During cooking, a complex series of thermally induced reactions between nonvolatile components of lean and fatty tissues occur, resulting in a large number of reaction products. The volatile compounds formed in these reactions are largely responsible for the characteristic flavors associated with cooked meat.”78

73 Li X, Li W, Wang H, et al.. Cats lack a sweet taste receptor. J Nutr. 2006 July; 136(7 Suppl): 1932S–1934S.

74 Callaway E. Carnivores have evolved to pick meat over sweets. Scientific American, March 12, 2012.

75 Coren, op.cit., 83.

76 Speth JD. The Paleoanthropology and Archaeology of Big-Game Hunting. Interdisciplinary Contributions to Archaeology, DOI 10.1007/978-1-4419-6733-6_8, Springer Science+Business Media, LLC 2010. 119-120.

77 Ibid.

78 Mottram DS, Koutsidis G, Oruna-Concha M, et al.. Analysis of Important Flavor Precursors in Meat. In: Deibler KD, Delwiche J, Handbook of Flavor Characterization: Sensory Analysis, Chemistry, and Physiology. Marcel Dekker, New York, NY, 463-472.

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Humans enjoy the umami flavor (provided by the sodium salt of the amino acid L-glutamate) often described as meaty. However, we can’t detect umami in raw animal flesh; it only occurs in cooked, salted, or fermented meats. Since no nonhuman animal prepares its flesh meals by cooking, salting, or fermenting, and no early human ancestor did so either, the ability to detect umami probably did not get naturally selected as an adaptation or guide to eating flesh. Speth comments:

“Thus, unless we allow early hominins the regular control of fire and some degree of ‘haute cuisine,’ it is doubtful that umami played much of a role in attracting our early ancestors, or chimpanzees, to meat.”79

Further, several experiments in humans and other species have shown that protein-deficient animals do not have a preference for the umami flavor; in fact, a preference for umami emerges only among individuals who have no signs of protein or amino acid deficiency.80 In contrast, people deficient in calories or carbohydrates will show a strong preference for the sweet flavor. Therefore, the ability to detect and enjoy the umami flavor probably does not serve as a biological mechanism for ensuring intake of any type of protein, let alone flesh.

Table 3.2: L-glutamate (Glutamic Acid), Percent of total protein Food Percent Food Percent Plant Foods Wheat (hard red winter) 32 Pumpkin seeds 20 Almonds 32 Cornmeal (wholegrain) 19 Sunflower seeds 27 Walnuts 19 Oats 24 Peanuts 19 Pecans 22 Potato (white) 17 Sesame 22 Lentils 15 Rice (brown) 20 Beans (black) 15 Animal products Milk (cow) 23 Salmon 15 Pork 15 Beef 14 Chicken 15 Egg 13 Source: USDA, www.cronometer.com

Moreover, the umami flavor arises from detection of free L-glutamate and nucleotides, which occur in many vegetables, including mushrooms, ripe tomatoes, spinach, seaweeds, celery, and Chinese cabbage. In fact, in comparison to animal products, grains, legumes, seeds, and nuts tend to have as much or more

79 Speth JD, op. cit., 121.

80 Ibid., 122.

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of their protein as free L-glutamate (Table 3.2). Therefore, our ability to detect and enjoy umami probably arose as a result of evolutionary natural selection of individuals who enjoyed eating plant foods.

We also differ from flesh-eating animals in our taste for salt. Animal flesh contains significantly more sodium than fruits and vegetables. Since all mammals require sodium, those that eat plant-based diets have a tendency to sodium deficiency, while those that eat flesh-rich diets have a tendency to sodium sufficiency or excess. Hence, among animals adapted to plant-based diets, natural selection will favor those individuals who have a strong detection of, attraction to, and sense of pleasure from the salty flavor, to prevent sodium deficiency. On the other hand, among animals evolving on flesh-based (therefore sodium-rich) diets, natural selection will favor individuals who are indifferent or averse to the salty flavor, to prevent sodium excess. Coren comments:

“Humans and many other mammals have a strong taste response to salt. We seek it out and like it on our food…Salt is needed to balance our diet and there is not much of it to be found in vegetables and grains [or any other botanical fruits]. Dogs, however, are primarily carnivores and, in the wild, most of their food is meat. Because of the high sodium content in meat, the wild ancestors of dogs already had a sufficient amount of salt in their diet and did not develop the highly tuned salt receptors and salt-craving of humans.”81

Similarly, whether sodium deficient or not, cats show no taste preference for sodium-rich foods.82 Cats or canines eating their natural diet (meat) have no need for sodium detection or preference because their diet inevitably provides sufficient sodium. Conversely, the fact that we have highly tuned salt receptors and salt cravings demonstrates that we have a physiology adapted to a diet that contained very little sodium and therefore, lots of plants and very little if any flesh.

Animals having a metabolism naturally selected for consumption of animal flesh also differ from humans in having specific taste receptors for water. According to Lindemann, although water does elicit various physicochemical responses in taste receptors, to humans water “has no reportable taste quality of its own.”83 In contrast, according to Coren:

“Dogs also have taste buds that are tuned for water, which is something they share with cats and other carnivores but not humans…This ability to taste water may have evolved as a way for the body to keep internal fluids in balance after the animal has eaten things that will either result in more urine being passed or will require more water to adequately process. One thing that will do this is meat, with its high sodium content, which makes this a particularly useful sense for

81 Coren, op. cit., 83.

82 Yu S and Morris JG. Sodium Requirement of Adult Cats for Maintenance Based on Plasma Aldosterone. J Nutr 1999 Feb 1;129(2):419-423.

83 Lindemann B. Taste Reception. Physiological Reviews 1996 Jul 1;76(3):719-66. 750.

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carnivores. It certainly appears that when these special water taste buds are active, dogs seem to get an extra pleasure out of drinking water and will drink copious amounts of it.”84

The high protein intake produced by eating flesh also increases water requirements to flush out ammonia and acids released when cells metabolize excess amino acids to obtain glucose.

Since fruits and vegetables have a very high water content (up to 99 percent) but low sodium and protein content, animals that live on diets based on fruits or vegetables do not typically need to drink much water to meet water requirements. Therefore, the fact that we lack taste buds specifically tuned to water supports the conclusion that our physiology evolved on a diet consisting of foods that supplied a surplus of water and low amounts of sodium and protein, i.e. a diet predominantly consisting of fresh fruits and vegetables.

In short, just as “carnivores have evolved to pick meat over sweets,”85 humans have evolved to pick sweets over meats.

Fat Taste

Some authors have suggested that humans have a unique taste for fat that arose as a result of some early human species living as hunters of fatty animal flesh.86 However, to support their hypothesis, these authors point to studies that show that rats and mice also prefer high-fat foods.87, 88 These rodents did not have ancestors who lived by hunting fatty animals, nor did they evolve unusually large brains. Wild animal flesh is not the only nor the richest source of fats; wild nuts (palm, etc.) can provide more fat and kcalories than wild game. Therefore, the preference for fat-rich food is not unique to carnivores, nor do we have reason to believe that it uniquely guides us to consumption of animal flesh.

Further, the ability to taste fats apparently varies significantly among humans.89 Given that humans do not have any dietary requirement for any fat uniquely supplied by animal flesh,90 we have no reason to believe that our taste for fat arose as a mechanism to ensure that we eat animal flesh. Nor do we have

84 Coren, op. cit., 86.

85 Callaway E, op. cit.

86 Leonard WR, Snodgrass JJ, Robertson ML. Evolutionary Perspectives on Fat Ingestion and Metabolism in Humans. In: Montmayeur JP, le Coutre J (eds.). Fat Detection: Taste, Texture, and Post Ingestive Effects. CRC Press, 2010. Chapter 1.

87 Slafani A. Psychobiology of food preferences. Int J Obes Relat Metab Disord 2001 Dec;25 Suppl 5:S13-6.

88 Besnard P, Gaillard D, Passilly-Degrace P, et al.. Fat and taste perception. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2010;5()32):1-9.

89 Mattes RD. Fat Taste in Humans: Is It a Primary? In: Montmayeur JP, le Coutre J (eds.). Fat Detection: Taste, Texture, and Post Ingestive Effects. CRC Press, 2010. Chapter 7.

90 Food and Nutrition Board, National Academy of Sciences. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients). National Academies Press, 2005. 422-541.

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any reason to believe that only our ancestors’ pursuit of animal flesh could have selected for this characteristic.

A taste for fats enables an organism to detect the presence of essential fatty acids as well as the relative energy density of food. Every mammal has a requirement for some dietary fats. Dietary fats also provide more energy per unit volume than carbohydrates or proteins. If the available foods tend to have a low content of essential fats or a low energy density, natural selection would favor animals that can detect and prefer dietary fats because these animals will have greater success in meeting their essential fatty acid and energy needs.

Recall that carnivores have the ability to taste water, whereas humans do not, apparently related to the fact that a meat-based diet lacks water and increases water requirements, whereas a fruit and vegetable rich diet has an abundance of water. If an organism evolved on a diet continuously rich in fat and energy, it would always have food rich in fat and under these circumstances natural selection would not favor individuals having a taste for fatter foods. Indeed, such an animal might continuously face the possibility of toxic overdose of fats (e.g., disabling obesity), and in this case, natural selection would likely favor those individuals who preferred the less fatty of available foods.

In contrast, if an animal has a habitual diet that has a relatively low fat content, the ability to detect fats and prefer to consume them when available becomes critical to reproductive success. (This would apply to primates, hominins, and rats.) In short, the fat taste and preference for fat consumption probably evolved as a mechanism to prevent fat deficiencies in animals that have adapted to a low-fat diet, just as the carnivores’ ability to taste water probably evolved as a mechanism to prevent dehydration. In short, possession of a marked taste and preference for fatty foods is probably an indication of basic adaptation to a low fat diet, not to a high fat diet.

The hypothesis that the human taste and preference for fat evolved as an adaptation to a low-fat, plant- based diet is compatible with the large body of evidence indicating that populations that sustain a high fat intake (beyond the essential) and particularly high animal flesh intake, such as the Mongolians and Argentinians, have an increased risk of obesity, diabetes, cardiovascular diseases, and cancers, in comparison to those that sustain a low intake of fats, mostly from plants, such as rural Chinese, and the Japanese of the early 20th century. It is also compatible with the large body of evidence that these diseases arise as adaptations to an overdose of fats (particularly saturated fats) and energy. In contrast, this data contradicts the hypothesis that humans are specifically adapted to consuming diets high in animal flesh or fats by their taste for fats.

In summary, the human ability to taste fat probably indicates that the habitual ancestral diet was low in fat, and that fat-rich foods were relatively scarce, making it advantageous for our ancestors to be able to clearly detect and prefer to consume whatever foods had the greatest fat content, which were relatively scarce and difficult to obtain. This adaptation has led us to consume a toxic amount of fats whenever we have had the opportunity to indulge it.

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The Taste For Liver

Evolutionary psychology would predict that almost all healthy individuals belonging to any animal species biologically adapted to eating animal flesh would experience pleasure when eating or contemplating eating animal guts, as we find in wild carnivores and omnivores. Distaste for a food deters an individual from eating that food, which contradicts the survival drive, so every individual of every species needs to have a natural enjoyment of the foods it naturally pursues in its native habitat. If most members of a species dislike a certain type of food, this strongly supports the hypothesis that the species lacks the naturally selected psychophysical equipment required to survive on that type of food (absent cultural conditioning, a.k.a. learning, or acquired taste).

An animal biologically adapted to flesh-eating enjoys sight of a dead, disemboweled, bleeding animal, and it relishes sticking its head into a bloody carcass to rip out organs, bowels containing half-digested food and feces, and pieces of flesh. Animals biologically adapted to eating meat enjoy the sight, smell, taste, and texture of of raw flesh including organs like liver without cooking or condiment. In contrast, an animal primarily adapted to eating fruits or vegetables naturally enjoys the sight, smell, and flavors of its favored fruits or vegetables and may feel aversion to eating raw flesh.

For example, dogs and cats thoroughly enjoy eating liver without cooking or condiment. In contrast, many people find just the thought of eating liver – particularly raw liver – repulsive. Among U.S. readers of AOL Food, a poll found that liver is the most hated food.91 A survey in Britain also found liver among the ten most hated foods, along with snails, tripe (intestines), oysters, squid, anchovies, cockles, kidneys, black (blood) pudding, and olives.92

Note that nine of ten of those most hated foods in Britain consist of flesh and blood. No evolved carnivore or omnivore would reject such foods as distasteful. The sole plant food on the list, olives, results from saline fermentation. The fact that despite cultural conditioning favoring flesh-eating, so many people feel revulsion at even the thought of eating liver and other viscera indicates that humans lack one of the most basic psychophysical adaptations characterizing flesh-eating animals.

These surveys provide further evidence that humans do not have the inborn aesthetic sense of an animal biologically adapted to eating flesh, and that any tolerance humans have for eating animal flesh comes not by nature but by culture, including disguising the flesh via the culinary arts (artifice), i.e. butchery, cooking and condiments.

Reader, test yourself. Which do you find most beautiful, fragrant, inviting, and appetizing, a bleeding corpse with its guts exposed (e.g., road kill) , or plant foods like a pile of fresh, ripe fruits, or a plate of rice and colorful vegetables? Would you prefer to decorate your home with flowers and fruits, or with

91 America’s Most Hated Foods. All About Food, 2008 June 24. http://about-food.livejournal.com/76665.html

92 London B. Fussy food nation: Tripe, black pudding, cockles and olives top poll of Britain’s most hated foods. Mail Online, 17 August 2012. www.dailymail.co.uk/femail/article-2189814/Tripe-black-pudding-cockles-olives-poll-Britains-hated- foods.html.

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carcasses and entrails? How many people do you know who decorate their homes with actual or virtual flowers and fruits, or with actual or virtual carcasses and entrails? If you met someone who decorated his home with carcasses and entrails, how would you respond?

Behavioral Adaptations

Humans commonly prepare meats with marinades or condiments derived from sweet-tasting plant foods, such as teriyaki sauce or ketchup, essentially aiming to make meat taste more like fruits (sweet and sour). In comparison, humans typically enjoy any plant-sourced food rich in sugars, such as fruit and tender vegetables, without having to add condiments; we don’t add blood to our fruits to make them palatable. Thus our taste receptors and preferences guide us toward the sweet flavor, absent from meats but characteristic of specific parts of plants. This suggests that the human taste sensation evolved to help us to identify and enjoy edible plants, primarily those richest in sugars, i.e. fruits and starches, not meat.

The differences between the sensory systems of humans and canines probably explains why humans have long employed dogs as assistants when hunting. Since the human sensory system does not have the abilities found in animals really adapted to hunting, humans can have much more success at hunting if they employ the services of a dog to detect the odor and motion of prey animals. But the very fact that a human needs a dog to be really successful at tracking game indicates that natural selection did not equip humans with the senses required to efficiently capture animals.

Additionally, humans have employed cats as assistants in hunting rodents. If humans had the equipment necessary to efficiently hunt rodents, why would they have cats do it? I suggest that humans have employed cats and dogs to scare rodents away from the foods that rodents and humans both enjoy, namely fruits, vegetables, and seeds.

Summary

In summary, humans have a sensory system naturally and specifically adapted to gathering fruits, vegetables, nuts, and seeds, and not well adapted to hunting animals. Note also that the human and the omnivore/carnivore systems don’t have much overlap, meaning that the canine or feline sensory capacities will not make dogs or cats very successful at gathering fruits and vegetables, and the unassisted human’s sensory system does not have the powers necessary for survival by hunting. In other words, canines (and felines) have a sensory system poorly adapted to living predominantly on fruits, while humans have a sensory system relatively poorly adapted to living by hunting.

Nevertheless, in certain habitats, such as within the arctic circle, given weapons, sophisticated hunting strategies, a sufficiently large supply of large enough and relatively unwary game, and canine assistance, humans have sensory capacities good enough to enable them to pursue a carnivorous lifestyle. Just as the panda survives on bamboo in spite of its maladaptation to the task (Chapter 2), not because of it, humans can pursue hunting in spite of their lack of specific sensory equipment for the task, not because of adaptation to it.

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Our sensory system provides evidence that human evolution was powered by plants.

SENSATION & NUTRITION – 49

4: Locomotion

Most animals, including humans, need to move in order to acquire foods. In the prehistoric setting in which human food acquisition adaptations evolved, the type of movement required for hunting animals differed markedly from the type of movement required for gathering plant foods. Simply, game animals move rapidly away from predators, and fight back against a predator’s capture, whereas plants remain stationary when approached by a gatherer.

This means that a mammal biologically well adapted to hunting (and hence eating animal flesh) will have a locomotive system capable of efficiently producing bursts of speed and strength greater than that of its prey, while a mammal well adapted to gathering plants (and hence a plant-based diet) will have a locomotive system highly adapted to standing still for efficient gathering of fruits, vegetables (leaves, roots, etc), or seeds.

Stance

Stance provides the basis of locomotion. Mammals exhibit three types of stance based on how their foot bones relate to the ground: plantigrade, digitigrade, and ungligrade.93 These basic stances evolved as adaptations to different feeding strategies.

In the plantigrade stance, the foot rests on the ground from heel to toe. Rodents, rabbits, and all primates, including humans, have a plantigrade stance. This stance has the shortest tarsal bones, and occurs in species that spend a lot of time standing stationary on two feet while holding something, often food, in the hands. It offers the most balance and support while also allowing for a grip for holding onto branches, foods, or tools. It does not allow the greatest speed or strength, but mammals with this stance can climb and jump well.

In the digitigrade stance, characteristic of predators, only the ball of the foot and the toes rest on the ground, and the distance from toes to heel is relatively longer than for the plantigrade stance. Canines and felines have a digitigrade stance.

The digitigrade stance includes maintenance of a bend at the knee, which engages the largest and most powerful muscles of the body, the quadriceps, on a continuous basis. This enables the digitigrade animal to powerfully pounce or sprint on a moment’s notice, as soon as the individual detects a potential prey. You can get an idea of the difficulty and energy cost of this stance by squatting down to produce a 90 to 100 degree angle at the knee while also standing on the balls of your feet and holding this position as long as possible. Because of the energy cost of this stance, cats and dogs tend to avoid standing for very long and take every opportunity to sit or lie down. Animals with the digitigrade stance are well-adapted to moving rapidly and powerfully to capture prey, but maladapted to standing still for long periods of

93 Mammalian Stances: Plantigrade, Digitigrade, and Ungligrade. http://campus.murraystate.edu/academic/faculty/tderting/ CVA_atlases/mammalian_stances/CoyoteBiomechanics.html.

time. This makes them adapted to acquiring moving foods (animals) but not to acquiring large amounts of stationary foods (plant foods).

The digitigrade stance offers the optimum limb lengths and orientations for production of the combined speed and strength required to capture and butcher prey. This stance allows a cheetah to produce top speeds of 60 miles per hour, but only in short bursts. Humans rarely adopt a digitigrade stance – on the balls of the feet, with knees bent at about 90 degrees – such as when in the starting blocks for a sprint.

In mammals with the ungligrade stance, a hoof replaces the toes, and only the hoof rests on the ground. This stance produces relatively the longest distance from toe (hoof) to heel. This gives animals with a ungligrade stance more efficient transmission of force to the ground than the digitigrade stance, with the result that animals with the ungligrade stance have less speed and power but much greater endurance than those with the digitigrade stance.

Mammals using the ungligrade stance spend a lot of time standing to graze on foods. To stand for long periods of time, they extend their knees to an angle close to 180 degrees, which greatly reduces the load upon and metabolic work of the thigh muscles, and increases the energy efficiency of standing. Since the food of ungulates (typically grass) stands still, natural selection favored those with a neuromusculoskeletal system well adapted to standing still.

Human Stance

Humans can extend their knees to 180 degrees, which minimizes standing energy expenditure, and our hip joint allows a pendulum-like action that utilizes momentum to facilitate locomotion. This greatly improves the efficiency of standing still and walking while keeping the arms free for gathering and holding food. Humans do not spontaneously assume a bent-legged stance suitable for sprinting, a key ability in carnivores.

When we compare the foot print relative to total limb length of the squirrel (plantigrade), coyote (digitigrade), and deer (ungligrade), we find that in the squirrel, about 31 percent of the lower limb makes contact with the ground, in the coyote, 14 percent, and in the deer, only 3 percent.94

Humans have limb lengths similar to the squirrel. For example, in my case, my foot measures about 12 inches long, and I measure about 32 inches from hip to foot, so my foot length is about 28 percent of the total length of my lower limbs (measured from hips to toes).

These facts suggest that humans have a physique primarily adapted to gathering plants, not chasing animals.

94 Mammalian stances: bone length ratios. http://campus.murraystate.edu/academic/faculty/tderting/CVA_atlases/ mammalian_stances/BoneLengthRatios.html.

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Bipedalism Not Optimal for Hunting

The human stance appears particularly poorly adapted to hunting on an open savannah as proposed in some stories about human evolution. It seems clear that human survival depended upon maintaining an upright stance on two feet, but this natural human stance makes it possible for any potential prey animal to detect the advance of a human hunter by both odor and sight, particularly since the presumably dark skin and hair color of our African ancestors stands out against a background of yellow and green grasses. All large animals biologically adapted to hunting on the African savannah have a more camouflaged yellow-based coloration (e.g. lions and tigers) and a stance low to the ground, enabling them to easily conceal themselves in the tall grasses while stalking prey. Regardless of size or geographic location, natural selection has equipped predators with bodies and behavior conducive to hug-the-ground stealth. Crawford and Marsh commented on this:

“The idea of an upright primate scoring by being able to peer over the tops of the grasses is an appealing one – to anyone who has no experience of hunting. In reality the main difficulty facing any hunter is not spotting his prey but preventing his prey from spotting him. A polar bear, for all its white camouflage, will slip into the icy water and move, virtually submerged, towards the seal lying on the edge of the ice. If you watch a cat stalk a bird, it squeezes its body as close as possible to the ground: it seems to flow forward in controlled, silent motion with its eyes fixed unwaveringly on the position of its prey. The big cats do the same with frightening ease....

“A hunter stalking antelopes or wild pigs with a modern rifle will do his best to emulate the Tasmanian and the cat. Creeping about the savannah on your stomach is extremely uncomfortable but unless you want your target to spot you first it is what you had better do, even if it means that for much of the time you cannot see the animal you are stalking. Beginners who attempt this method, or still worse try to move crouching on all fours, often betray their presence by their give-away rear end protruding above the grass. Anyone trying it will soon be left in no doubt that the human anatomy, with its upright stance, is not designed for stalking prey.”95

Bipedalism Originated In Forest-Dwelling Frugivores

The savannah hunting story of human origins has for more than 150 years rested on the following syllogism: Humans are bipedal, but other great apes are quadrupedal. Most modern humans do not live in forests, but most other primates do live in forests. Therefore, human bipedalism represents an adaptation to living on open plains, and running after animals on the open plains “made us human.” Verhaegen et al. have made an important comment on this syllogism:

“But while this might seem an obvious conclusion, it is in fact a logical fallacy of the type: post hoc, ergo propter hoc (‘after that, therefore because of that’), and our comparative research suggests to the contrary that there is no evidence that the two (leaving the trees and becoming bipedal) are causally related: in fact, ground-dwelling and savannah primates such as patas

95 Crawford M and Marsh D. Nutrition and Evolution. Keats, New Canaan, CT, 1995. 156-157.

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monkeys and hamadryas baboons are more quadrupedal than forest and arboreal primates such as indris, tarsiers, proboscis monkeys and gibbons.” 96

According to the savannah story, climatic changes caused forests to shrink and arid open plains to expand, more or less “forcing” our arboreal ancestors to leave the forests and occupy grasslands, which naturally selected for bipedalism.

“Current interpretations of the savannah hypothesis state that the evolution of African mammalian fauna, including early hominids, was primarily attributable to the step-like development of cooler and drier and more open conditions which occurred since the late Miocene.”97

However, according to deMenocal, “Current evidence indicates that bipedality was established millions of years before the widespread expansion of savannah grasslands.”98

“Bipedality is a fundamental characteristic of the human family (Hominidae) and early bipedality is evident in the late Miocene (ca. 5.8 Ma) hominid Orrorin tugensis [12] and in earliest Pliocene hominid specimens dating to 4.4–4.2 Ma [108–112]. The hominid footprint trackways of three individuals preserved in a volcanic ash bed at Laetoli, northern Tanzania (Fig. 1), provide striking confirmation that obligate bipedality was established by at least 3.6 Ma [13], well before the expansion of savannah grasslands.”99

When Raynor et al. reconstructed the habitat of bipedal Australopithecus africanus, they found evidence suggesting that “sub-tropical forest was the hominins’ preferred habitat rather than grassland or bushveld, and the adaptations of these animals were therefore fitted to a forest habitat.”100 In other words, it appears that natural selection favored bipedalism for survival in the forest, not as a mode of locomotion for hunting animals. Possibly, bipedalism allowed early hominins to cover more forest territory each day, in search of ripe fruits, at a lower energy cost than quadrupedalism, while at the same time making it possible to harvest low-hanging fruits from the ground, possibly using the hands to hold long sticks and dislodge fruits from the canopy, as modern fruit-pickers do, thereby saving the great energy costs of tree-climbing. In addition, since many plant foods–particularly various fruits– have seasonal or regional availability, natural selection would have favored bipedal locomotion in a hominin

96 Verhaegen M, Munro S, Vaeechoutte M, et al.. The Original Econiche of the Genus Homo: Open Plain or Waterside? In: Ecology Research Progress, ed by Sebastian I Munoz. Chapter 6. Nova Science Publishers, Inc, 2007. 4.

97 deMenocal PB. African climate change and faunal evolution during the Pliocene–Pleistocene. Earth and Planetary Science Letters 2004; 220:3-24.

98 Ibid.

99 Ibid.

100 Raynor RJ, Moon BP, Masters JC. The Makapansgat australopithecine environment. Journal of Human Evolution 1993 March; 24(3):219-231. Abstract.

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who engaged in relatively long-distance seasonal north-south migration as a way to maintain year-round access to required fruits and vegetables.

Moreover, deMenocal also states that “the paleoclimatic record does not support unidirectional shifts to permanently drier conditions” during the period of putative early hominin evolution.101 Finally, deMenocal notes that “Pliocene–Pleistocene shifts in African climate, vegetation, and faunal assemblages thus appear to be roughly contemporary, although detailed comparisons are hampered by sampling gaps, dating uncertainties, and preservational biases in the fossil record.”102

In regard to preservational biases, bones deposited on a dry savannah will have a far greater chance of surviving millenia, in comparison to bones left in a rainforest where moisture, microbes, and mycelia degrade all organic matter in relatively short order. This bias receives reinforcement from the fact that we find it much easier to dig deeply in open grasslands lacking the dense root infiltration found in African rainforests.

Locomotion, Speed, and Endurance

Whereas all non-human cursorial animals have inborn speed or endurance, humans achieve extraordinary sprinting or endurance running only with specific genetics and extensive specialized training. In addition, many prey animals have a combination of speed and endurance that humans can’t match, regardless of training.

A pronghorn antelope can achieve a top speed of 55 mph over short distances, and can maintain 30 mph for up to 20 miles; an untrained horse can achieve a top speed of 50 mph over short distances and maintain 11 mph for up to 20 miles; an untrained camel can achieve a top speed of 40 mph and can maintain an average of 25 mph for 20 miles; and an ostrich can achieve a top speed of 50 mph and maintain 30 mph for 20 miles.103

Evolved predators have the ability to move more quickly than their prey; and to avoid excessive energy expenditure that increases food requirements, a predator must have the ability to reliably achieve the required speed without spending a lot of energy in training for its hunting. A cheetah spends no energy in training yet can achieve top speeds of 60-70 mph over short distances, sufficient to enable it to succeed at capturing antelopes and other fast prey animals frequently enough to maintain body mass and reproductive capacity.

In contrast, no untrained human can achieve a speed sufficient to capture an antelope, horse, or deer over a short distance. Although genetically gifted, highly trained human sprinters can attain speeds of nearly

101 deMenocal, op. cit.

102 Ibid.

103 Resnick B. The Animal Kingdom’s Top Marathoners. Popular Mechanics Online. http://www.popularmechanics.com/ outdoors/sports/physics/animal-kingdom-top-marathon-runners-pronghorn-antelope#slide-1.

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25 mph in the 100 meter sprint, no human can maintain this speed for a mile or more, regardless of training. And, although highly trained distance runners can run 20 miles at a speed of 12-13 mph, no untrained human can achieve this level of performance, which falls far short of the abilities of prey species, as illustrated above.

This strongly suggests that human ancestors did not have a lifestyle exerting a sustained natural selection pressure for inborn speed and endurance as a requisite for successful food acquisition. It supports the hypothesis that human evolution was primarily powered by plants.

Energy Cost of Locomotion

Compared to non-human quadrupeds, humans also have a relatively low energy cost of walking but relatively high energy cost of running.104 For humans, the cost of locomotion “is minimized at intermediate walking speeds of 4.5–5.4 kmh−1 (1.25–1.5 ms−1) and rises rapidly as speed increases above or decreases below this optimum,” and “humans are 60–70% more economical when they walk than when they run.”105 This indicates that natural selection favored a human locomotive system primarily adapted to walking in preference to running. Walking serves us well as a way to gather plant foods but not as a way to hunt animal prey.

Moreover, human running performance depends upon sufficient glycogen stores derived from dietary carbohydrate. A classic study found that athletes fed a carbohydrate-free diet (such as consumed by carnivores) had a maximum endurance time of 57 minutes; when fed a diet supplying 55 percent of calories from carbohydrates (sugars) they had a maximum endurance time of 114 minutes; and when they ate a diet providing 83 percent of calories from carbohydrate, they had a maximum endurance time of 167 minutes.106

Thus, to support regular high-performance endurance running, humans need to have plenty of reliable, carbohydrate-rich foods. Animal flesh provides virtually no carbohydrate. The idea that humans evolved their carbohydrate-dependent ability to run long distances by route of chasing animal prey and subsisting on a low carbohydrate animal-based diet lacks immediate plausibility.

Persistence Hunting

Some authors have suggested that, starting two million years ago, early humans regularly hunted larger, faster animals by running them to exhaustion over several hours and a distance of 16 to 22 miles in a technique called “persistence hunting.” The idea arises from the fact that modern hunters of the Kalahari desert have practiced this technique.

104 Steudel-Numbers KL. The energetic cost of locomotion: humans and primates compared to generalized endotherms. Journal of Human Evolution 2003;44: 255–262.

105 Carrier DR, Anders C, Schilling N. The musculoskeletal system of humans is not tuned to maximize the economy of locomotion. Proc Natl Acad Sci U S A. 2011 November 15; 108(46): 18631–18636.

106 Whitney EN and Rolfes SR. Understanding Nutrition, 10th edition. Thompson Wadsworth, 2005. 483.

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If this was an energetically viable method of living by hunting, it seems likely that at least one other flesh-eating animal would have adapted to this method. However, no non-human living large flesh- eating animal relies primarily on this technique to acquire food. The reason probably lies in the fact that it would involve expending far more energy in the course of hunting than the hunter could recoup from the occasional success.

No flesh-eating animal succeeds in capturing every prey animal it pursues. For example, tigers have ten to twenty percent success rate; lions about twenty percent; wolves about ten to fifty percent (depending on season); and cheetahs about fifty percent (average).107 If any flesh-eating animal used the persistence hunting technique, it would necessarily spend an enormous amount of energy in several failed hunts for every successful hunt. Without a plant-based fallback diet, this would mean that a successful hunt would have to yield enough food energy to cover the costs of the successful hunt and all of the failed hunts.

Among the Kalahari San (Ju/’hoansi ), one of the African tribes known to do persistence hunting, Richard Lee found a hunting success rate of about twenty-three percent.108 Moreover, they sometimes fail to obtain prey for several weeks, and they have the lowest success rate when pursuing ungulates, the targets of persistence hunting:

“…in 1968, John Yellen observed the Ju/’hoansi for a period of 80 days. Unlike Lee’s earlier work, Yellen’s study spanned part of the wet season as well as a portion of the subsequent dry season. During this period, men made no attempt to hunt on 14 days and failed to procure anything on an additional 25 days, indicating that on nearly 50% of the days the hunters made no successful kills. Moreover, most of what they caught were small animals, especially porcupines and springhare, as well as a number of birds (Hitchcock et al. 1996:175). If one considers only the ungulates, their success rate was much lower.”109

African Hadza hunters have no greater success:

“Observations over more than 2000 hunter-days show an overall average acquisition rate of only one large animal every 30 hunter-days. Periods of more than ten days in which no hunter in a local cohort of 5-6 took a large carcass are not uncommon in this sample. Scavenging alone produced about 20% of this total—on average, one animal every 140 hunter-days, just over one

107 For exemplary data, see: Sunquist M, Sunquist F. Wild Cats of the World. University of Chicago Press, 2002.. 26, 292; and Mills S. Tiger. Firefly Books, 2004. 14.

108 Speth JD, op. cit., 89.

109 Ibid.

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per cohort-month. During 1985-88, several periods longer than a month passed during which our co-resident study population (30-50 people) had no scavenging opportunities of any kind.”110

Given that adult ungulate animals can run dozens of miles at speeds greater than humans before reaching exhaustion, a team of humans who depended upon persistence hunting for survival (i.e. a principal source of energy) might run several marathons in a week or month before successfully chasing one victim to exhaustion.

Each 16 to 20 mile persistence hunt would cost 1600 to 2000 kcalories above body maintenance requirements per individual involved. If five men composed each team, and the average success rate was one in four hunts, the team(s) would spend a total of 32,000 to 40,000 kcalories in hunting every week. If highly dependent on hunting for sustenance, these men would have to run most of those marathons in a fasted or semi-fasted state, an unrealistic proposal. Humans do not run very quickly or for long distances when they are in negative energy balance and ketosis. The idea that some human ancestors ran 64 to 80 miles per week, primarily to obtain a meal that won’t even supply the nutrient most depleted by long-distance running, without falling back on carbohydrate-rich plant foods, strains credulity.

In fact, from modern sports nutrition science, we know that to perform such a feat more than once weekly, a man would need to follow a high carbohydrate diet to replenish glycogen stores. Since “Approximately 50%-60% of energy during 1-4 h of continuous exercise at 70% of maximal oxygen capacity is derived from carbohydrates,” the American College of Sports Medicine has stated:

“Carbohydrate recommendations for athletes range from 6 to 10 g·kg-1 body weight·d-1 (2.7-4.5 g·lb-1 body weight·d-1). Carbohydrates maintain blood glucose levels during exercise and replace muscle glycogen. The amount required depends on the athlete's total daily energy expenditure, type of sport, sex, and environmental conditions.” 111

To maintain endurance performance over time, a 70 kg male running 40 or more miles per week would need a diet supplying 420 to 700 grams of carbohydrate daily, the equivalent of about 16 to 28 medium sweet potatoes or bananas. This carbohydrate-dependence would not have survived natural selection if human ancestors had depended upon virtually carbohydrate-free animal flesh for survival.

Thus, people probably would have done this type of hunting only if they were habitually well fed on a high carbohydrate, plant-based diet. In fact, field studies show that the Kalahari San spend the most time hunting and eat the most flesh when they have more than adequate supplies of high carbohydrate plant foods and they spend the least time hunting and eat the least flesh in seasons when they have the

110 Lupo KD, O’Connell JF. Cut and Tooth Mark Distributions on Large Animal Bones: Ethnoarchaeological Data from the Hadza and Their Implications For Current Ideas About Early Human Carnivory. J Archaeological Science 2002; 29: 85-109.

111 American Dietetic Association, Dietitians of Canada, American College of Sports Medicine, et al.. American College of Sports Medicine position stand: Nutrition and athletic performance. Med Sci Sports Exerc 2009 Mar;41(3): 709-31.

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least supplies of plant foods.112 This suggests that they do not hunt for sustenance but for sport or other reasons, and supports the hypothesis that the evolution of human running/hunting abilities was powered by cooked starchy plant foods such as tubers and seeds.

Moreover, humans can only engage in very long distance running in warm climates (such as equatorial Africa) if constantly supplied with water. The ACSM has stated:

“Dehydration (water deficit in excess of 2-3% body mass) decreases exercise performance; thus, adequate fluid intake before, during, and after exercise is important for health and optimal performance. The goal of drinking is to prevent dehydration from occurring during exercise and individuals should not drink in excess of sweating rate. After exercise, approximately 16-24 oz (450-675 mL) of fluid for every pound (0.5 kg) of body weight lost during exercise.”113

Temperatures in the regions of Africa where humans appear to have originated typically reach near 100 degrees at midday, when, according to the persistence hunting hypothesis, humans would pursue prey until the animal suffered hyperthermia.

However, even if supplied with water, modern humans frequently suffer dehydration and hyperthermia when running long distances in hot climates. At the 2012 Boston Marathon, temperatures reached into the upper 80s (℉) and more than 2,100 runners suffered from dehydration and heat exhaustion, despite the presence of numerous drinking and water spray stations along the route.114 Ancient African hunters would not have run a planned course with water stations to keep them from dehydration, so persistence hunting would have presented a real danger of death. If ancient humans depended on persistence hunting for survival, this activity would have exerted a strong natural selection favoring the reproduction of humans who could conserve water (rather than rapidly waste it in sweating) and modern humans would have a high resistance to dehydration and hyperthermia when running in hot temperatures. Crawford and Marsh commented on this:

“In savannah conditions man too is helplessly dependent on a supply of water, though he only needs to drink it....On another expedition in Uganda with Neil Casperd we measured the loss of water from our bodies when we were on a foot safari in Tonia-Kaiso. We discovered that between 10 a.m. and 4 p.m. we were losing it at the rate of 1.6 litres an hour, or over two gallons in six hours. Our African colleagues were losing water at the same rate...

“Animals in an arid environment cannot possibly afford to treat a very scarce resource with extravagance. If man is a savannah species he is the only one that rigidly controls its body temperature and uses a copious loss of water through the skin to do so.”115

112 Speth JD, op. cit., 97.

113 American Dietetic Association, et al., op. cit..

114 Johnson CY, Sampson ZT. Marathon Heat Proves A Heartbreaker. Boston Globe, Boston.com, April 17, 2012.

115 Crawford M and Marsh D. Nutrition and Evolution. Keats, New Canaan, CT, 1995. 167.

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The fact that more than 2000 individuals (about ten percent of the entrants) suffered from dehydration and heat exhaustion at the 2012 Boston Marathon despite temperatures ten to twenty degrees lower than expected on an African savannah suggests that early human ancestors probably never depended on persistence hunting for their survival, and further that those modern tribes who practice persistence hunting have probably done it for reasons other than survival, such as status, social benefits (especially sex), sport, or test of manhood.

Additionally, unless supplied with sugar during the event, at the end of a long distance run, particularly in a hot climate, humans experience exhaustion and weakness, particularly if they deplete their glycogen stores. For this reason, the ACSM recommends:

“During exercise, primary goals for nutrient consumption are to replace fluid losses and provide carbohydrates (approximately 30-60 g·h-1) for maintenance of blood glucose levels. These nutrition guidelines are especially important for endurance events lasting longer than an hour when the athlete has not consumed adequate food or fluid before exercise or when the athlete is exercising in an extreme environment (heat, cold, or high altitude).”116

Glycogen depletion most severely impairs human ability to sprint or engage in high intensity activity against resistance, as would be required to either escape or fight a predator, because the human energy system depends on glucose for generation of peak high intensity efforts. Thus, unless supplied with sugar during their persistence hunt, glycogen depletion would impair a hunter’s ability to protect the carcass from other predators and carry it back to camp, or to sprint to escape predators.

Observers report that the San lose something like 50 percent of the animals they track to other predators regardless of hunting strategy, due to the number of times the animal evades the humans and the frequency with which other predators reach the fatigued or injured prey before the humans.117 In this light, imagine several men investing 10,000 kcal in pursuit of an animal over a few hours, only to have the animal escape or captured by a large cat or hyena, leaving the humans nutritionally drained, dehydrated, unfed, and unable to sprint or fight effectively, making them prime targets for another easy meal for the large social carnivores of the stone age.

“These same early humans also had to contend with a larger array of large-bodied carnivores, some of which may have been highly social (e.g. Turner, 1990; van Valkenburgh, 2001), factors that should have shifted the balance further in favour of the carnivores, either in defending the prey they themselves had killed, or in appropriating it from others, including early humans.”118

116 American Dietetic Association, Dietitians of Canada, American College of Sports Medicine, et al., op. cit..

117 Speth JD, op. cit., 94.

118 Lupo KD, O’Connell JF, op. cit..

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Frequent repetition of such scenarios would have exerted a strong natural selective pressure favoring any mutants who had the ability to recover rapidly from sustained exertion without consumption of carbohydrates and also fight off ancient large-bodied carnivores (e.g. social saber-tooth cats) with bare hands or sticks and stones (since those early human species did not have any other projectile weapons).

Also, modern humans doing long distance runs in specialized foot gear on paved surfaces experience a very high rate of joint injuries and immune suppression. A review of reports of the incidence of lower extremity injuries in long distance runners found that the reported incidence ranged from 19.4% to 79.3%.119 Ancient runners would have run barefoot on uneven, rock-strewn surfaces, greatly increasing the risk of injury. If our ancestors had depended upon persistence hunting for survival, the activity would have imposed a natural selection for people who could run long distances regularly without incurring injuries that would keep them from repeatedly running.

Finally, running long distances suppresses the activities of the immune system for up to 72 hours after the effort, with the effect greatest when runners do not ingest carbohydrate before, during, and after the effort.120 In modern, well-fed athletes, this immunosuppression results in a significantly increased risk of upper respiratory infections. If humans had depended upon persistence hunting for survival, we would expect that ingestion of animal protein or fat after heavy endurance activity would reduce this immune suppression. Scientists have tested the ability of several nutritional interventions to reduce the immunosuppressive effect of endurance exercise, including zinc and the amino acid glutamine, two nutrients supplied by meat, and only carbohydrate supplementation before, during, and after the activity has shown any significant beneficial effect.121 This suggests that human ancestors did not undergo a natural selection process favoring the reproduction of individuals who could quickly recover from persistence hunting by eating the flesh resulting from such hunting. On the other hand, this supports the hypothesis that early humans developed their endurance running/persistence hunting abilities while dependent for survival on a carbohydrate-rich plant-based diet.

Phinney reported that humans can sustain submaximal endurance running while eating a very low carbohydrate, ketogenic meat-based diet, but only if limiting protein intake in favor of fat and using supplements providing potassium (as bicarbonate) that fruits and vegetables would supply, and even then they lost sprinting ability which a persistence hunter might require.122 Phinney modeled his diet on that of the Arctic-dwelling Inuit who hunt animals having a very high body fat (e.g. whales, seals, etc.) and cook in brackish partially desalinated sea water. Early human species located in Africa would not have had potassium bicarbonate supplements, brackish sea water, knowledge of the optimal protein intake (according to Phinney, 1.2 g/kg per day or 15-25% of energy) and how to achieve it, nor consistent access to fat-laden game necessary to sustain an 75-85% fat diet to prevent protein overdose.

119 Van Gent RN, Siem D, van Middlekoop M, et al.. Incidence and determinants of lower extremity running injuries in long distance runners: a systematic review. Br J Sports Med 2007; 41: 469-480. doi:10.1136/bjsm.2006.033548

120 Nieman DC. Immune response to heavy exertion. Journal of Applied Physiology May 1, 1997; 82(5): 1385-1394.

121 Ibid.

122 Phinney SD. Ketogenic diets and physical performance. Nutrition and Metabolism 2004; 1:2.

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“But as already alluded to, most African ungulates have low average levels of body fat by comparison to levels found in larger mammals elsewhere in the world, including the Neotropics (e.g., Ledger 1968; Hill et al. 1984:111). Norman Smith (1970:127) notes that ‘…many East African ungulates…have very little, if any, fat under the skin.’ Not only isn’t there much fat on African game animals in prime condition, at any given point during the year many individuals may be nutritionally stressed and partially to severely fat depleted (e.g., males during the rut, females carrying a full-term fetus or nursing, older animals whose teeth are wearing out, injured or sick animals that have difficulty obtaining sufficient food, very young individuals, animals under drought conditions, and so forth). Thus, on any chunk of African real estate, the number of animals that are in reasonably good condition is likely to be much smaller than the total number of animals in the population.”123

Moreover, the American College of Sports Medicine explicitly advises athletes to avoid high fat intakes: “Fat intake should range from 20% to 35% of total energy intake....High-fat diets are not recommended for athletes.”124

As already noted, humans already have an extraordinary water requirement in dry climates due to our use of evaporative cooling by sweating. The high animal protein diet Phinney recommends increases human requirements for water for diluting and excreting the urea and acids produced from deamination of excess amino acids, thereby increasing the risk of fatal dehydration in arid climates. If human ancestors had any significant dependence upon hunting and eating flesh in the African homeland, natural selection would have favored the reproduction of any individuals who depended less upon evaporative cooling so as to conserve water for waste elimination. These same conditions would have favored individuals who had a strong taste for water. Modern humans don’t have these characteristics, providing more evidence against the hypothesis that meat-eating played an important role in natural selection of modern human physiology.

Since flesh lacks carbohydrate and has a relatively low potassium and water content, but has a high protein and sodium content, both of which increase water requirements, it provides poor nutritional support for performance and recovery from the long distance running involved in persistence hunting. If natural selection had favored humans adapted to dependence on persistence hunting and meat-eating for survival, modern science would find that modern humans recover most quickly from strenuous endurance activity when fed carbohydrate-free, high fat or high protein animal flesh, the post-event meal provided by persistence hunting. However, the ACSM has stated:

“After exercise, dietary goals are to provide adequate fluids, electrolytes, energy, and carbohydrates to replace muscle glycogen and ensure rapid recovery. A carbohydrate intake of

123 Speth JD, op. cit., 88.

124 American Dietetic Association, Dietitians of Canada, American College of Sports Medicine, et al., op. cit..

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approximately 1.0-1.5 g·kg-1 body weight (0.5-0.7 g·lb-1) during the first 30 min and again every 2 h for 4-6 h will be adequate to replace glycogen stores.”125

Since animal flesh does not provide the large dose of carbohydrate a human requires to replace muscle glycogen and ensure rapid recovery from strenuous exertion, we have more evidence that humans have no significant adaptation to persistence hunting as a means of survival.

Human physiology suggests that only people well supplied with high carbohydrate plant foods as well as abundant water could nutritionally afford to engage in persistence hunting and that foragers practiced persistence hunting primarily for cultural purposes, for example, as a sort of sporting event that would confer status and sexual opportunities on the winner(s) who brought home the buck.126 This gains support from the fact that the two cultures recently observed to practice persistence hunting––the Kalahari San and the Central American Tarahumaras––eat diets consisting primarily of plants, the fact that the Kalahari San spend the most time hunting and eat the most flesh when they have more than adequate supplies of plant foods and they spend the least time hunting and eat the least flesh in seasons when they have the least supplies of plant foods,127 and the fact that the San use suboptimal weapons for hunting:

“[The Bushman bow] was not a means of acquiring as much meat as possible in as little time as possible, as that would have led them to adopt the power bow. What they wanted was something which would require great skill, endurance and patience when used for hunting, and which would make the hunt as long as possible. These requirements have all the hallmarks of a recreation activity, indulged in mainly for non-economic benefits such as personal gratification and social prestige.”128

Like the Bushman bow, persistence hunting reduces efficiency, prolongs the hunt and requires endurance, patience, and skill. In short, it has the aforementioned hallmarks of a recreation activity, indulged in primarily for sport and the social benefits that accrue to winners of sporting events.

The persistence hunting scenario depicts prehistoric human ancestors expending many hours and lots of glucose running after prey, in order to obtain animal flesh that did not supply the carbohydrate, water, or potassium necessary to support or recover from the hunt. It simply does not make biological sense, so begs a non-biological explanation.

125 Ibid.

126 Speth JD, op. cit., 97.

127 Ibid.

128 Noli, H. D., 1992. Archery in Southern Africa: The Evidence from the Past. Unpublished PhD Dissertation, Department of Archaeology, University of Cape Town, Rondebosch, South Africa. As quoted by Speth JD, op.cit., 95.

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While we do have what appear to be endurance running adaptations,129 we can explain these in part as follows: Among human ancestors, the males who most frequently brought home meat via persistence hunting had high social status and the most sexual opportunities, even though the hunting itself was an insufficient means of supporting a family. To spread his genes, the hunter did not have to bring home enough meat to feed a family, he only needed to bring home enough to impress others with his virility, i.e. an amount similar to or, preferably, somewhat greater than that brought home by other males in his tribe. He was not competing with other carnivores, he was competing with other males in his tribe, all of whom had the same inborn handicaps for hunting that he had. By this hypothesis, our ability to hunt did not evolve by natural selection, but by sexual selection.

Certainly, humans can also gather slow moving animals (say, insects, turtles, etc.), but the high protein, low carbohydrate, low fat nature of small animal flesh makes it very difficult for a human to obtain adequate energy by eating the flesh of these animals. Humans can only benefit nutritionally from hunting small game if they have a largely adequate intake of a plant-based diet.

Table 4.1: Locomotive System Comparison Squirrel Dog (African Wild) Pronghorn Antelope Human Stance Plantigrade Digitigrade Ungligrade Plantigrade Top speed 12 mph 45 mph 55 mph 25 mph1 Average speed for one Unknown 15 mph 30 mph for up to 20 15 mph1 mile or more miles Maximum knee angle <180 <180 180 180 Standing energy Intermediate High Low Very low expenditure Primary foods Plants Animals Plants Plants 1. Only attained by genetically gifted or highly trained athletes. Untrained humans do not achieve those speeds or distances.

The human locomotive system has features that improve the ability to stand and walk slowly for a long time on two feet, which features improve the efficiency of collecting fruits, roots, and leaves from stationary plants. The human locomotive system does not have features that would indicate natural selection for the ability to chase fast-moving prey such as deer, cattle, and bison as a primary means of survival.

Behavioral and Technological Circumvention of Our Locomotive Limits

Since we don’t have the natural speed or endurance required to succeed at capturing large prey animals, we have adopted a number of behavioral and technological approaches to overcoming our inability to outrun prey animals. These include using dogs (top speed of 40-45 mph) and predatory birds (e.g. falcons) to chase down prey; and implementing projectiles that can move faster than a human can on

129 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 9.

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foot, such as slingshots (95 mph), bow and arrow (an 80 lb. bow projects arrows at 184 mph), and most recently, firearms (900-2000 mph); and using traps of various sorts.

Of interest in this context, Williams reported that Native Americans attempting to live by hunting buffalo were “less well nourished” prior to introduction of horses and firearms, despite having weapons far superior to early human species:

“...it should be borne in mind, that in their primitive condition these savages had no horses and no firearms; consequently it was no easy matter for them to kill the fleet buffaloes, on which they mainly depended for subsistence; hence, in their primitive condition, they were generally less well nourished than when, after contact with whites, they had, by the acquirement of horses and firearms, become assured of a constant supply of their favourite food.”130

The fact that humans must employ true carnivores and tools to really succeed at hunting affirms that the human does not have a physique biologically adapted to hunting, just as our need to build tools to enable us to travel to the moon shows that we don’t have a physique biologically adapted to space travel or living on the moon. Behavior and technology always evolve much more rapidly than biology, and technology can easily allow us to do something contrary to our biology, like deep-sea diving, visiting the moon, smoking cigarettes, or eating animals.

Some people claim that the use of dogs, horses, and tools enabled humans to biologically adapt to hunting and eating animal flesh. On the contrary, the use of dogs and tools (and cooking) removes natural selection pressures that would favor the evolution of human physiology in the direction of greater adaptation to hunting and consumption of flesh. The use of these tools and techniques allows humans to succeed at an enterprise for which they are biologically ill-equipped.

Furthermore, during the time period when some authors claim that hunting and flesh-eating profoundly affected human biological (particularly neurological) evolution, the purported human ancestors (e.g., Homo habilis) did not have these tools and techniques. If those purported ancestors had inhabited an environment that required them to hunt in order to survive to reproduction, natural selection would have strongly favored the survival of individuals having mutations that would make them innately faster and stronger than the available prey.

Although some might argue that natural selection favored the survival of those human ancestors who could invent, fashion, and adopt tools and behaviors that allowed them to overcome their biological limits, this argument fundamentally admits that humans adapted to hunting and flesh-eating by culture, which does not necessarily entail adaptations in other aspects of physiology and metabolism. As I have already stated, when a species finds a way to adapt to some extent to a new diet by altering behavior, this tends to forestall genetic/biological adaptations to the new diet.

130 Williams WR. The Natural History of Cancer. William Wood and Company, New York, 1908. 16.

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Summary

The fossil record indicates that bipedal locomotion developed in the hominin lineage long before hominins primarily inhabited grasslands and engaged in technology-assisted persistence hunting. The modern human locomotive system has features (plantigrade stance, 180 degree extension of the knee) suggesting a primary adaptation to standing still and efficient walking, activities primarily suited to gathering plants. Although our locomotive musculoskeletal system is well-adapted to endurance running, we require the high carbohydrate diet supplied by a starchy plant based diet to repeatedly engage in persistence hunting. Therefore, our locomotive system provides evidence that human ancestors ate a plant-based diet, which powered their foray into persistence hunting.

66 – HUMAN NUTRITIONAL ADAPTATIONS 5: Manual Endowments

Manual Dexterity and Tactile Sense

Can you imagine a dog or cat attempting to peel an orange or remove peas from their shell?

The edible parts of plants have high variable textures, and some, such as seeds, are small and must be carefully unpacked from other, inedible plant structures, such as peas in pods. This type of feeding, particularly on seeds, requires a relatively high tactile sensitivity to textures. In contrast, a mammal that feeds on flesh does not need to make fine tactile distinctions in order to kill and consume other animals.

Animals that specialize in eating animal flesh use their claws to capture animals, but they neither need nor have the manual dexterity nor the tactile sensitivity necessary to hold a fruit and carefully separate the inedible peel from the edible portion. They can paw and claw at objects, but they can’t carefully separate them into distinct parts.

We find separated digits, high levels of manual dexterity, and the tactile sensitivity required to separate the edible from the inedible in plant foods in animals that specialize to some degree in eating fruits, nuts, and seeds while holding them in the hands, such as some rodents (mice, rats, squirrels) and especially all primates. Apparently natural selection favors high tactile sensitivity and manual dexterity in animals that specialize in botanical frugivory.

As noted by Milton, “primates feed very selectively, favoring the highest-quality plant parts––for instance, even primates that eat leaves tend to choose very immature leaves or only the low-fiber tips of those leaves.”131 In other words, primates are by nature picky eaters. If to survive some primate specialized in feeding very selectively on high energy but relatively fragile or small foods easily damaged by rough handling, such as very ripe fruits, especially berries; or requiring careful manual processing, such as peeling and seeding; or found in small packages requiring careful removal, such as peas in pods or small nuts or seeds in shells; natural selection would rapidly favor the reproduction of those individuals having the greatest manual dexterity and tactile sensitivity and control.

Australopithecus garhi, dated to 2.5 mya, apparently used stone tools, and fossils of Au. afarensis have hands indicating human-like adaptations for manual dexterity dating to 3.2 mya.132 Panger et al. comment:

“Thus, adaptations for manual dexterity appear well before the earliest known evidence of modified stone tools. These adaptations suggest that early hominins used or made tools, possibly including modified stone tools, or engaged in other manipulative tasks, such as food preparation,

131 Milton K. Diet and Primate Evolution. Scientific American 1993 August: 86-93. 90.

132 Panger MA, Brooks AS, Richmond BG, Wood B. Older than Oldowan? Rethinking the Emergence of Hominin Tool Use. Evolutionary Anthropology 2002;11:235-45.

that are more complex than those practiced by extant great apes before the earliest known stone tool record.”

Since the hand movements involved in manufacturing and using a hand-held stone tool are similar to those involved in processing fruits, vegetables, nuts, and seeds before consumption, I suggest that, most likely, the ability to handle stones as tools and modify (process) stones to produce tools arose from the ability to use the hands to engage in very picky plant food eating and processing.

As we have seen, the human sensory system guides us toward botanical fruits, not toward flesh, suggesting that our manual dexterity must also have evolved to facilitate consumption of botanical fruits. Since the relatively frugivorous chimpanzees and orangutans have more manual dexterity and tactile sensitivity than any other type of mammal, and humans have a sensory system tuned to flowers, fruits and vegetables, and more manual dexterity and tactile sensitivity than these apes, it seems likely that human ancestors specialized in consuming those botanical fruits or vegetables that were most accessible to those individuals endowed with great tactile sensitivity and manual dexterity.

It seems possible that we owe a large portion of our ability to do arts and crafts, to play musical instruments and pen poems, to the demands placed on manual dexterity and tactile sensitivity to “picky eating” among human ancestors engaged in an highly specialized highly frugivorous plant-based lifestyle.

Hand and Brain

In humans, the brain has a disproportionate amount of area devoted to motor and sensory functions of the hands (Figure 5.1). About one-quarter of the motor cortex of the brain is devoted to the muscles that move the hands. In the sensory cortex, the area devoted to the hand ranks second only to the face, and in the motor cortex, the area devoted to the hand is comparable to that devoted to the face.

Figure 5.1: Sensory and Motor Homunculi. (After Penfield and Rasumussen, 1950)

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This indicates that evolutionary increases in manual dexterity, sensitivity, and control require coevolution in brain cortical capacity. In other words, specialization in “picky feeding” on fragile fruits, fruits requiring peeling or seeding (including small nuts and seeds), and the tenderest leaves would naturally favor manual sensitivity and dexterity and the increases in brain size necessary to accommodate the sensory and motor functions of the hands.

Manual Dexterity and Manufacture of Hunting Tools

I find the idea that human manual dexterity arose primarily as an adaptation to manufacture and use of tools for hunting or meat-processing unconvincing, for several reasons.

First, as noted above, we have evidence of hominins using, and possibly manufacturing, stone tools, at least a million years before the first evidence of use of tools for removing muscle from animal bones. A. afarensis appears to have had the manual dexterity necessary for tool use and manufacture 3.2 mya, whereas the first evidence for use of stone tools to remove muscle from bone dates to 2.5 mya.

Second, manufacture of the earliest stone tools did not require the same type of tactile sensitivity and manual dexterity involved in manual processing of fruits, seeds, and nuts. Panger et al. describe the probable early hominin tool-making process thus:

“Hard-hammer percussion, the most frequent technique used to manufacture Oldowan-type tools, apparently involved striking a hand-held hammer stone against a hand-held core. However, it is likely that some Oldowan tools were made by placing a core against a substrate and then striking it with another stone or by striking or throwing a stone against a hard surface.”133

I suggest that the reader compare the manual abilities involved in the above scenarios with those involved in shelling peas, picking fragile berries, extracting sunflower seeds from their shells, making twine, or sewing clothing. Which requires the greater fine motor control, picking berries and shelling peas, or hitting two rocks together to remove flakes? Which of those two skills more likely presages the current human ability to build tiny, fragile model ships inside glass bottles?

Third, since extant chimpanzees and orangutans make various non-hunting tools from grass, leaves, sticks, and stones, early hominins probably did so as well.134 Chimpanzees make probing tools and sponges from sticks, bark, grass, leaves, or other vegetation, and use unmodified stone and wooden

133 Panger MA, Brooks AS, Richmond BG, Wood B. Older than Oldowan? Rethinking the Emergence of Hominin Tool Use. Evolutionary Anthropology 2002;11:235-45.

134 Ibid.

MANUAL ENDOWMENTS – 69

hammers to crack open nuts.135 Orangutans habitually and spontaneously make hammers, probes, and scrapers from sticks136 and use leaves to make rain hats and leak-proof roofs for their nests.137

Individuals who could manufacture the best tools for harvesting fruits or roots, such as picking sticks or baskets (a long stick with a hook or basket on the end); or wicker baskets or packs, knives, nut crackers, scrapers, shovels, or other tools to facilitate collection or processing of plant foods would receive the most return from collection of plant foods, and have a greater chance of leaving more offspring. In other words, those hominins who had the best manual dexterity made the best tools for facilitating collection of plant foods, and received the most return from gathering, and therefore left the most descendants. However, no tools made from plant-based materials would survive in the archaeological record, and some stone tools (e.g. nut crackers) may not even look like tools to us and so be archaeologically invisible.138

Further, those who had the manual abilities to use stone blades to harvest wood and fibrous grasses to create the most secure shelters, beds, hammocks, ropes, blinds, barriers, hats, and other gear that helped them protect their families from weather and predators also would have left the more offspring than others who had lesser abilities.

Individuals who made the best weapons for protection from predators would enjoy a similar advantage, and these weapons would also probably also look like weapons for hunting. Individuals who made the best tools for constructing wooden shelters (e.g. axes) as well as the best shelters would probably also leave more descendants than those who did not.

Although some have proposed that Acheulian handaxes served primarily as hunting weapons, this is unlikely because they perform poorly as projectiles.139 Further, the distribution and characteristics of the so-called handaxes associated with Homo ergaster, H. erectus, and H. heidelbergensis suggest that males probably primarily used many of them to attract females, not as tools for hunting, butchery, woodworking, or any other utilitarian purpose.140 Just as a modern male may present a woman with diamonds to display his ability to provide everything she may need, we have evidence that early man sought to impress early woman with his fitness for mating by presenting her with his own hand-made artfully cut and sufficiently rare but relatively useless rocks. Like the diamonds in wedding rings, these rocks had sharp edges primarily for show, not for cutting. In the same way that the male peacock’s plumage signals his ability to avoid predators and find food sufficient to support a functionally

135 Ibid.

136 Ibid.

137 Leake J, Dobson R. Chimps knocked off top of the IQ tree. The Sunday Times 2007 April 15.

138 Panger et al., op. cit.

139 Lieberman DE, Pilbeam DR, Wrangham RW. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 7.

140 Kohn M, Mithen S. Handaxes: Products of sexual selection? Antiquity 1999; 73:518-26.

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superfluous tail fan, it seems that by providing these artfully crafted rocks a man signals that he has so much command of resources that he can afford to spend a significant portion on comparatively useless displays.

Since any of the above could have influenced natural selection of our tactile sensitivity and manual dexterity, I suggest that we consider how our manual dexterity relates to our organism as a whole. I would consider it reasonable to suppose that our manual dexterity evolved primarily or largely to facilitate flesh consumption if other flesh-eating mammals had similar manual endowments or humans also had a large number of other characteristics similar to the physiology of other flesh-eating mammals, unequivocally suited primarily to acquisition, digestion, assimilation, and metabolism of flesh.

On the other hand, since (as I progressively demonstrate) humans have the basic physiology of a species adapted to a plant-based diet, I suggest that our tactile sensitivity and manual dexterity probably initially evolved primarily to facilitate consumption of botanical fruits, particularly very small items, such as berries, nuts, seeds, and similar plant foods. Clever humans have learned to apply these endowments to other purposes including sewing, weaving, making ropes, wood carving, constructing computers, making sharp stones, and watch-making, but the endowments arose before the clever applications. Probably early tool-making contributed to the refinement of this endowment, but we have absolutely no reason to believe that early humans only made stone tools nor that stone tools were only used for the purpose of hunting or butchery. Modern humans use axes, knives and other blades to cut wood and grass and chop fruits and vegetables, giving us good reason to assume that even the earliest of human species used blades for similar purposes, which would have enhanced reproductive fitness as surely as butchering bison.

Claws Versus Nails

Animals biologically adapted to eating animal flesh have sharp claws that play a vital role in gripping and capture of prey, acting essentially as hooks. Valmik Thapar, author of Tiger – The Ultimate Guide, explains:

“A tiger's claws can take the face off a human in one swipe, and deer lucky enough to escape a confrontation with a tiger often bear the scars of the encounter on their hides. Claws play a critical role in the tiger's hunting abilities, helping it to grab and hold prey until its teeth can inflict the final blow. The claws can be a fearsome ten centimeters (four inches) long. A tiger has four of these deadly weapons on each paw, with an extra dewclaw on the front ones. Dewclaws are set back a little and do not touch the ground when the tiger is walking; they are used like thumbs in gripping prey and in climbing.”141 [Italic added.]

141 Thapar V. “Anatomy of a supreme hunter.” From: Tiger–The Ultimate Guide. CDS Books, 2004. 23-33. http:// www.jvbigcats.co.za/tigeranatomy.htm.

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Many four-legged plant-eaters, such as squirrels, also have claws. In tree-climbing species, these provide with a strong grip on wood to enable the individual to scale a surface that it can’t otherwise grab tightly, such as a tree trunk.

Like chimpanzees, gorillas, and other primarily herbivorous primates, humans have nails instead of claws. Nails do not act as hooks nor help a primate climb trees; primates are large enough relative to the trees they climb to use their hands and feet to grasp branches. For primates, nails play a role in food acquisition: they help a primate peel skins and husks off of edible fruits, seeds, and nuts. Thus, our finger- and toenails provide further evidence that humans are primarily adapted to a plant-based diet, not to eating flesh.

If you doubt this, the next time you have the opportunity, attempt to sink your fingers into the flesh of a cow, pig, or chicken. By the way, a natural carnivore would enjoy sinking its claws into the flesh of prey. If you find the suggestion or image of your fingers sinking into the flesh of a cow and ripping it open at all repulsive, you don’t have the constitution of a carnivore.

Lacking claws, humans have invented various tools to perform the functions of claws when hunting animals. These include lassos, spears, fishing hooks, hooked knives, forks, and similar items. Our need to use these tools to succeed at hunting demonstrates that we do not have biological adaptation to hunting.

Once again, use of these tools actually removes selection pressure for the development of physical adaptations suitable for hunting.

72 – HUMAN NUTRITIONAL ADAPTATIONS 6: Face, Mouth, and Throat

Facial Musculature, Jaws, and Throat

Mammals primarily adapted to eating flesh have jaws that have their hinges on or very nearly on the same plane as the jaws themselves, which allows them to open to a diameter exceeding the diameter of the individual’s head. Natural selection favors a large mouth filled with sharp teeth in animals that specialize in eating flesh, because these allow the carnivore to capture and hold the struggling prey with the mouth, rip large bites of meat from its prey, and even to swallow prey animals whole without even chewing (e.g. crocodiles, snakes).

The jaws of carnivores do not move side to side but only vertically, because a jaw with side-to-side motion has insufficient stability for the powerful bite required for ripping into live flesh. Flesh-eating animals usually have a large and powerful tongue capable of quickly tossing large chunks of meat into the throat. The carnivore’s throat expands to allow the passage of the meal, allowing the animal to “wolf down” the flesh without significant chewing.

In contrast, the jaws of primarily plant-eating animals have hinges above the plane of the molars, resulting in a relatively small opening for the mouth, adapted to intake of small bits of food. The jaw joint of plant-eating animals also allows slight side-to-side movement necessary for grinding fibrous materials. The throat of primarily plant-eating animals has a fixed diameter, and can easily get blocked by any firm, unchewed flesh, causing choking.

Primarily plant-eating animals such as primates, horses, cattle, and sheep all have fleshy lips and cheeks that enable the individual to grasp small bits of fibrous food with the lips and chew it extensively. Natural selection favors fleshy, expandable cheeks in animals that specialize in eating fibrous plant foods, because these allow room for movement and expansion of the mouth contents during vigorous chewing and mixing with saliva. In contrast, animals highly adapted to eating flesh have virtually no facial musculature, no fleshy lips and no cheeks.

Due to this difference in facial musculature, carnivorous species can only lap up water, whereas plant- eating species take water by sipping. Also, plant-eating species can form the lips to give a kiss, whereas carnivorous species cannot kiss because they have no lips. Plant-eaters have the ability to form facial expressions with their muscular faces, whereas carnivores can’t form facial expressions due to lack of facial musculature.

How about humans? We have fleshy lips and expandable cheeks, our jaw hinges above the plane of the molars and also moves side-to-side, and our throat has a fixed diameter which makes it impossible for us to “wolf-down” our foods without risk of choking. We can kiss, sip water, and make faces. We owe all of this to our adaptation to a plant-based diet.

Teeth

Cats, dogs, and other mammals adapted primarily to flesh-eating have very sharp, shearing teeth, often with significant interdental gaps. In contrast, primates, horses, cattle, sheep, and other mammals primarily adapted to eating plants have very closely spaced teeth, and molars with a relatively flat grinding surface (which may have cusps for shearing tough plant fibers), necessary for extensive chewing of fibrous plant foods.

In carnivores belonging to the order Carnivora:

“Incisors and canines are used to apprehend food and kill prey, pointed premolars pierce and hold prey, and molars are involved in both slicing and crushing functions....the slicing function of the molars is produced by occlusion between the carnassials, the lower first molar (m1), and the upper fourth premolar (P4). The m1 is usually the only tooth involved in both slicing and crushing/grinding. It is divided into an anterior blade (trigonid) and posterior basin or ‘heel’ (talonid).”142

As the hypercarnivores (e.g. cats) evolved from mesocarnivorous ancestors, they developed a dentition sharper and more shearing than found in mesocarnivores. On the other hand, as the hypocarnivores evolved from their mesocarnivorous ancestors, they developed grinding molars.143 The dentition of canines (foxes, dogs) exemplifies that typical of mesocarnivores (50 to 70 percent of diet from flesh), and that of bears and raccoons exemplifies the hypocarnivore dentition.144

Despite their dental evolution of large grinding molars, hypocarnivores such as the panda retained the gut proportions and shape found in other carnivores (short and simple). This suggests that dentition may evolve more rapidly than gut features. If so, and humans have genetically adapted to a flesh-based, mesocarnivorous diet, as suggested by Loren Cordain, Ph.D., then we might reasonably expect that humans have a dentition more similar to that of mesocarnivores (e.g. wolves) than other apes.

However, the evolution of dentition in hypocarnivores also illustrates the concept of naturally selected kluges. The term “kluge” comes from computer design, and refers to a system constituted of poorly matched elements or elements originally intended for other applications, which may be clumsy or inelegant, but nevertheless solves a problem.

In the case of pandas, bears in general, and other hypocarnivores, we have systems wherein the diet, dentition, and gut are poorly matched; the gut originally evolved to process animal flesh, and has retained the typical carnivore form and function, but natural selection has partially remodeled the teeth

142 Van Valkenburgh B. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47(1): 147-163.

143 Ibid.

144 Ibid.

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for improved function in mastication of plant foods. Their guts remain a match for an animal-based diet and a mismatch for a plant-based diet. We can’t say that the panda’s system as a whole is really well- adapted to a plant-based diet, but, combined with behavioral changes (discussed in Chapter 2), the kluge works “good enough” to support continued though tenuous reproductive success.

Therefore, we must keep in mind that even if humans do have teeth specifically adapted to consumption of animal flesh, if the rest of human physiology remains primarily adapted to a plant-based diet, we just have another example of a naturally selected kluge: an evolved solution to a problem that resulted in a system consisting of somewhat mismatched parts.

Human Dentition In Comparison To Other Extant Apes

According to Thompson, in comparison to the other anthropoid apes, modern humans have dental features least similar to flesh-eating animals:

“In the Apes there is a diastema in front of the canine above into which the lower canine closes. In man there are no spaces between the teeth…In the Apes the canines are very large and long, with sharp edges behind like the Carnivora, and are larger in the male than in the female. In man they are reduced to a level with the other teeth, the animal features are obliterated, and there are no sexual differences in these teeth.”145

“The teeth in general are larger, thicker, and coarser in the Apes, are more square and angular, and the cusps and edges more prominent and sharp. In man the teeth are smaller and finer in texture, the crown is narrower and rounder, the angles are reduced, and the cusps and edges are short and blunt.”146 [Italic added]

Lieberman et al. state:

“Human and chimpanzee teeth lack shearing crests necessary to comminute raw, tough meat effectively. A chimpanzee can spend as many as 11 hours consuming a few kilograms of colobus monkey, yielding a meager return of approximately 380-400 Kcal/hr, similar to eating fruits… Preliminary experiments involving Harvard undergraduates (Lieberman, unpublished data) also indicate that raw meat is difficult to chew for humans, requiring more force per chew and more chews per unit of mass to break down into pieces small enough to swallow.”147

Simply, humans do not have the type of teeth required to process raw meat.

145 Thompson AH. A manual of comparative dental anatomy for dental students. The S.S. White Dental mfg. co., 1899. 155. Accessed on Google Books Online on October 13, 2012.

146 Ibid., 155-156.

147 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 12.

FACE, MOUTH, AND THROAT – 75

Further, Australopithecines did not have teeth adapted to raw meat-eating either. According to Hawks, in comparison to chimpanzees, orangutans have jaw musculature and teeth more comparable to Australopithecines.148 Hardus et al. reported:

“According to orangutan data (ingestion rate of 185 kcal/h), Australopithecus africanus would have had to chew for ca. 2 h to achieve 25% of these caloric requirements purely from meat (Table III, orangutans x A. africanus), while achieving the remaining 75% of its caloric requirements from food sources with faster chewing/intake rates, e.g. leaves or insects. This constitutes a considerable period of the day for orangutans, which spend ca. 6 h/d feeding (Morrogh-Bernard et al. 2009), and does not include the time necessary for the collection of vertebrate prey.”149

This has two implications: 1) Australopithecus species probably could not have lived on an animal-based diet because they could not obtain enough food in a day from such a diet; 2) Lacking fire, animal tissue probably was an elective, luxury item for Australopithecus, indulged in only when plant food resources were abundant and easy to procure; 3) early humans could not have afforded to dedicate much if any foraging time to acquisition of animal flesh until they had control of fire so they could cook it, which makes it easier to chew.

The fact that both fossil and modern humans lack teeth suitable for chewing raw meat indicates that the human lineage never depended on raw meat for survival, because if the ability to obtain adequate energy from raw meat had been requisite for survival in the human lineage, natural selection would have favored individuals with dentition suitable for making short work of chewing raw meat.

Nevertheless, some have argued that natural selection favored dental changes in early humans as an adaptation to a carnivorous diet. In the following, I evaluate these claims.

Canine Teeth

Some people have argued that humans have reduced canine teeth because our ancestors used stone tools to kill animals and eat meat. They believe that natural selection eliminated large canines from the human lineage by favoring those individuals who had small canines but big tools.

This argument appears to rest on the incorrect assumption that possession of enlarged canine teeth unequivocally indicates that the owner uses the teeth primarily for hunting, such that use of tools for hunting would relax the natural selection for this dentition. However, modern chimpanzees, gorillas, and orangutans all have sharp canines that project well beyond the level of the other teeth, yet none of them eat nutritionally significant amounts of animal flesh (see Appendix D for extensive discussion of

148 Hawks J. Orangutan loris capture and meat-eating. John Hawks Weblog. Retrieved Nov 12, 2013 from http:// johnhawks.net/weblog/reviews/behavior/orangutans/orang-hunting-hardus-2012.html#ref1 .

149 Hardus ME, Lameira AR, Zulfa A, et al.. Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii). Int J Primatol 2012;33:287-304.

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chimpanzees). Their failure to use their canines for hunting has not resulted in reduction of their canines. Thus, we have no evidence to support the hypothesis that natural selection has favored large canines in hominoids only or primarily because they improve success at bare-handed hunting; nor for the hypothesis that failure to regularly use the canines to kill prey results in selection for smaller canines in hominoids.

Fossils of an apparently bipedal ape, Orrorin tugenensis, dated to about 6 mya, have small, low crowned canine teeth.150 Australopithecus afarensis lived about 3.7-3.0 million years ago. Afarensis had somewhat reduced canines compared to modern chimpanzees. It appears that afarensis used sharp rocks to remove animal flesh from carcasses as early as 3.39-3.2 mya, but evidence suggests that this behavior “was probably infrequent and did not result in the large accumulations of artefacts and bones that usually catch the eye of archaeologists and palaeontologists.”151 The Orrorin fossils indicate that reduced canines first emerged in the hominin lineage some 2.7 my before Australopiths were using stones to remove flesh from bones.

Australopithecus africanus lived about 3.3-2.5 million years ago. Like modern humans, africanus had relatively large front teeth and their canine teeth did not project much beyond the others. Archaeologists have found remains of africanus alongside broken animal bones, but it appears that predators such as lions, leopards, and hyenas had not only left those bones, but also preyed upon africanus individuals.152 Although africanus may have been prey more than predator, s/he also might have eaten some animal flesh:

“More likely, they obtained meat by scavenging what remained on the abandoned corpses of large animals killed by lions and other predators. It is possible that they also did some hunting of small animals in much the same inefficient manner of chimpanzees today. They probably ate insects and eggs as well.”153

Hence, assuming that humans descended from either Orrorin or australopiths, it appears that natural selection started favoring canine reduction in hominins well before 3.7 mya, and canine reduction to modern levels was completed by 3.3 mya, well before hominins had well-developed stone technology and efficient hunting skills, and probably before they had control of fire. Therefore, it seems unlikely that technology-assisted hunting or meat-eating was the primary factor that selected for dental canine reduction in the human lineage.

150 Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis:Perspectives on Hominin Evolution. Cambridge University Press, 2012. 110. http://books.google.com/books?id=PrJ1lmjMakoCandpg=PA116#v=onepageandqandf=false

151 Braun DR. Australopithecine butchers. Nature 2010 Aug 12;466(7308):828.

152 Smithsonian National Museum of Natural History. What does it mean to be human? Australopithecus africanus: How They Survived. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/australopithecus- africanus .

153 Early Hominin Evolution: Analysis of Early Hominins. Retrieved on October 16, 2013 from http://anthro.palomar.edu/ hominid/australo_2.htm

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Dental Shearing Quotient

Some anthropologists believe that a diet of tough foods, possibly animal flesh, selected for sharper, more shearing teeth in early humans. Ungar performed detailed analysis of the occlusal relief and shearing quotient (SQ) (slicing ability) of the molars of early human specimens (H. habilis and H. erectus) in comparison to Australopithecus afarensis and living apes (chimpanzees and gorillas).154 He states that studies of SQ “are limited to unworn teeth” and “few, if any, early hominin taxa are well enough represented by unworn teeth to allow statistical comparisons with extant baseline series.”

“There are, for example, fewer than 10 unworn M2s [second molars] in the entire collection of unpublished australopith teeth from South Africa....The picture for early Homo is even bleaker, 155 with no available unworn M2s of H. habilis, H. rudolphensis, or African H. erectus.”

Ungar wrote this in 2004. In 2012, he reported that, prior to 2007, the sample sizes for H. habilis and H. erectus amounted to “five and eight individuals, respectively” and by 2012 the sample size for H. habilis had increased to ten specimens, while the number of H. erectus specimens remained at eight.156 Thus, we base our knowledge of these species on a very small number of specimens, and all of the early human specimens have worn teeth.

Ungar stated that “It is not possible at this time to evaluate form-function relationships for individual species of early Homo because of very limited sample size,” so for his topography analysis he had to combine all worn molars of all early Homo (H. habilis, H. rudolfensis, and H. erectus ) teeth to compare them to australopithecus teeth.157 Therefore, the data he produced does not support any supposition or claim that the teeth (or diet) of H. habilis differed markedly from those of H. erectus.

According to Ungar’s topographic analysis:

“Gorilla gorilla specimens tend to have the steepest slopes and most relief, followed by early Homo, then Pan troglodytes [chimpanzees], and finally A.afarensis, which has the flattest slopes with the least relief...early Homo slope and relief mean values are smaller than those of G. gorilla in all six cases and larger than those of P. troglodytes in five of six cases.”158

154 Ungar P. Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution 2004:46:605-622.

155 Ibid., 606.

156 Ungar et al.. Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007. Journal of Human Evolution 2012 Aug 1;63(2):429-437.

157 Ungar, Dental topography and diets of Australopithecus afarensis and early Homo., op. cit., 608.

158 Ibid., 612.

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Thus, these early human teeth had less shearing ability than modern gorilla teeth. Ungar notes that the differences between chimpanzee and gorilla teeth correlate with differences in diet. Although both prefer fruits:

“Differences between the two taxa are notable at times of scarcity...when gorillas fall back on tougher, more fibrous foods (such as leaves and stems) than those eaten by chimpanzees.”159

According to Ungar, gorillas have steeper crests on their teeth in order to deal with these leaves and stems:

“Several studies have shown that gorillas have longer shearing crests and steeper cusps than do chimpanzees....These occlusal differences clearly reflect differences in the mechanical demands of their diets. Tougher fallback items taken by gorillas require long tooth-tooth contact times, and steep planes of contact for shearing and slicing.” 160

According to Ungar, the fact that early humans molar crests were steeper than A. afarensis, but not as steep as gorillas, suggests that “early Homo may have relied more on tough fallback resources, perhaps including meat.”161 However, since meat is not the only possible tough food on the menu, he also states “Hopefully, other approaches to the reconstruction of diet, such as bone and tooth chemistry analyses, will provide further evidence with which to evaluate this hypothesis.”162

Further, Ungar goes on to say:

“Such hypotheses must, however, be tempered by the acknowledgement that, while a great deal of research has focused on the paleoenvironmental context of the Plio-Pleistocene hominins...we cannot know the full complement of foods available in the past, let alone infer their material properties.” 163

Since limited tool use appears to have first emerged among the later australopithecus species (flatter teeth), and H. erectus had greater mastery of stone tools than australopithecus, Ungar’s report indicates that sharper teeth and greater tool use evolved concurrently during the emergence of early humans. This suggests that use of external blades at that time did not reduce the need for dental adaptation to whatever those early hominins habitually consumed. With this in mind, he remarks:

159 Ibid., 615.

160 Ibid., 615.

161 Ibid., 618.

162 Ibid., 617.

163 Ibid., 617-18.

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“Tool use introduces another possible confounding variable for interpreting dental morphology in early Homo...If early Homo became increasingly reliant on tools...selective pressures on their jaws and teeth may have changed along with properties of foods as they were altered by preparation...If selective pressures changed accordingly, this could make it even more difficult to use form-function relationships to reconstruct the diets of these hominins.”164

Given the foregoing, the fact that early humans had sharper teeth than Australopiths fails to provide unequivocal evidence that natural selection favored these teeth specifically and primarily as an adaptation to eating flesh. Since early Homo dental crests are not even as sharp as those found in living gorillas, and gorillas use their teeth to process vegetation, not meat, natural selection may have favored those early humans who had sharper teeth because they facilitated consumption of a diet containing tough plant foods, such as tough fruits, or leaves and stems.

As noted in Chapter 1, it is highly unlikely that meat would have served as a fallback food for early Homo species, for several reasons: 1) those people would have had relatively poor hunting skills when well-fed and worse skills when poorly fed with an inadequate carbohydrate intake; 2) wild African game is too low in fat and energy, especially during times of nutritional stress, to serve as a fallback food for humans with insufficient carbohydrate intake; 3) contemporary African hunters fall back on plant foods, not animal flesh. Therefore, most likely, meat was a luxury food, not a fallback food, for early Homo. Since natural selection is most intense when a population is under nutritional stress, this would imply then that the sharper crests of early Homo teeth represent an adaptation to some fall back plant food.

In 2011 Li et al. reported that the AhR receptor in human intestinal immune cells apparently requires ligands derived from I3C, a compound present in cruciferous leafy vegetables, to maintain full function.165 In the absence of ingestion of these vegetables, the intestinal immune system loses its ability to regulate intestinal microbiota and this allows pathogenic microbes to proliferate, potentially leading to colitis. This suggests that humans have a dietary requirement for green leafy vegetables from the Brassica family, to maintain gut health. Although modern people frequently eat these foods steamed or boiled, late Australopithecines and early Homo did not have the vessels necessary for cooking green leafy vegetables, so they probably would have eaten them raw. Viewing the human as an integrated system, I hypothesize that the increased shearing quotient of human teeth may have evolved to facilitate the consumption of raw green leafy vegetables as a fallback food, just as in gorillas.

In 2012, Ungar also conducted a microwear analysis of H. erectus molars, and reported:

“The dispersion of [microwear texture] complexity values for H. erectus is most similar to that of P. robustus, which has been reconstructed to be a hard-object ‘fallback feeder.’”166

164 Ibid., 618.

165

166 Ungar et al.. Dental microwear texture analysis of hominins etc. Journal of Human Evolution 2012 Aug 1;63(2):429-437. 435

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Thus, in 2004, Ungar believed that the steeper crests of H. erectus molars indicated that H. erectus may have used a tough food, perhaps meat, as a fallback food, and in 2012, he reported evidence that H. erectus teeth showed microwear similar to a hard-object fallback feeder. So which was it, tough-elastic foods, or hard foods? According to Ungar, “These [microwear] results were interpreted to suggest that the H. erectus individuals examined may have eaten a somewhat higher proportion of tough or hard- brittle foods prior to death than did H. habilis.”167 In other words, the dental data did not permit deciding between the alternatives.

Ungar also remarked:

“Finally, it must be remembered that the H. erectus craniodental complex still showed rather thick jaws and tooth enamel compared with living great apes.”168

In other words, H. erectus still had a craniodental complex compatible with a plant-based diet.

While discussing the dentition of australopithecus species, Ungar (with Teaford) has also pointed out that heavy reliance upon tough fruits (in contrast to juicy, soft fruits) would also select for sharp, shearing, slicing teeth:

“Interestingly, as suggested by Lucas and Peters (46), another tough pliant food they [early hominins] would have had difficulty processing is meat. In other words, the early hominids 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. In contrast, given their flat, blunt teeth, they were admirably equipped to process hard brittle objects. What about soft fruits? It really depends on the toughness of those fruits. If they were tough, then they would also need to be precisely retained and sliced between the teeth. Again, early hominids would be very inefficient at it. If they were not tough, then the hominids could certainly process soft fruits.”169

Ungar and Teaford have indicated that some evidence (dental and otherwise) supports the hypothesis that early human ancestors may have had a diet rich in underground storage organs of plants,170 and Ungar co-authored a report of evidence that Australopithecus sediba, a species claimed by some to be the link between the Australopiths and the earliest humans, consumed wood and bark, foods at least as tough as meat, and certainly favoring those individuals with more shearing teeth.171 Further, Ungar has also reported that although the shape of teeth can tell us what an ancient species was capable of eating,

167 Ibid., 435.

168 Ibid., 436.

169 Teaford MF, Ungar PS. Diet and the evolution of the earliest human ancestors. PNAS 2000; 97(25): 13506–13511.

170 Ibid.

171 Henry AG, Ungar PS, Passey BH, Sponheimer M, et al.. The diet of Australopithecus sediba. Nature 2012/06/27/online.

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tooth shape does not necessarily tell us what the species actually did eat.172 Thus, to reiterate, the fact that some early erectus specimens had sharper teeth than australopithecus specimens does not unequivocally indicate that the shape of their teeth arose primarily as an adaptation to consumption of meat, rather than other tough foods, like bark, leaves and stems.

Johns Hopkins University anthropologist Alan Walker examined fossil teeth from hominids of the 12– million–year period leading up to Homo erectus and found that every one of them had microwear markings consistent with a primarily frugivorous diet; not until Homo erectus did he find dental signs of flesh consumption.173 Walker noted that the frugivorous diet of these early human ancestors probably included tougher, more substantial fruits such as (his example) acacia pods and seeds as well as soft, sweet, juicy fruits.

Acacia belongs to the legume family, and Cordain et al. list acacia seeds as one of the foods consumed by modern hunter-gatherers.174 Its seeds have a crude content (by weight) of about 27% protein, 52% carbohydrate and 6% fat, and a relatively high energy content of about 3.5 kcal/g.175 The carob tree (Ceratonia siliqua), native to north Africa, produces a tough but edible pod. Carob pod is edible raw and supplies 2.2 kcal/g, and (by weight) consists of 5% protein, 49% sugars, 40% fiber, and 1% fat. In comparison, Eaton et al. reported that 21 species of African wild game flesh supply an average of 1.4 kcal/g, less than half of acacia and 36% less than carob.176 As noted by Ungar and Teaford, a diet including significant amounts of tough fruits like acacia or carob would have naturally selected for sharper teeth.

To summarize, the shearing quotient of the teeth of early humans does not even reach the same level as that found in the primarily folifrugivorous gorilla, and we have no evidence to support or reason to believe claims that the increased SQ of early human teeth evolved specifically to facilitate consumption of animal flesh rather than tough leaves and fruits.

Dental Carbon Isotope Studies

Trees, bushes, and many herbaceous plants use C3 photosynthesis, which primarily incorporates carbon-12, while tropical grasses and some sedges use C4 photosynthesis, which incorporates relatively

172 National Science Foundation. Ancient “Nutcracker Man” Challenges Ideas on Evolution of Human Diet. Press Release 08-070. April 30, 2008.

173 Rensberger B. Teeth Show Fruit Was The Staple. New York Times, May 15, 1979. C1.

174 Cordain L, Brand-Miller J, Eaton SB, Mann N, Holt SHA, Speth JD. Plant-animal subsistence ratios and macronutrient energy estimations in worldwide hunter-gatherer diets. Am J Clin Nutr 2000 Mar;71(3):682-692.

175 Aganga AA, Tsopito CM, Yeboah SO, et al.. Evaluation of the chemical composition of some locally available acacia seeds as animal feed in Botswana. www.internationalgrasslands.org/files/igc/.../2-23-003.pdf ; Corcoran M. Acacia Seeds. Australian National University, 1998. http://fennerschool-associated.anu.edu.au/fpt/nwfp/acacia/acacia.html ; Maslin, Thomson LAJ, MacDonald MW, Hamilton-Brown S. Edible Wattle Seeds of Southern Australia. Csiro Publishing, 1998.

176 Eaton SB and Konner M. Paleolithic Nutrition: A consideration of its nature and current implications. NEJM 1985 Jan 31;312(5):283-289.

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more carbon-13. When animals eat these plants, the carbon isotopes enter tooth enamel, and remain there for millions of years.

In 2012, Oxford University researchers reported finding isotopic evidence that some Australopithecus groups primarily ate the roots, corms, or bulbs of tropical grasses.177 One of the researchers involved in this report stated:

"Based on our carbon isotope data we can't exclude the possibility that the hominins' diets may have included animals that in turn ate the tropical grasses. But as neither humans nor other primates have diets rich in animal food, and of course the hominins are not equipped as carnivores are with sharp teeth, we can assume that they ate the tropical grasses and the sedges directly."178

Carbon isotope studies suggest that by 2.5 million years ago, early Homo species consumed a diet containing carbon derived from both C3 and C4 plants; by 1.7 million years ago, 35% of the diet came from C4 sources, and by 1.4 million years ago, 55% of the diet came from C4 sources. This indicates that early human species probably ate either 1) some part of tropical grasses and sedges, or 2) animals that ate tropical grasses.

As already mentioned, humans do not have teeth sharp enough to efficiently chew raw meat. Hardus et al. estimate that a male H. erectus would have had to chew on raw meat for 3.10 to 6.72 hours daily to obtain 50% of his energy from raw meat.179 This does not include the time required to hunt and butcher the animal, and the time required to consume the other 50% of energy from plant foods.

The hypothesis that H. erectus got 55% of his diet from raw grass-fed animal flesh lacks plausibility for several reasons. First, it requires individuals to spend a minimum of 6 hours daily engaged in chewing foods (at least 3.1 h chewing meat, and at least 3.0 h chewing raw plants), in addition to spending hours daily obtaining the foods. Secondly, it requires H. erectus to bring home meat more often than do modern African hunters. Third, it proposes a protein intake that would be toxic or lethal, particularly to pregnant women and their infants (as discussed in Chapters 11 and 12). Fourth, it would require H. erectus to engage in persistence hunting without a high carbohydrate intake, whereas we know that humans require a high carbohydrate intake to sustain frequent endurance running (Chapter 4). Fifth, it proposes that humans were inhabiting grasslands highly populated with social carnivores without having fire as a passive defense against predation.

177 Lee-Thorpe J, Likius A, Mackaye HT, et al.. From the Cover: Isotopic evidence for an early shift to C4 resources by Pliocene hominins in Chad. PNAS 2012 109 (50) 20369-20372; published ahead of print November 12, 2012.

178 University of Oxford (2012, December 14). Scientists 'surprised' to discover very early ancestors survived on tropical plants, new study suggests. ScienceDaily. Retrieved September 16, 2013, from http://www.sciencedaily.com/releases/ 2012/12/121214200916.htm

179Hardus ME, Lameira AR, Zulfa A, et al.. Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii). Int J Primatol 2012;33:287-304. Table III

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Therefore, if by 1.4 mya 55% of erectus/ergaster diets came from C4 sources, it is highly unlikely that much of this would have come from raw meat. On the other hand, if as the evidence from Koobi Fora and Swartkrans indicates (Chapter 1), they had control of fire by 1.4 or even 1.7 mya, they could consume large amounts of the abundant bulbs, corms, roots, tubers, and seeds of C4 type plants. This basic starch-based diet then would allow them to engage in endurance running as a means of hunting in times of luxury. Unlike the meat hypothesis, this scenario is consistent with the carbohydrate- dependence of human endurance running metabolism (Chapter 4) as well as our modest protein requirements and low tolerance for high protein diets, particularly during pregnancy (Chapters 11 and 12).

According to Ungar, the teeth of African H. erectus specimens have, in comparison to H. habilis specimens, increased numbers of small pits, which also suggest consumption of more hard-brittle or tough foods, and “hint that H. erectus may have included at least some more fracture resistant foods compared with H. habilis.”180 Grass seeds are hard-brittle foods. H. erectus may have included raw or roasted carbon-13 rich grass seeds in his diet.

In any case, even if the carbon-13 in H. erectus teeth was only from animal flesh, this only shows us that they did eat animal flesh, not that their teeth were naturally selected specifically to facilitate consumption of animal flesh. As noted above, H. erectus still had jaw and tooth enamel characteristics suitable for consumption of a plant-based diet, and natural selection would have favored sharper teeth in a species consuming tough plant foods, as it apparently did in gorillas.

Tropical Grasses, Tools, and Teeth

Sorghum (Sorghum bicolor) is a large, drought- and flood-tolerant grass native to Africa that has a sugar- and mineral-rich juice, much like sugar cane (which is native to south Asia). This grass can grow to more than 10 feet in height. Today, sorghum is Africa’s second most important cereal crop.

Modern humans can and do peel the green skins of both the sorghum and sugar canes, and chew on the raw, tough inner tissue (no cooking required). We can do the peeling by tooth and hand, but use of a sharp blade makes it much easier. Stone blades used as sickles would also make harvesting these grasses much easier. Presumably chewing these grasses would have been easier for H. erectus, with his thicker tooth enamel and jaws, than it is for us.

Fallback or habitual use of leaves and stalks of tropical grasses would favor individuals who had sharper, shearing teeth, such as found in early Homo species, just as leaf-eating did in gorillas. Sorghum and other tropical grasses use the C4 pathway to produce carbohydrates, so any hominin that utilized sorghum or similar grasses (stalks, leaves, or seeds) for habitual or frequent fallback food would ingest the carbon-13 found in C4 plants and the flesh of animals that eat such grasses.

180 Ungar et. al. Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007. Journal of Human Evolution 2012 Aug 1;63(2):429-437. 436.

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Evolutionary scenarios that depict humans primarily as highly carnivorous hunters of grassland animals lack a reasonable explanation for how this highly carnivorous species managed to adapt in a relatively short time to a subsistence based on consumption of grass seeds (the so-called agricultural revolution). In contrast, a hominin who specialized in eating raw grass stems and seeds (perhaps consumed in the green state, like green peas or fresh corn) could easily develop a symbiotic relationship with the grass and serve as its seed disperser. This would naturally develop into agriculture over time, with no “revolution” required.

Megadontia Quotient

Comparing modern humans to ancient, the primary difference consists of modern humans having much smaller molars relative to body size. McHenry’s megadontia quotient (MQ) relates molar surface area to body mass. Australopithecus afarensis had an MQ of 1.7, Homo habilis 1.9, Homo erectus, 1.0, Homo neanderthalensis 0.7, and modern Homo sapiens sapiens, 0.9, due to concurrent reductions of molar surface area and increase in body size in the human lineage since the time of Australopithecus species.

Ben-Dor et al.181 and others, believe that larger MQs indicate greater dependence upon fiber-rich plants and that lesser MQs indicate greater dependence on fiber-free animal flesh. Based on this assumption, along with the assumption that H. habilis and H. neanderthalensis obtained 10% and 80% of their energy from animal flesh, respectively, Ben-Dor et al. have created an equation correlating MQ to plant- animal subsistence ratio. Using this, they estimated that H. erectus had and modern humans have a “maximum long-term plant protein ceiling” of 38% and 32% of energy from plants, respectively.182

Generally, to establish form-function relationships in evolution, we require a consistent relationship between form and function in separate lineages (i.e. convergent evolution). Although Ben-Dor et al. repeatedly refer to Ungar as their expert of choice on dentition, they seem to have missed his clear statement that

“...dental allometry is not simple to interpret; witness the fact that frugivorous cercopithecoids [Old World monkeys] tend to have relatively larger molars than folivorous ones, whereas the opposite is true for platyrrhines [New World monkeys].”183

In other words, in one primate lineage, larger molars correlate with dependence on less-fibrous foods (fruits), but in the other, larger molars correlate with dependence on more fibrous foods (leaves). Further, the apparently bipedal ape Orrorin that lived 6 mya had, among other human-like features,

181 Ben-Dor et al.. Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

182 Ibid.

183 Ungar et. al. Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007. Journal of Human Evolution 2012 Aug 1;63(2):429-437. 435.

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small molar teeth, making this species a microdont,184 yet this species apparently ate a plant-based diet.185 Some experts believe that Orrorin is a far better candidate for a human ancestor than any of the Australopithecus species (Appendix C). Given this, we can’t have confidence that smaller molars in the human lineage unequivocally indicates adaptation to to less fibrous food in general, let alone a positive adaptation to flesh in particular.

Further, molar size constitutes only a portion of the craniodental complex. Since, as noted above, H. erectus “still showed rather thick jaws and tooth enamel compared with living great apes,”186 and modern apes consume plant-based diets, this casts further doubt on Ben-Dor et al.’s hypothesis that H. erectus was dentally incapable of consuming a plant-based diet.

As noted above, Ungar also cautioned that “we cannot know the full complement of foods available in the past, let alone infer their material properties.” He also warned that “Tool use introduces another possible variable for interpreting dental morphology” which “could make it even more difficult to use form-function relationships to reconstruct the diets of these hominins.”

In addition, use of fire would add to the difficulty of establishing a linear relationship between MQ and plant-animal subsistence ratio, because it dramatically softens both plant and animal foods, reducing the need for large teeth to process plants or sharp teeth to process meat. Ben-Dor et al. reject the evidence for H. erectus control of fire 1.6 mya (Chapter 1) which they must to maintain their thesis. However, their thesis predicts that human endurance running performance increases by restricting plant foods and consuming a flesh-and-fat-based diet, which is not supported by available evidence (Chapter 4). Further, as I show throughout this book, their thesis that humans evolved a dependence on an animal- based, high-fat diet is undermined by many lines of evidence.

Hence, no one has established a linear relationship between MQ and plant-animal subsistence ratio, in primates in general or in tool-using hominins in particular.

Another Kluge?

As discussed earlier in this chapter, pandas. other bears, and some other hypocarnivores belonging to the order Carnivora have dentition better adapted to consuming plants than do mesocarnivores (e.g. canines) or hypercarnivores (e.g. felines), yet they retain the typical carnivore gut and metabolism. As stated, their dental evolution illustrates that natural selection processes can cobble together a “good enough” solution – a kluge – to a problem that has little impact on the basic physiology of the organism.

184 Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis:Perspectives on Hominin Evolution. Cambridge University Press, 2012. 110. http://books.google.com/books?id=PrJ1lmjMakoCandpg=PA116#v=onepageandqandf=false

185 Smithsonian National Museum of Natural History. What does it mean to be human? Orrorin tugenensis: How They Survived. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/orrorin-tugenensis .

186 Ibid., 436.

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The evidence I discussed above casts much doubt on claims that humans have teeth specifically adapted to eating animal flesh. Nevertheless, even if someone succeeds in showing that humans have some dental characteristic that is specifically, unequivocally, and primarily or exclusively a naturally selected adaptation to consumption of animal flesh, this would not show that human physiology as a whole is specifically adapted to or requires consumption of animal flesh. Rather, the human body could have a naturally selected kluge that makes us a sort of inverse of the panda. Whereas the bears are animals basically adapted to carnivory, who happen to have teeth somewhat adapted to eating plants, humans could be an animal basically adapted to eating plants, which happens to have teeth somewhat adapted to eating animal flesh.

Comparative Oral Anatomy

Table 6.1 compares the general oral structure and functions of non-primate herbivores, primates, humans, and the cat (hypercarnivore) and dog (mesocarnivore/omnivore). Humans clearly have a general oral anatomy more similar to that of plant-eating primates and non-primate mammals than to that of animals primarily adapted to flesh consumption.

Table 6.1: Oral structures and functions in herbivores, primates, humans, dogs, and cats Horses, cattle, sheep, Primate Human Cat or Dog deer, etc. Jaw joint Above plane of molars Above plane of molars Above plane of molars Almost same plane as molars Jaw movement Rotary Rotary Rotary Vertical only Mandible angle Large Large Large Small Cheeks Fleshy and expandable Fleshy and expandable Fleshy and expandable None Lips Fleshy and dextrous Fleshy and dextrous Fleshy and dextrous None Tongue Short extension Short extension Short extension Long extension Drinking Sips Sips Sips Laps Molars Grinding surface Grinding surface Grinding surface Sharp, no grinding Space between teeth Minimal Minimal Minimal Significant Throat Fixed diameter Fixed diameter Fixed diameter Expandable Primary foods Plants Plants Plants Animal flesh

A Mastication Experiment

To anyone who wonders whether modern humans have dentition significantly adapted to eating raw animal flesh, I suggest the following experiment. Get ahold of a whole (skin intact) carcass, and, without using cooking or knives to prepare the carcass in any fashion, try consuming the raw flesh with only your bare hands and teeth.

FACE, MOUTH, AND THROAT – 87

For this experiment you must use a raw, unprocessed carcass because cooking tenderizes pliant, tough raw flesh, making it easier to masticate with teeth not well adapted to processing animal flesh, and no early hominin species claimed to have dentition adapted to shearing meat clearly had control of fire. You must not use any tool, not even a knife, to slice any part of the flesh, because doing so would not enable you to test how well your teeth can slice and dice raw animal flesh.

Finally, compare how easily you can masticate the unprocessed raw meat to your ability to masticate any raw fruit, any raw leafy green, raw peas in a pod, a raw sweet potato, and a raw carrot. Decide for yourself whether your teeth can more easily process raw meat, or raw plant foods.

Saliva

Salivary glands in the mouth secrete saliva, which keeps the mouth moist, protects the teeth, and in some species contributes to digestion. Animals primarily adapted to eating animal flesh have saliva substantially different from animals primarily adapted to eating plants.

Mammals primarily adapted to an animal-based diet have saliva with an alkaline pH and lacking amylase, a starch-digesting enzyme. For example:

“The pH of dog saliva varies between 7.34 and 7.8 (Altman and Dittmer, 1968), whereas the average value for cat saliva is 7.5 (Awati, 2000). Like many species, dogs and cats lack the α- amylase enzyme that would initiate the process of starch digestion.”187

Animals primarily adapted to eating low-starch grasses, such as horses, also have little amylase in their saliva, while animals adapted to eating more starchy underground storage organs (roots and tubers), such as pigs, produce more:

“Amylase production in horses is limited, however. As a basis for comparison, horses produce approximately 8-10% as much amylase as an adult pig does.”188

In comparison, human saliva ranges between 6.75 and 7.0 pH189 and contains more amylase than other known mammalian species. Compared to chimpanzees, on average humans produce six to eight times more amylase.190

187 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 7.

188 Kentucky Equine Research Staff. Keeping tabs on carbs in equine diets. Equinews 2005 Nov 17. Retrieved September 17, 2013 from http://www.equinews.com/article/keeping-tabs-on-carbs-in-equine-diets.

189 Marieb EN. Human Anatomy and Physiology, Fifth Edition. Benjamin Cummings, New York, 2001. 898.

190 Perry GH, Dominy NJ, Claw KG, et al.. Diet and evolution of human amylase gene copy number variation. Nat Genet. 2007 October; 39(10): 1256–1260. Retrieved September 17, 2013 from http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC2377015/

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Why do we have more acidic saliva than found in cats and dogs? Probably to facilitate the starch- digesting action of amylase, which functions optimally in a pH range of 6.7 to 7.0.191

Of interest, seed-eating rodents (such as squirrels, mice, rats, and chipmunks) share in common with humans both a plantigrade stance (as noted above, suitable for spending a lot of time standing still while holding and eating fruits and seeds) and a duplication of the salivary amylase enzyme gene.192 This suggests that ancestors of both rodents and humans had starchy diets exerting strong natural selection for increased amylase production:

“Independent convergent evolution of salivary amylase in humans and rodents indicates that there has been strong positive selection for salivary amylase at some points during mammalian evolution….

“What selective advantage of salivary amylase might we propose to account for multiple independent evolutionary origins? Because the enzymatic activities of pancreatic and salivary amylases are quite similar, and all mammalian species produce pancreatic amylase, there is no obvious advantage to duplication of the digestive activity per se in the two organs. One interesting suggestion is that sweet-tasting sugars, produced in the mouth by the action of amylase on complex carbohydrates, might function as signals for identifying nutritious food sources.”193

Amylase has only one function, namely to digest starch, a primary component of leaves, stems, fruits, seeds, and roots of plants. Animal flesh, milk, and eggs contain virtually no starch.

Salivary amylase reduces starch to glucose. To identify dietary starch as a nutritious food source, an animal would need both salivary amylase and the ability to taste sugars. Humans have both of these characteristics, which implies that humans are “hardwired” to identify both sugars and starches– nutrients concentrated only in plants– as nutritious foods. In contrast, no one has as yet identified any human taste for any substance concentrated in and unique to animal flesh, such as animal protein or cholesterol. Thus, human salivary amylase production and pH represent a naturally selected heritable adaptation to a plant-based diet.

Apparently all humans (including those from tribes with a history of relatively low starch diet) have at least two copies of the salivary amylase coding gene, similar to wild chimpanzees, but humans carry on average three times more amylase-coding genes than chimpanzees.194 The mutation responsible for

191 Worthington Biochemical Corporation. Introduction to Enzymes. Retrieved September 17, 2013 from http:// www.worthington-biochem.com/introbiochem/effectsph.html.

192 Meisler MH, Ting CN. The Remarkable Evolutionary History of the Human Amylase Genes. Critical Reviews in Oral Biology and Medicine, 4(3/4):503-509 (1993).

193 Ibid., 508.

194 Perry et al., op. cit..

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some humans carrying more than two copies of the amylase gene and producing very large amounts of salivary amylase (relative to other species) appears to have emerged within the last 200,000 years,195 making it a relatively new adaptation compared to the taste receptors that detect the sweet flavor of all sugars, which we share with all great apes and emerged more than thirty-five million years ago in the hominoid primate lineage.196

The mutation conferring high amylase production emerged in coincidence with the first appearance of anatomically modern humans (H. sapiens sapiens) about 200,000 years ago.197 Thus, high salivary amylase production appears to constitute one of the key characteristics of modern humans, i.e. one that makes modern humans different from ancient hominins (e.g. H. habilis and H. erectus) and unique among living primates. It indicates that the direct ancestors of modern humans inhabited a niche wherein natural selection favored the reproduction of individuals who could detect the sugars present in starch-rich plant foods.

Salivary Proline-Rich Proteins

Plant foods contain large amounts of tannins, which some people call anti-nutrients, because they bind and reduce the digestibility and bioavailability of dietary proteins. However, salivary proline-rich proteins (PRPs) help an animal extract nutritional value from plant foods by binding with dietary tannins, and studies of mice and rats have shown that PRPs neutralize the detrimental effects of tannins.198

Ben-Dor et al. and other advocates of the hypothesis that humans require a diet based on animal flesh claim that prehistoric humans could not have relied on nuts or seeds for nourishment because those foods contain tannins.199 Apparently they do not know that about 70% of the proteins in human saliva consist of PRPs.200 Humans have a salivary PRP content consistent with an evolved physiological commitment to to a plant-based diet.

Some authors go so far as to suggest that humans have a “taste” for tannins since we seem to even seek out and prefer foods with a certain level of tannins, such as tea, red wine, beer, chocolate, smoked foods,

195 Ibid.

196 Nofre C, Tinti JM, and D. Glaser D. Evolution of the Sweetness Receptor in Primates. II. Gustatory Responses of Non- human Primates to Nine Compounds Known to be Sweet in Man. Chem Senses 1996 Dec; 21: 747-762.

197 University Of Utah (2005, February 28). The Oldest Homo Sapiens: Fossils Push Human Emergence Back To 195,000 Years Ago. ScienceDaily. Retrieved September 17, 2013, from http://www.sciencedaily.com/releases/ 2005/02/050223122209.htm

198 Mehanso H, Butler LG, Carlson DM. Dietary Tannins and Salivary Proline-Rich Proteins: Interactions, Induction, and Defense Mechanisms. Annual Review of Nutrition 1987 Jul 1;7(1):423-40.

199 Ben-Dor et al.. Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

200 Mehanso H, et al., op. cit., 424.

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herbs, and spices.201 Also, we have evidence that tannins (polyphenols, flavonoids) act as important chemopreventers of infectious and chronic diseases in humans; they have antioxidant, anti- inflammatory, vasoprotective, vasodilatory, antibacterial, antiallergic, hepatoprotective, antithrombotic, antiviral, neuroprotective, and anticarcinogenic effects.202, 203 Thus, classifying tannins as ‘anti- nutrients’ for humans shows ignorance of evidence of human adaptation to tannins, as well as of the benefits of tannins, so it greatly oversimplifies their influence on human health.

This also calls into question claims that other plant components – such as phytates and protease inhibitors – act as anti-nutrients in human diets. Whether any of the so-called anti-nutrients has any harmful effects in humans depends entirely on whether humans have specific metabolic adaptations to these compounds.

Summary

Due to the time lag in evolution, the heritable characteristics (e.g. shape) of the teeth of any early human species (H. habilis, H. erectus) probably tells us what their ancestors ate, not necessarily what that species was eating. For example, if the forerunners of Homo habilis inhabited a niche wherein they needed to eat grass leaves and stems to reproduce successfully, this would have imposed a natural selective pressure favoring the evolution of dentition adapted to processing grass leaves and stems. If enough time passed and enough other genetic mutation and natural selection also took place, the new species (hypothetically, Homo habilis) would (according to this theory) emerge having dentition adapted to the leaves and stems that its ancestors ate. If during this process, the species was also learning to make and use stone tools, or to use fire, this process would have a different affect on dental evolution than if the species was without tools or fire. Hence, the dental characteristics of H. habilis most probably represents adaptation to something that its ancestors heavily depended upon, not something that those ancestors did not heavily depend upon nor something new to H. habilis.

Therefore, if anyone wants to suggest that early human species had teeth uniquely adapted to eating flesh, s/he should provide evidence that for some very long period previous to the emergence of this species, the ancestors of this species had sufficient, obligate dependence on meat-eating to exert a natural selective pressure favoring the survival of a sufficiently large set of individuals, all of whom shared the same genetic mutation producing a new dental form specifically adapted to flesh, and not other tough foods (like acacia fruits).

Based on our knowledge of the diets of hominin species considered ancestors of early humans, it seems that a Darwinian would wonder whether the sharper teeth of early human species represented a naturally selected mutation favored among pre-humans who for millennia relied on tough fruits; or bark and

201 Ibid., 424.

202 Habauzit V, Morand C. Evidence for a protective effect of polyphenols-containing foods on cardiovascular health: an update for clinicians. Ther Adv Chronic Dis 2012 Mar;3(2):87-106. PMC3513903.

203 Soobrattee MA, Bahorun T, Aruoma OI. Chemopreventive actions of polyphenolic compounds in cancer. Biofactors 2006 Jan 1:27(1):19-35. 21.

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wood; or roots, corms and bulbs of tropical grasses. Since current evidence does not suggest that the reproductive success of proposed prehuman hominins (e.g. australopithecus species) primarily depended upon their ability to procure and consume nutritionally significant quantities of animal flesh, it remains unlikely that natural selection favored any characteristic of early humans specifically and primarily or exclusively because it facilitated consumption of animal flesh rather than tough plant foods.

From the above, it seems clear that modern humans have facial and oral characteristics indicating a physiology primarily adapted to a plant-based diet, and lack the specific, heritable characteristics that would make humans well-adapted to consuming flesh.

Our technology affirms the poverty of our native equipment for flesh-eating. Since we can’t efficiently kill or chew an animal with our small mouths, weak jaws and relatively flat, dull, and closely packed teeth, we use technology, namely knives, to accomplish the task that an evolved carnivore performs with its sharp shearing teeth. Carnivores never get meat stuck between their widely spaced teeth; since we get meat caught between our closely spaced teeth, we use a toothpick, to remove it. When we choke on a piece of animal because our throat does not expand to accommodate it, we use the Heimlich maneuver or other behaviors to dislodge it. Thus, we have invented technology and behavior to circumvent the limits of our biology, just as we have invented clothing to circumvent the limits imposed by our relative hairlessness, and airplanes to circumvent our poor aerodynamics.

92 – HUMAN NUTRITIONAL ADAPTATIONS 7: Stomach

Mammals biologically dependent upon flesh-eating may catch prey only once every few days. Lacking refrigeration, a carnivore has an advantage if it has a large, expandable, highly acidic stomach so that it can intermittently gorge itself with a huge amount of flesh with a minimal risk of bacterial infection.

Homo sapiens sapiens lived without any type of refrigeration until about fifty thousand years ago, when some of them migrated from Africa into Eurasia, and then some of them had natural refrigeration part of the year. Some hominins appear to have adopted tool-based hunting and flesh-eating as early as two million years ago in Africa, where ambient temperatures favor quick spoilage and toxic bacterial infestation of raw meat if not immediately consumed. If early human ancestors had heavily depended on hunting and flesh-eating for survival to reproduction, natural selection would probably have favored the reproduction of humans having genes or mutations giving them highly acidic stomachs and immunity to flesh-borne bacterial infections, so that they could consume large amounts of flesh safely before and even during spoilage.

Among animals adapted to eating plants, ruminants such as cows and sheep have stomachs with multiple chambers wherein fermentation takes place, while non-ruminant plant-eating species like horses and chimpanzees have single-chambered stomachs. Since both carnivores and non-ruminant plant-eating species have single-chambered stomachs, it is incorrect to interpret the simple stomach as evidence of adaptation to a flesh-based diet, as claimed by some advocates of meat-based “stone age” diets.204 Instead, we need to compare the human stomach to that of carnivores and non-ruminant plant-eaters.

Primarily or heavily frugivorous primates typically have a simple stomach; primarily or heavily folivorous primates e.g. chimp, gorilla, have either a complex stomach, an enlarged cecum, or an enlarged colon for foregut or hindgut fermentation; and primarily faunivorous primates have a simple stomach.205 As already noted, among primates, only those with small bodies (less than 1 kg) eat primarily faunivorous diets. On this basis, humans have the type of stomach typically found in heavily frugivorous primates.

Stomach Volume

In carnivores and obligate omnivores, the stomach may comprise as much as 60 to 70 percent of the volume of the total digestive tract, to accommodate the large, infrequent meals of freshly killed animals. An animal dependent upon flesh-eating typically has the ability to consume an amount of flesh equal to 30 percent or more of its own body weight at one meal.

The African wild dog (Lycaon pictus) hunts cooperatively and feeds primarily on medium-sized ungulates such as impala, gazelle, kudu, and springbok. One dog can consume a volume of flesh equal

204 For example, Voegtlin WL. The Stone Age Diet. Vantage Press, New York, 1975.

205 Fleagle JG. Primate Adaptation and Evolution. Academic Press, Sep 21, 1998. 293.

to half its body weight in a single sitting, which enables an individual to regurgitate portions of meals to feed pups or other pack members while still meeting its own nutritional needs.206 This ability enables an animal dependent on flesh-eating to maximize the energy return from a single successful hunt, enabling it to live for days without eating and even feed its offspring yet remain in energy balance over the long term.

In comparison, in the horse the stomach comprises ten percent of capacity of whole digestive tract.207 The Ohio State University Horse Nutrition Bulletin actually compares the horse stomach to the human stomach:

“The horse is a nonruminant herbivore. Nonruminant means that horses do not have a multi- compartmented stomach as cattle do. Instead, the horse has a simple stomach that works much like a human’s. Herbivore means that horses live on a diet of plant material.”208 [Italic added]

Chimpanzees consume on average an approximate 50:50 mix of fruits, on the one hand, and leaves and other fibrous plant parts, on the other. The chimpanzee has a stomach comprising about twenty percent of the total gut volume.209 Humans have a stomach comprising approximately seventeen percent of total gut volume,210 proportionately much smaller than that of flesh-eating species and even than chimps but larger than that of horses.

If humans had the stomach capacity of an African wild dog, a 55 kg (120 pound) woman or 68 kg (150 pound) man could consume 27 kg (59 pounds) or 34 kg (75 pounds), respectively, of animal flesh at a single meal. Fully expanded, the typical human stomach holds only about 4 litres (1 gallon) of food,211 which would generally weigh no more than about 4 kg (9 pounds), about 5 to 10 percent of human body mass. Proportionately, a wild dog can in a single sitting consume at least 5 times as much food as a human.

The human stomach has a volume biologically adapted to processing frequent, relatively small, relatively quickly digested meals, a feeding strategy typical of animals primarily adapted to eating plant foods.

206 Potgieter KR, Davies-Mostert HT. A Simple Visual Estimation of Food Consumption in Carnivores. PLoS ONE 2012; 7(5): e34543. doi:10.1371/journal.pone.0034543

207 Ohio State University. Horse Nutrition. Bulletin 762-00.

208 Ibid.

209 Milton K. Primate Diets and Gut Morphology. In Food and Evolution, ed. by Marvin Harris and Eric Ross. Temple University Press, 1987. 99.

210 Ibid.

211 Marieb EN. Human Anatomy and Physiology, Fifth Edition. Benjamin Cummings, 2001. 904.

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Stomach Acidity

Ancient human species lived in Africa and like all other species lacked any type of rapid refrigeration. Animals biologically adapted to eating flesh of large game animals often obtain more meat from a kill than they can eat in a single day, despite having very large stomachs that we lack. They will guard the carcass for several days while continuing to feed on the rotting flesh, in order to maximize return on the energy that they invested in the hunt.

To succeed at this lifestyle, animals biologically adapted to eating flesh produce sufficient stomach acid to keep the stomach at a pH of approximately 1.0-2.0 during food digestion, a necessity for killing microbes and parasites present on raw and decaying meat and for denaturing the large amount of protein that meat supplies.

Most studies have shown that killing of bacteria requires a pH of less than 2.0, which in humans is “rarely maintained for any length of time, especially during food intake.”212 The inability of the human stomach to maintain a pH below 2.0 for very long during food digestion makes it possible for microbes to survive and even colonize the human stomach, as illustrated by the fact that humans frequently contract infections of H. pylori and zoonotic microbes such as E. coli, salmonella, and campylobacter.

According to the CDC, one in six Americans contracts a food-borne illness every year.213 Human defenses against these microbes are quite weak. For example, a single drop of raw chicken juice can infect a person with campylobacter.214 In comparison, up to thirty percent of clinically normal adult dogs and cats carry campylobacter species and thus constitute vectors for campylobacter infection in humans, but campylobacter infections do not commonly occur in adult cats or dogs.215 This indicates that adult cats and dogs have a higher natural immunity to campylobacter than adult humans.

These pathogens occur with similar frequency in both animals raised “organically” or on pasture and those raised conventionally or in confined animal feeding operations (CAFOs). A 2005 study comparing retail organic and conventional chicken found: “Most organic (76%) and conventional (74%) chickens were contaminated with campylobacters. Salmonellae were recovered from 61% of organic and 44% of conventional chickens.”216

212 Zhu H, Hart CA, Sales D, Roberts NB. Bacterial killing in gastric juice – effect of pH and pepsin on Escherichia coli and Helicobacter pylori. Journal of Medical Microbiology 2006; 55:1265–1270.

213 CDC 2011 Estimates of Foodborne Illness in the United States. Retrieved on September 17, 2013 from http:// www.cdc.gov/foodborneburden/2011-foodborne-estimates.html.

214 CDC. National Center for Emerging and Zoonotic Infectious Diseases. Campylobacter General Information. Retrieved on September 17, 2013 from http://www.cdc.gov/nczved/divisions/dfbmd/diseases/campylobacter/#top .

215 Olsen CW. University of Wisconsin School of Veterinary Medicine. Zoonotic Diseases Tutorial (2004 Dec 30). Selected Zoonotic Agents of Gastroenteritis That Can Be Acquired From Dogs and Cats: Campylobacter. Retrieved September 17, 2013 from http://www.vetmed.wisc.edu/pbs/zoonoses/gik9fel/campylobacter.html.

216 Cui S, Ge B, Zheng J, and Meng J. Prevalence and Antimicrobial Resistance of Campylobacter spp. and Salmonella Serovars in Organic Chickens from Maryland Retail Stores. Appl Environ Microbiol. 2005 July; 71(7): 4108–4111.

STOMACH – 95

Grass fed cattle can harbor the extremely pathogenic E. coli O157:H7.217 A 2010 study found no significant differences in the presence of total coliform bacteria, Escherichia coli, or Enterococcus species between grass-fed and conventionally fed beef.218 A review of literature found that studies of grass fed cattle do not consistently demonstrate that cattle fed only grass have lower levels of E. coli.219

Moreover, research has also shown that the flesh of several game animals (deer, wild boar, and hare) constitutes a reservoir for pathogenic strains of E. coli.220 E. coli O157 occurs in free-ranging wild deer,221 and people have contracted E. coli O157 infections from eating wild game flesh.222, 223

These data indicate that the pathogens commonly associated with animal flesh reside naturally in the intestinal tracts of wild as well as domesticated animals. These bacteria will contaminate the flesh when we eviscerate an animal, regardless of whether the animal lived in a CAFO or on pasture. This means that any animal eating wild animal flesh on a regular basis would have regular exposure to deadly strains of bacteria, and exposure to these bacteria would exert a rapid natural selection for resistance to the pathogenic effects of these bacteria.

Cats, dogs, and other animals biologically adapted to eating raw flesh have for millions of years had contact with these bacteria through food, and have evolved adaptations to render them highly resistant to their pathogenic potential. For example, most cats infected with toxoplasmosis show no symptoms,224 whereas humans infected with toxoplasmosis develop swollen lymph nodes and muscle aches and pains lasting a month or more.

217 Sargeant JM, Gillespie JR, Oberst RD, et al.. Results of a longitudinal study of the prevalence of Escherichia coli O157:H7 on cow-calf farms. American Journal of Veterinary Research 2000 November; 61(11):1375-1379.

218 Roos R. Study finds no clear safety advantage for grass-fed beef. CIDRAP News July 20, 2010. Center for Infectious Disease Research and Policy at University of Minnesota.

219 Callaway TR, Carr MA, Edrington TS, et al.. Diet, Escherichia coli O157:H7, and cattle: a review after 10 years. Curr Issues Mol Biol. 2009;11(2):67-79.

220 Angelika Miko, Karin Pries, Sabine Haby, et al.. Assessment of Shiga Toxin-Producing Escherichia coli Isolates from Wildlife Meat as Potential Pathogens for Humans. Appl Environ Microbiol. 2009 October; 75(20): 6462–6470.

221 Renter DG, Sargeant JM, Hygnstorm SE, et al.. Escherichia coli O157:H7 in free-ranging deer in Nebraska. J Wildl Dis 2001 Oct; 37(4):755-60.

222 Rabatsky-Ehr T, Dingman D, Marcus R, et al.. Deer meat as the source of a Sporadic Case of Escherichia coli O157:H7 Infection, Connecticut. Emerg Infect Dis. 2002 May; 8(5): 525–527.

223 Keene WE, Sazie E, Kok J, et al.. An outbreak of Escherichia coli O157:H7 infections traced to jerky made from deer meat. JAMA. 1997 Apr 16;277(15):1229-31.

224 American Association of Feline Practitioners and Cornell Feline Health Center. Toxoplasmosis in cats. Cornell University College of Veterinary Medicine 2008 April 8. Retrieved September 17, 2013 from http://www.vet.cornell.edu/fhc/brochures/ toxo.html .

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Scavenging

Some anthropologists and advocates of “paleolithic diet” venture the hypothesis that early humans lived as scavengers, taking scraps of rotting meat, brains, bone marrow, and other leftovers from carcasses of animals killed by flesh-eating animals like cats and canines. Our present immune physiology casts doubt on this hypothesis.

If human ancestors had consumed much raw flesh or fat, particularly decaying leftovers from carnivore kills, they would have had frequent contact with the sometimes deadly flesh-borne pathogens, and this factor would have led to natural selection of humans with mutations providing adaptations to minimize the possibility of infection (e.g. higher production of stomach acid). Our relatively high susceptibility to these pathogens (compared to canines and felines) indicates that human ancestors did not have frequent exposure to the vectors for these infections, namely raw animal flesh.

Some people may argue that exposure to these pathogens favored the reproduction of human ancestors who learned how to cook flesh, thereby destroying pathogens. In this scenario, those who could learn to sterilize meat with fire did not need to evolve physiological or immunological mechanisms for preventing infection. I find this unconvincing, for several reasons.

First, proponents of the scavenging hypothesis suggest that scavenging played an important role in Australopithecus nutrition and evolution, but this occurred at least one million years before H. erectus had control of fire.225

Secondly, cooking meat does not necessarily eliminate the risk of infection. During food preparation, pathogenic bacteria spread to hands and surfaces contacted by the raw flesh. A review found that in modern kitchens more infection risk arises from either 1) cross-contamination occurring from use of the same cutting surface for raw meat and vegetables without intermediate cleaning, or 2) by spreading of pathogens via the kitchen environment, than from undercooking.226

Modern humans do not spontaneously understand or implement the level of hygiene required to prevent cross-contamination or clean the food preparation surfaces of these pathogens, namely, washing all affected surfaces with bleach (cleaning those surfaces with hot water and detergent does not reduce contamination).227

Third, according to the CDC, modern humans contract intestinal infections from eating cooked meat as well as raw (Table 7.1).

225 University of Toronto (2012, April 2). Evidence that human ancestors used fire one million years ago. ScienceDaily. Retrieved September 17, 2013, from http://www.sciencedaily.com/releases/2012/04/120402162548.htm

226 Luber P. Cross-contamination versus undercooking of poultry meat or eggs –which risks need to be managed first? In J Food Microbiol 2009 Aug 31;134(1-2):21-8.

227 Cogan TA, Bloomfield SF, Humphrey TJ. The effectiveness of hygiene procedures for prevention of cross-contamination from chicken carcasses in the domestic kitchen. Lett Appl Microbiol 1999 Nov;29(5):354-8.

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Further, people who handle raw flesh containing these pathogens also contract extra-intestinal (urinary tract) infections, even though they eat the flesh cooked.228

The ancient hominins purportedly dependent upon scavenging for sufficient nutrition had no control of fire, no knowledge of the necessary hygiene, no hot water on tap, no detergent, and no hypochlorite bleach. Although later species (e.g. H. erectus, early H. sapiens) had control of fire, they had no understanding of the hygiene or technology required for prevention of cross-contamination. Consequently, among any stone-age hominins dwelling in Africa and highly dependent on either raw or cooked animal flesh for survival until reproductive success, given sufficient time, natural selection would have favored individuals with high immunity to flesh-borne pathogens.

In short, our relatively high susceptibility to the pathogens borne by animal flesh suggests that we do not have natural adaptations to consuming or even contacting the foods which harbor them, i.e., raw meat, poultry, fish, eggs, and dairy products. Further, it also provides evidence that early human ancestors (whoever they were) probably did not significantly rely upon scavenged raw meat for sustenance and reproductive success. Finally, it provides evidence in support of the hypothesis that early humans did not regularly consume nutritionally significant amounts of meat until after they had control of fire.

Table 7.1: Top five pathogens causing foodborne illness in the U.S. in 2011 Microbe Typical source U.S. cases, 2011 Norovirus Shellfish 5,461,731 Salmonella, nontyphoidal Poultry, eggs, ground beef, pork 1,027,561 Clostridium perfringens Meat and poultry 965,958 Campylobacter spp. Poultry 845,024 Staphylococcus aureus Milk and cheese 241,148 Source: US Centers for Disease Control. http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html

Summary

Our stomach does not have any of the characteristics we would expect to find in an animal evolved from ancestors who relied upon handling or consumption of raw flesh to reach reproductive age for a couple of million years. On the other hand, it does have the characteristics we would expect to find in an animal whose ancestors primarily consumed a plant-based diet.

228 Vincent C, Boerlin P, Daignault D, et al.. Food Reservoir for Escherichia coli Causing Urinary Tract Infections. Emerg Infect Dis 2010 Jan;16(1):88-95.

98 – HUMAN NUTRITIONAL ADAPTATIONS 8: Small Intestine

“Comparative studies have revealed a close relationship between intestinal characteristics, the natural feral diet, and nutrient requirements (Buddington, 1996).”229

Specifically, animals biologically adapted to consuming animal flesh have short small intestines relative to torso length, while animals biologically adapted to primarily plant-based diets have long small intestines relative to torso length. For example, primarily or heavily frugivorous primates typically have a relatively long small intestine, whereas primarily faunivorous primates have a short, simple gut.230

Using a Darwinian thought process, this difference probably occurs as a result of natural selection exerted by at least two factors: 1) the caloric density of plants compared to animal tissues, and 2) the bacterial hazard associated with animal flesh compared to plants.

The edible portions of plants generally contain more water and fiber and have a lower energy (caloric) density compared to animal flesh, which contains a relatively high amount of fat and no fiber. The absorptive capacity of an intestine depends on its surface area, which increases linearly in proportion to its length. Thus, an animal specializing in eating plants generally needs a relatively long small intestine to provide adequate transit time and surface area for thorough extractions and assimilation of nutrients in plants.

Animal flesh almost inevitably delivers pathogens discussed in the previous section. The shorter the intestinal tract, the less time those pathogens spend in the gut, reducing the risk of gut infections. Further, since animal flesh contains no fiber and has a higher content of energy-rich fat than found in most fruits and vegetables, animals that specialize in eating flesh do not need to invest in a lengthy, metabolically expensive intestine with a large mucosal surface area.

These issues make it difficult for any animal to have a gut equally well-adapted to eating plants and animal flesh. An animal with an intestine long enough to extract nutrition from plant foods will have a high susceptibility to the pathogens delivered by flesh as well as a tendency to extract excess energy from the flesh; and an animal with an intestine short enough to minimize the danger of infections will not have enough intestinal length to extract adequate nutrition from raw plant foods.

229 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 6.

230 Fleagle JG. Primate Adaptation and Evolution. Academic Press, Sep 21, 1998. 293.

Comparative Intestinal Length

“Dogs with a body length of 0.75 m have an intestinal length averaging 4.5 m (small intestine = 3.9 m; large intestine = 0.6 m). Cats with a body length of 0.5 m have an intestinal length of approximately 2.1 m (small intestine = 1.7 m; large intestine = 0.4 m).”231

Thus, dogs and cats have small intestines measuring about 5 and 3 times their body length, respectively. Dogs represent the intestinal features of mesocarnivores, i.e. animals who obtain 50% to 70% of their food from animal flesh, the group to which leading ‘paleo diet’ advocates believe that humans belong.

In comparison, the non-ruminant, primarily herbivorous horse has a small intestine measuring about 70 feet in length,232 about 12 times the length of the torso.

Gray’s Anatomy states that in one hundred cases, the average length of the small intestine in the adult male was 22 feet 6 inches, and in the adult female 23 feet 4 inches: ranging from 31 feet 10 inches, to 15 feet 6 inches in the adult male.233

Gray’s Anatomy also states:

“The vertebral column is situated in the median line, as the posterior part of the trunk; its average length in the male is about 71 cm. Of this length the cervical part measures 12.5 cm., the thoracic about 28 cm., the lumbar 18 cm., and the sacrum and coccyx 12.5 cm. The female column is about 61 cm. in length.”234

The torso of the average male thus measures about 2 feet in length, and the average woman slightly less. Thus the human small intestine has a length approximately 10 to 11 times that of the torso. This makes the human torso:small intestine ratio more similar to that of the horse than to that of the cat or dog.

Among non-human primates, orangutans, chimps and gorillas have DNA sequences very similar to humans. By some measures, the chimps and orangutans have DNA sequences 99 and 97 percent identical, respectively, to human DNA sequences.235, 236 Based on this data, many scientists believe that

231 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition, op. cit. 5.

232 Ohio State University. Horse Nutrition. Bulletin 762-00.

233 Gray H, Anatomy of the Human Body, 20th Edition. Thoroughly Revised and Re-Edited by Warren H Lewis. Philadelphia: Lea and Febiger, 1918. New York: Bartleby.com, 2000. XI. Splanchnology. 2g. The Small Intestine. Note 168. Retrieved September 18, 2013 from http://www.bartleby.com/107/248.html

234 Ibid.

235 Prufer K, Munch K, Hellmann I, et al.. The bonobo genome compared with the chimpanzee and human genomes. Nature 2012 June 13 online. doi:10.1038/nature11128.

236 Spencer G. NIH-funded scientists publish orangutan genome sequence. NIH News 2011 January 26. Retrieved September 17, 2013 from http://www.nih.gov/news/health/jan2011/nhgri-26.htm

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humans and chimps both descended from a common ancestor about six million years ago, although some believe that morphological, biomechanical, and behavioral evidence points to us having a closer relationship to orangutans (see Appendix C). Regardless, since both chimps and orangutans eat a fruit- rich diet, the common ancestor probably ate a fruit-rich diet.

According to one source, an average chimpanzee has a body length of 75 cm (29 inches) and a small intestine length of about 400-425 cm.237 The 75 cm figure includes the head, not only the torso, and an adult chimpanzee has a height of 5.5 feet, similar to many humans.238, 239 Subtracting 25 cm for neck and head, the chimpanzee would have a torso length of about 50 cm. This would give the chimpanzee a small intestine only about eight times as long as her body; relative to body length, a small intestine:body length ratio more like that of the dog than our own.

This reflects the fact that the small intestine and colon form about 23 and 52 percent of the chimp’s total gut, respectively; while in humans they form, respectively, 67 and 17 percent of total gut.240 In primates, the chimp’s gut proportions occur in species with a significant dependence on hindgut fermentation of fibrous leaves, while proportions similar to the human’s occur in highly frugivorous species.

Among other primates, the spider monkey has similar gut proportions to humans. In spider monkeys and humans, the small intestine forms about 62241 and 67242 percent of the total gut, respectively, whereas in chimps the small intestine forms about 23 percent of the total.

While both the chimpanzee and the spider monkey eat fruit-rich diets, Milton describes the spider monkey thus:

“Spider monkeys...are extremely frugivorous. Over an annual cycle on Barro Colorado, 72% of daily feeding time was spent eating fruit and 80% wet weight of the annual diet of spider monkeys is believed to come from fruit pulp....In Colombia, over an annual cycle, spider monkeys spent an estimated 83% of total feeding time eating fruit and only 7% eating leaves...During the transition season on Barro Colorado, as noted above, a time of low fruit

237 Stevens CE and Hume ID. Comparative Physiology of the Vertebrate Digestive System. Cambridge University Press, Nov 25, 2004. 75.

238 Redmond I. The Primate Family Tree. Firefly Books Ltd, 2008. 163. Online, see: Jameson E. Pan Troglodytes (Chimpanzee). http://www.edjameson.com/Endangered%20Animals/pages/chimp2.htm

239 Nowak RM. Walker’s Primates of the World. Johns Hopkins University Press, 1999. 182

240 Milton K. Primate diets and gut morphology: Implications for Hominid Evolution. In Harris M (ed.), Food And Evolution: Toward a Theory of Human Food Habits, Temple University Press, 1989. 93-116.

241 Milton K. Food choice and digestive strategies of two sympatric primate species. The American Naturalist, April 1981; 117 (4): 496-505.

242 Milton K. Primate diets and gut morphology: Implications for Hominid Evolution, 1989, op. cit.: 93-116.

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availability, spider monkeys still spent a daily average of 60% of feeding time eating fruit by exploiting all apparent fruit sources in the habitat.”243

Since chimpanzees spend on average about 50 percent of their foraging time eating fibrous leafy vegetation, they take in a large amount of fiber and rely on hind-gut fermentation to extract energy from that fiber. The spider monkey, in contrast, spends about three-quarters of its time (on average) feeding on fruits, which have a lower fiber and higher digestible sugar content than green leaves, giving advantage to individuals who have a long small intestine capable of enzymatic digestion of sugars, starches, proteins, and fats found in ripe fleshy and dry fruits, and decreasing the utility of a lengthy colon for hindgut fermentation.

Table 8.1: Small intestine and colon proportions in four primate species

Species Small Intestine Colon Diet (Botanical Fruits: Non-fruit plant foods)

Howler monkey1 54 29 42:58

Chimpanzee2 23 52 48:523

Spider monkey1 62 18 80:20

Human2 67 18 ≥80:≤20

1. Milton K. Food choice and digestive strategies of two sympatric primate species. The American Naturalist, April 1981; 117 (4): 496-505. 2. Milton K. Primate diets and gut morphology: Implications for Hominid Evolution. In Harris M (ed.), Food And Evolution: Toward a Theory of Human Food Habits, Temple University Press, 1989. 93-116. 3. The Chimpanzee Species Survival Plan. Caring For Chimpanzees. http://www.lpzoosites.org/chimp-ssp/ chimpanzees.htm

The fact that humans and spider monkeys have similar small intestine proportions, both dissimilar to what we find in carnivores, suggests that the human small intestine proportion represents a heritable adaptation to an “extremely” frugivorous diet. Once again, here, frugivory refers to a diet consisting of the edible portions of any botanical fruits or nutritionally similar foods, which includes sweet fruits, legumes, nuts, seeds, cereal grains, and tubers.

Intestinal Immunity

A considerable body of research indicates that the human intestine requires specific plant-derived compounds, including fiber, vitamins, and some specific phytochemicals, to maintain homeostasis and barrier immunity.244 In contrast, intake of animal flesh appears to promote inflammatory bowel disease.

243 Milton K. Food choice etc. (1981), op. cit..

244 Tilg H. diet and Intestinal Immunity. NEJM 2012 Jan 12;366(2):181-183.

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For example, research has revealed that the small intestine’s resident intraepithelial lymphocytes (IELs), which provide protection against pathogenic bacteria, require indole-3-carbinol (I3C) for activation.245 In the absence of stimulation by I3C, intestinal IELs “fail to survive in their target tissues.”246 Without activated IELs, the intestine loses immune regulation of gut bacteria and develops the hallmarks of inflammatory bowel disease (IBD). Vegetables in the cabbage (Brassica) family provide I3C.

This suggests that humans have a dietary requirement for cruciferous vegetables to maintain intestinal health. Animals evolve a dietary dependence on foods only when they have a more-or-less continuous intake of those foods. This finding supports the hypothesis that human small intestine metabolism evolved a dependence on a plant-based diet.

In contrast, ingestion of animal flesh appears to promote IBD and restriction of animal food intake prevents relapse in affected individuals. In a European study of 67, 581 people, high animal protein intake was associated with a tripled risk of IBD.247 In Japan, the incidence of IBD was very strongly correlated to increased dietary intake of total fat (0.92) , animal fat (0.88), animal protein (0.91), and milk protein (0.92).248 In a Japanese study, IBD patients assigned to a semi-vegetarian diet had an almost three times greater remission rate than those who continued to eat flesh daily (94% vs. 33%, respectively).249

This evidence casts considerable doubt on the hypothesis that the human small intestine evolved to its present form to accommodate a dependence upon an animal-based diet. It supports the hypothesis that humans evolved to their present form by dependence on a cooked plant-based diet.

The Expensive Tissue Hypothesis

The Expensive Tissue Hypothesis of Aiello and Wheeler suggested that brain size in mammals negatively correlates with mass of digestive tract.250 Aiello and Wheeler reported that the human gut has only 60% of the mass expected for a primate of comparable size.251 They believed that the apparently reduced mass of the human gut combined with the larger human brain points to a human dependence on

245 Tilg H. diet and Intestinal Immunity. NEJM 2012 Jan 12;366(2):181-183.

246 Moens E, Veldhoen M. Epithelial barrier biology: good fences make good neighbors. Immunology 2012 Jan;135(1):1-8.

247 Jantchou P, Morois S, Clavel-Chapelon F, et al.. Animal protein intake and risk of inflammatory bowel disease: The E3N prospective study. Am J Gastroenterol 2010 Oct:105(10):2195-201.

248 Shoda R, Matsuedo K, Yamato S, Umeda N. Epidemiologic analysis of Crohn disease in Japan: increased dietary intake of n-6 polyunsaturated fatty acids and animal protein relates to the increased incidence of Crohn disease in Japan. Am J Clin Nutr 1996 May:63(5):741-745.

249 Chiba M, Abe T, Tsuda H, et al.. Lifestyle-related disease in Crohn’s disease: Relapse prevention by a semi-vegetarian diet. World J Gastroenterol 2010 May 28;16(20):2484-2495.

250 Aiello LC, Wheeler P. The Expensive-Tissue Hypothesis. Current Anthropology 1995 Apr; 36(2): 199-221.

251 Ibid.

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foods with a high energy density, and they suggested that animal flesh and cooked foods would be “obvious” candidates.

Navarrete et al. subjected the Expensive Tissue Hypothesis to an empirical test and “found that, controlling for fat-free body mass, brain size is not negatively correlated with the mass of the digestive tract or any other expensive organ, thus refuting the expensive-tissue hypothesis.”252

“Contrary to the predictions of the expensive-tissue hypothesis, we found no negative correlations between the relative size of the brain and the digestive tract, other expensive organs or their combined sum among mammals or within non-human primates, controlling for fat-free body mass, even though statistical power was sufficient to detect these negative correlations if they existed (see Table 1). We also did not find any trade-offs among other expensive organs (Fig. 1). These results therefore refute the expensive-tissue hypothesis as a general principle to explain the interspecific variation of relative brain size in mammals. In our view, this finding reduces the plausibility of the argument that human encephalization was made possible by a reduction of the digestive tract1,5.” [Italic added]

Navarrete et al. indicate that the efficiency of human bipedal locomotion dramatically reduces the energy demands of movement thus allowing the system to invest in other energy-intensive organs, such as the brain.

“One likely trade-off could be found between brain size and the costs of locomotion. The efficient form of bipedal locomotion that arose with the transition from australopithecines to early Homo27 could have led to major reductions in energy expenditure in two ways. On one hand, its low costs in comparison with the climbing and quadrupedal locomotion of nonhuman apes28 should have lowered daily energy expenditure on locomotion,7 and on the other hand, bipedalism may reduce the effect of increased weight due to adipose depots on the energy costs of locomotion (Supplementary Information 3.7).”253

However, they emphasize that multiple factors may have coincided in human evolution to reduce total non-brain energy requirements sufficiently to make it possible for humans to evolve a relatively compact gut and yet extract adequate energy from food to support an expanded brain.

“In sum, we do not claim unique processes operating exclusively in human evolution. All these processes are known to operate among mammals in general. We propose that during human evolution improved diet quality, allomaternal subsidies, cognitive buffering, reduced locomotion costs and reduced allocation to production all operated simultaneously, thus enabling the extraordinary brain enlargement in our lineage.”254

252 Navarrete A, van Shaik CP, Isler K. Energetics and the evolution of human brain size. Nature 2011 Dec 1; 480: 91.

253 Ibid.

254 Ibid.

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Of interest, neither Aiello and Wheeler nor Navarette et al. account for the contribution of colonic microbial fiber fermentation to human energy economy. In Chapter 10, I will discuss evidence that suggests that humans consuming a diet sufficiently high in fiber (100-150 g/d) would derive enough energy from colonic microbial fiber fermentation to significantly offset the energy requirements of the brain.

While “improved diet quality” may have contributed to both gut reduction and brain enlargement, we have no evidence from non-human lineages that increased reliance on animal flesh supports both gut reduction and brain enlargement. While carnivores compared to herbivores have relatively reduced gut size, they do not have relatively large brains or encephalization quotients (EQ, Chapter 17). Further, humans do not have the ability to depend on animal protein as the primary source of the large amount of glucose required for ongoing brain metabolism; high protein diets have toxic effects on humans, particularly during pregnancy (Chapter 11). Finally, as discussed in Chapter 1, it seems likely that cooking of starchy plant foods would have increased the dietary energy intake of early humans much more than eating an animal-based diet. Therefore, it seems most likely that cooking of starchy foods provided the increased dietary energy density and glucose intake required to allow the lineage to increase body and brain size while keeping the smaller gut size of the earlier, smaller-bodied members of the lineage (pre-Homo).

The similarity between the spider monkey and human guts, combined with the relatively small size of the human gut, suggests the possibility that humans descended from a strongly frugivorous ancestor having an approximately 40% smaller body size than modern humans. Hypothetically, the discovery of control of fire allowed this ancestor to extract more energy from plant foods, which then made it possible for the body and brain size to increase while retaining the same gut size and proportions.

A Plant Food Ceiling? Pandas, and Fiber in Wild Versus Cultivated Plants

As noted in Chapter 5, Ben-Dor et al. argued that modern humans have a “maximum long term plant food ceiling” of 32% of energy from raw plants largely due to presumed limitations imposed by human dentition and gut mass.255 Ben-Dor et al. contend that “pre-agriculture highly fibrous plant foods” would deliver an “avalanche of fiber” impossible for the human dentition and gut to process. This raises two questions: Do “pre-agriculture plant foods” have a higher fiber content than cultivated plant foods of the same types? and Do we have evidence for a ceiling of fiber intake in either ancient or modern humans?

Before delving into those questions, I would like to suggest that pandas may present a challenge to any one who thinks that any particular genetic, dental, or gut structure imposes a strict raw plant-food ceiling on the human species. Li et al. sequenced the panda genome and reported:

255 Ben-Dor et al.. Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

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“Of interest, our analysis of genes potentially involved in the evolution of the panda’s reliance on bamboo in its diet showed that the panda seems to have maintained the genetic requirements for being purely carnivorous even though its diet is primarily herbivorous.”256

As discussed in Chapter 1, pandas have typical short, simple, and smooth carnivore intestines, with no fermentation chambers and relatively little surface area compared to the guts of plant-eaters and humans, yet they sustain themselves, albeit somewhat precariously, on a diet of very highly fibrous raw bamboo stalks. Since the pandas can sustain themselves on a very high fiber raw plant food diet despite lacking any significant genetic or gastrointestinal adaptation to a food as fibrous as bamboo stalks, it seems unlikely that prehistoric or modern humans having a genetic and gastrointestinal constitution inherited from strongly frugifolivorous ancestors would face any rigid plant food ceiling restricting their ability to subsist on botanical fruits and vegetables.

Table 7.2 shows the fiber content of 38 commonly consumed cultivated vegetables, fruits and nuts. These 38 have a mean fiber content of 4.3 g/100 g and 5.2 g/100 kcal. Cooking does not change the fiber content of foods.

Table 8.2: Fiber content of 38 cultivated raw botanical fruits and vegetables

Food groups Fiber (g/ 100 g) Fiber (g/ 100 kcal)

Fruits, sweet1 2.4 4.1

Berries2 3.4 7.3

Nuts3 9.4 1.7

Seeds4 9.0 1.6

Leaves, stems, and flowers5 2.0 7.0

Bulbs, roots and tubers6 3.0 5.1

Legumes7 3.5 7.1

Fruits, savory8 2.0 7.7

Mean 4.3 5.2

1. Equal parts apple, banana, mango, orange, pear. 2. Equal parts blackberry, blueberry, grape, raspberry, strawberry. 3. Equal parts almonds, coconut, hazelnut, pecan, walnut. 4. Equal parts hemp, pumpkin, sesame, and sunflower seeds. 5. Equal parts kale, broccoli, asparagus, celery, leeks 6. Equal parts carrot, sweet potato, onion, water chestnut, parsnip, rutabaga. 7. Equal parts green peas, green snap beans, snow peas. 8. Equal parts cucumber, eggplant, okra, tomato, sweet red pepper.

Data source: USDA Food Nutrient Database.

256 Li et al.. The sequence and de novo assembly of the giant panda genome. Nature 2010 Jan 21;463:311-17.

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According to Cordain et al.,257 optimal foraging theory suggests that foragers would favor the plant foods that return the most food energy for each unit of time invested in foraging. This would lead them to favor sugar-rich fruits and berries, oil-rich nuts and seeds, and starch-rich underground storage structures (tubers, roots, and bulbs). Among the modern cultivars selected for Table 7.2, these groups each have mean fiber contents of 2.4, 3.4, 9.4, 9.0, and 3.0 g/100 g, respectively. The plants with the highest energy density, nuts and seeds, have the highest fiber contents. The five groups have a mean of 5.4 g fiber/ 100 g. This all suggests that optimal foraging from this selection of cultivated plant foods would lead to a higher fiber intake than suboptimal foraging.

Eaton et al. reported that 44 wild plant foods (vegetables, fruits, beans, nuts, and seeds) consumed by the San, Hadza, Tasaday, and Australian Aborigines had a mean fiber content of 3.12 g/100 g (standard deviation 0.62).258 According to that figure, wild plant foods may have a lower fiber content than the 38 foods listed in Table 7.2!

Brand-Miller and Holt reported that 829 wild plant foods consumed by Australian Aborigines had a mean fiber content of 11 g/100 g with a standard deviation of 11.259 The standard deviation indicates that some Australian Aborigine (AA) wild plant foods have very little fiber, others more. Given that humans have preferences, it is unlikely that native Australian foragers consumed equal portions of all 829 plant foods in their habitat. For example, the data set may include some very highly fibrous plant foods that Aborigines only use as food when they have no other choices, and some relatively low fiber plants that they consume on a regular basis. Brand-Miller and Holt themselves admit this in their own comments on the records from which they drew their data set:

“However, the relative contribution of individual foods is difficult to determine from the records.”260

“Of the plant foods listed, most appear to have been eaten infrequently, with only a few staples contributing significantly to the diet. In desert areas some plant species were important staples, but this desert existence may have been unnatural, the result of forced exile from their traditional lands. Nor did Aborigines eat everything that was edible.”261

257 Cordain et al.. Plant-animal subsistence etc. Am J Clin Nutr 2000 Mar;71(3):682-692.

258 Eaton and Konner. Paleolithic Nutrition. NEJM 1985 Jan 31;312(5):283-289.

259 Brand-Miller J, Holt SHA. Australian Aboriginal plant foods: a consideration of their nutritional composition and health implications. Nutrition Research Reviews 1998;11:5-23.

260 Ibid., 6.

261 Ibid., 6.

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“However, we do not know to what extent AA exploited all the species available or limited themselves to an optimal foraging strategy based on relatively few species.”262

Hence, a mean fiber content based on a data base of this sort could overestimate the mean fiber content of plant foods they most habitually consumed. Without any data indicating which of these 829 plant foods Australian Aborigines consumed as regular staples, and which served only as fallback foods in lean times, we can’t conclude that they regularly consumed plants having a fiber content of 11 g/100 g.

Clearly, Brand-Miller and Holt recognized that their data does not permit any firm conclusions about the fiber content of the pre-agriculture plant foods that either contemporary or Paleolithic foragers habitually consumed. Surprisingly, despite this, and without making any attempt to decide which of those 829 foods AAs used as staples and which they rarely or never consumed, Brand-Miller and Holt used their 11 g/100 g figure to estimate the fiber intake of both AAs and other Paleolithic humans!

The two data sets present an interesting dilemma. If the data set used by Eaton et al. more accurately represents the fiber content of the “pre-agriculture plant foods” that both modern and Paleolithic foragers preferred and habitually consumed, then they have a mean fiber content lower than the 38 commonly consumed cultivars I listed in Table 7.2. On the other hand, in the unlikely event that the Australian data set used by Brand-Miller and Holt represents the fiber content of the “preagriculture plant foods” habitually preferred and consumed by our African ancestors, then those plant foods had a mean fiber content nearly three times that of the 38 commonly consumed cultivars listed in Table 7.2. Clearly, the data on the fiber content of wild plant foods consumed by contemporary foragers lacks sufficient precision to permit convincing conclusions about how much fiber prehistoric humans consumed.

Beyond this, we have the question of what constitutes a “pre-agriculture plant food.” Brand-Miller and Holt state:

“AA did not practise agriculture, although they did modify the environment to increase food production by innovated methods (i.e. ‘fire stick’ farming) and the germination of many favoured plants was assisted by regular burning of discrete areas of land.”263

While these actions may not fit Brand-Miller and Holt’s conception of agriculture, they illustrate that foraging humans have acted as agents of natural selection and therefore probably have influenced the characteristics and composition of the foods they have selected throughout their evolution. Similarly, Bailey et al. have stated:

“The present diverse composition and distribution of plants and animals in the [African] rain forest is the result of introduction of exotic species, the creation of new habitats and the manipulation by the forest-dwelling people for thousands of years. No areas are what most

262 Ibid., 22.

263 Brand-Miller and Holt. Australian Aboriginal plant foods. Nutrition Research Reviews 1998;11:5-23.21.

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proposals and reports refer to as ‘pristine,’ ‘untouched,’ ‘primary,’ or ‘mature’ forest. Present-day biological diversity exists in central Africa, not in spite of human habitation but because of it.”264

Thus, we have reason to believe that “pre-agriculture plant foods” have co-evolved with humans as a result of humans making their natural (i.e. spontaneous) selections and taking deliberate actions to favor some plants over others. People who accept Darwinian evolution must therefore integrate into their genesis account the coevolution of humans and the plants with which they had a symbiotic relationship. In such an account, since coevolution probably did happen, humans probably did not have to adapt to, or abandon, any fixed “pre-agricultural highly fibrous plant foods” because any plant foods that humans naturally selected would probably have evolved in composition as humans evolved in their natural selections.

Eaton et al. reported that the 44 wild plant foods they included in their data set (averaging 3.12 g fiber/ 100 g) also have a mean energy density of 1.29 kcal/g.265 Ben-Dor et al. believe that H. erectus had an energy requirement of 2705 kcal but did not have the dental or digestive ability to consume more than 1014 kcal from plants.266 Using Eaton et al.’s data on the fiber content of 44 wild plants (3.12 g/ 100 g) we can calculate that at Ben-Dor et al.’s “plant food ceiling” H. erectus would have consumed some 786 g of plants that provided 25 g fiber per day. Notably, this falls short of the 38 g minimally Adequate Intake for dietary fiber for modern adult males set by the National Academy of Science’s Food and Nutrition Board on the basis of known benefits of fiber-rich diets.267 Further, modern humans can easily consume 786 g of raw plant foods in a day. For example, 1 medium banana, 1 medium apple, 1 naval orange, 23 almonds, 1 cup of peas, and 1 cup of blueberries weighs 761 g, supplies 634 kcal and 25 g fiber, and can easily be consumed in less than one-half hour.

If H. erectus obtained all of his required 2705 kcal entirely from Eaton et al.’s 44 wild plants he would consume 2096 g (2.1 kg) of plant food daily, resulting in a fiber intake of 65 g per day. Does this identify the theoretical “avalanche of fiber” and mark the “plant food ceiling”? No. Agricultural people in Uganda consumed as much as 150 g fiber per day and maintained gastrointestinal health superior to people consuming only 25 g of fiber per day.268

On the other hand, if male H. erectus had to select from plants having the mean fiber and energy contents that Brand-Miller and Holt found for their sundry collection of 829 edible wild plants found in

264 Dembner SA. Forest peoples in the central African rain forest: focus on the pygmies. Adapted from two papers by Bailey RC, Bahuchet S, Hewlett B, Dyson M., published in: Cleaver K, Munasinghe M, Dyson M, Egli N, et al., eds. Conservation of West and central African rainforests. World Bank, 1992. FAO Corporate Document Repository. Retrieved September 17, 2013 from http://www.fao.org/docrep/w1033e/w1033e03.htm

265 Eaton and Konner. Paleolithic Nutrition. NEJM 1985 Jan 31;312(5):283-289

266 Ben-Dor et al.. Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

267 Food and Nutrition Board of the Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients). National Academies Press, 2005. 339-421.

268 Jenkins DJA, Kendall CWC, Popovich DG, et al.. Effect of a Very-High-Fiber Vegetable, Fruit, and Nut Diet on Serum Lipids and Colonic Function. Metabolism 2001 April;50(4):494-503.

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Australia (11 g/100 g and 1.7 kcal/g, respectively), then at the “plant food ceiling” suggested by Ben- Dor et al., he consumed 596 g of plant foods supplying 66 g fiber. As shown by Ugandan farmers, this very certainly does not constitute a plant food or fiber ceiling for humans. If instead H. erectus obtained all of his 2705 kcal from these foods, he would have eaten 1.6 kg of plant foods and 176 g fiber daily, only 26 g more than the modern agriculturalists of Uganda. As we shall see, we have no evidence that either of these surpasses any ceiling for humans’ intake of plant food with its constituent fiber.

Brand-Miller and Holt performed their own calculations and wrote that if AAs (or Paleolithic H. erectus) ate a diet having a plant:animal weight ratio of 80:20, then

“...they ate 1.4 kg plant food/d, such a large amount that it seems unlikely to have been the case. Much of each day would have been devoted to the simple act of eating.”269

Brand-Miller and Holt seem unaware that modern people habitually consume 1.4 kg of plant foods in a day, in a very short period of time. Lawton et al. found that subjects consumed a mean of 432 g of food in a single ad libitum low-energy density meal (64% carbohydrate, <25% fat, 677 kcal) and 438 g of food when given a high energy density (65% fat, 1336 kcal) meal.270 If a person consumed three such meals daily, s/he would ingest 1.3 kg of food, without devoting “much of each day” to it. Koebnick et al. reported that a large group of German raw food dieters consumed an average of 1.8 kg raw fruits and vegetables daily.271 In two different studies by Jenkins et al., people consumed 2 to 5 kg of whole plant foods in a day for a week at a time (see below). I have habitually consumed more than 2 kg of food daily for more than 15 years. On the YouTube channel “Plant Based Guerilla” [sic] you can witness a man consuming 30 bananas–approximately 3.5 kg of food–in just 20 minutes.272

Brand-Miller and Holt calculated that if AA (or, presumably, any stone age human species) had gotten 80% energy from plants, they would have consumed 160 g fiber/d. They suggested that such a high fiber intake from fruits and vegetables would have detrimental effects on the absorption of macro- and micronutrients.273 Since according to Darwinian evolutionary accounts humans descended from a lineage of primates that obtained virtually 100% of their nutrition from fruits and vegetables for several hundred thousand generations, and modern humans have greater than 97% genetic similarity to extant apes who live primarily on fruits and vegetables, a Darwinian account would presume that humans retain digestive adaptations to diets rich in fibrous fruits and vegetables until proven otherwise.

269 Brand-Miller and Holt. Australian Aboriginal plant foods. Nutr Res Rev 1998;11:5-23. 20.

270 Lawton CL, Burley VJ, Wales JK, Blundell JE. Dietary fat and appetite control in obese subjects: weak effects on satiation and satiety. Int J Obesity 1993;17:410-416.

271 Koebnick C, Garcia AL, Dagnelie PC, et al.. Long-term Consumption of a Raw Food Diet etc. J Nutr 2005 Oct 1;135(10): 2372-2378. Table 2.

272 Plant Based Guerilla. Man eats 30 bananas in one sitting. Published Oct 6, 2013. Retrieved October 15, 2013 from https:// www.youtube.com/watch?v=QCeeWeKRwVs

273 Brand-Miller and Holt, op. cit., 21.

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Further, although the fiber present in fruits and vegetables may reduce absorption of some nutrients, a diet of fruits and vegetables can still supply more than adequate levels of both macro- and micronutrients because these foods have such a high nutrient density. For example, Brand-Miller and Holt state that the plant foods in their data set provide a mean of 4 mg zinc and 15 mg iron per 100 g.274 As already discussed above, they also state that people consuming 80% of energy from these plants would have consumed 1.4 kg plant foods daily, which ergo would have provided 56 mg zinc and 210 mg iron. Pregnant women have the highest daily requirements for these two nutrients: 13 mg and 27 mg, respectively. Consequently, if they ate 1.4 kg daily of AA plant foods (equal portions of the 829 in the Brand-Miller and Holt data set) they would obtain 4 times and 8 times their zinc and iron requirements, respectively. Thus, even if the fiber in those plants rendered unavailable 77% of their zinc and 87% of their iron contents, pregnant women would still obtain sufficient iron and zinc from them. However, I have not seen anyone provide any evidence that dietary fibers have an impact of this magnitude in any wild primate species or humans.

In addition, fruits and vegetables contain other nutrients, including protein and citric and ascorbic acids, which enhance mineral absorption, countering effects of fiber. According to Brand-Miller and Holt, the 829 foods in their data base have mean protein and ascorbic acid contents of 6 g and 25 mg per 100 g. Hence, 1.4 kg composed of equal portions of the 829 foods would supply 84 g protein and 350 mg ascorbic acid, respectively 1.5 and 5.8 times the current recommended daily intakes for a 68 kg individual.

Brand-Miller and Holt wrote their opinion in 1998. Ten years earlier, in 1988, Kelsay et al. reported finding no difference in mineral balance over 6 weeks in humans fed either a low fiber diet or one containing 0.9 to 1.1 kg fresh fruits and vegetables daily, including high oxalate spinach on alternating days.275 In 1991, Torre et al. reviewed evidence on the effect of fiber on nutrient metabolism and concluded that if increases in vegetable protein, ascorbic and citric acids accompany increases in fiber intake, as would occur with large intakes of fruits and vegetables, the increased fiber intake will have no detrimental effect on mineral balances.276 I wonder why Brand-Miller and Holt did not check the research literature relevant to their thesis.

In 2011, Ben-Dor et al. again suggested that very high intakes of dietary fiber and oxalates may impair nutritional status in humans.277 Apparently they did not read Kelsay et al., Torre et al., nor the Food and Nutrition Board’s 2005 review of evidence for adverse effects of dietary fiber, wherein:

274 Ibid. 14.

275 Kelsay et al.. Mineral Balances of Men Fed a Diet Containing Fiber in Fruits and Vegetables and Oxalic Acid in Spinach for Six Weeks. J Nutr 1988 Oct 1;118(10):1197-1204.

276 Torre et al.. Effects of dietary fiber and phytic acid on mineral availability. Crit Rev Food Sci Nutr 1991;30(1)1-22. Abstract.

277 Ben-Dor et al., Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

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“It is concluded that as part of an overall healthy diet, a high intake of Dietary Fiber will not produce significant deleterious effects in healthy people. Therefore, a Tolerable Upper Intake Level (UL) is not set for Dietary Fiber.”278

Hence, the idea that a high intake of fruits and vegetables would cause nutrient imbalances in humans has lacked basic Darwinian theoretical and evidential support for more than 25 years. Nevertheless, proponents of “paleolithic,” “traditional,” and low-carbohydrate diets continue to drum up fears of fiber and talk about “plant-food ceilings.”

Brand-Miller and Holt calculated that a preagricultural diet providing 65% of energy from plant foods would supply 130 g of dietary fiber. They note that although this “seems exceptional by today’s standards,”

“...the archaeological evidence based on coprolite analysis suggests that such large amounts of fibre were typical in other parts of the world (Kliks, 1978).”

If stone age people had “typical” intakes of 130 g fiber/d, and the food had Brand-Miller and Holt’s mean of 11% fiber, then this implies a typical plant food intake of 1.2 kg providing 2040 kcal, or at least 75% of the energy requirements of an active stone age human. Yet as noted above, Brand-Miller and Holt contended that this level of plant food intake is “unlikely” for a forager because “much of the day would be devoted to the simple act of eating.” I strain to understand how Brand-Miller and Holt could label such intakes of total plant foods and fiber both unlikely and typical.

Further, the coprolites may underestimate the contribution of plant foods to early human energy requirements, because they would not contain residues of fibers fermented to SCFAs. In Chapter 10 I will discuss evidence that indicates that fermentation of fibers may contribute very significantly to energy requirements in humans consuming diets providing more than 100 g of fiber daily.

Worthy of note, if Eaton et al. have the more correct calculation of the mean fiber intake of “preagricultural plant foods” (~3%) then the coprolites predict a plant food intake of 4.3 kg/d. Not even this surpasses a plant-food ceiling for humans, because, as I will discuss below, Jenkins et al. showed that people can consume more than 5.0 kg of whole plant foods daily.

The coprolite data also contradicts Ben-Dor et al.’s claim that the plant food ceiling for humans lies at 32% of energy. As shown above, even if we use 11% fiber as representative of the mean for uncultivated plant foods (more than double the mean for the 38 cultivars in Table 7.2), and those who left the coprolites had only gotten 32% of their energy from plants, their diet would have contained only about 70 g fiber. Yet the coprolites show intakes in the range of 130 g/d, which as already stated would suggest that those who left the piles obtained at least 75% of their energy from fiber-rich plants. Apparently, some piles of fossilized feces cast serious doubt on the calculations of Ben-Dor et al..

278 Food and Nutrition Board, Dietary Reference Intakes for Energy, etc, National Academies Press, 2005. 395.

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To summarize the main points in this section:

1) We have no clear data on the fiber content of plant foods habitually consumed by stone age or contemporary foraging people; according to one data set used by proponents of stone age diets for modern humans, those plants may have even had on average less fiber than the 38 cultivars listed in Table 7.2. 2) Proponents of the idea that stone age humans ate meat-based diets low in whole plants have themselves cited coprolite evidence that suggests that prehistoric people had very high fiber and plant food intakes. 3) Darwinian theory does not support the idea that early humans would suffer harm from diets very high in fruits and vegetables; since by this theory humans have descended from frugifolivorous ancestors, and modern humans have a high level of genetic similarity to that of other extant apes, it guides us to presume that we have retained a high level of adaptation to the frugifolivorous diet. 4) Finally, empirical data does not support the claim that high intakes of fruits and vegetables and their constituent fiber impairs human nutrition. The Food and Nutrition Board of the National Academies of Science has stated that we have no evidence to support any claim for a ceiling for or adverse effects of very high dietary fiber intake from fruits and vegetables in humans.

Let us now consider the quality of other evidence frequently cited in support of the hypothesis that the stone age human gut could not have extracted adequate energy from a diet composed primarily of raw fruits and vegetables because of its supposedly excessive bulk and fiber. Please note that I am not advocating a diet composed exclusively of raw foods, but only discussing the merits of claims that early humans (H. erectus/ergaster) could not have lived on diets composed largely or entirely of raw fruits and vegetables.

Plant Food Ceiling Part 2: Modern Raw Dieters

As noted above, Ben-Dor et al. argued that H. erectus had and modern humans have a “maximum long term plant food ceiling” of 38% and 32% of energy from raw plants, respectively, due to the limitations imposed by human dentition and gut mass.279

This is an empirical claim requiring experimental test. We can’t perform experimental tests on any extinct human species. Nor can we make any certain claims about the availability of plant-foods to extinct human species because, as stated by Ungar, “we cannot know the full complement of foods available in the past, let alone infer their material properties.”280 Therefore, we can only test this claim by performing experiments wherein we restrict humans to consumption of those plant foods that are edible raw (botanical fruits and vegetables) and observe whether these humans can obtain from such a diet adequate energy. If so, this refutes the claim that modern humans are biologically dependent on

279 Ben-Dor et al., Man the Fat Hunter, PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

280 Ungar P. Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution 2004:46:605-622.

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animal flesh or cooked foods, and casts doubt on claims that ancient hominins could not have lived on raw plant foods.

In an attempt to provide empirical support for their claim, Ben-Dor et al. wrote:

“A significant contribution to the understanding of the physiological consequences of consuming a raw, largely plant-based diet was made by Wrangham et al. [17], [18]. A physiological limitation seems to be indicated by the poor health status of present-day dieters who base their nutrition on raw foods, manifested in sub-fecundity and amenorrhea [17], [18]. Presumably this limitation would have been markedly more acute if pre-agriculture highly fibrous plant foods were to be consumed.” 281

Of seven studies282, 283, 284, 285, 286, 287,288 investigating the health status of people eating raw food diets, only one “questionnaire survey” of German raw food dieters by Koebnick et al.289 attempts to address the issues of body mass, menstruation and fecundity. Hence, Wrangham et al.290 primarily based their conclusion that present-day raw food dieters are sub-fecund and amenorrheic on a single “questionnaire survey.” Such a survey falls far short of the requirements for determining whether a “raw food ceiling” or “plant-food ceiling” exists for modern humans, since a survey can only determine what people habitually do, and can never determine what they can do.

For example, the U.S. Centers for Disease Control found by survey that about 53% of U.S. people surveyed do not engage in vigorous activity for 75 to 150 minutes or moderate activity for 150-300 minutes each week. Such data does not permit the conclusion that people can’t engage in that level of

281 Ben-Dor et al., op. cit.

282 Rauma AL, Torronen R, Hanninen O, et al.. Antioxidant status in long-term adherents to a strict uncooked vegan diet. Am J Clin Nutr 1995:62:1221-1227.

283 Douglass J. M., Rasgon I. M., Fleiss P. M., Schmidt R. D., Peters S. N., Abelmann E. A. Effects of a raw food diet on hypertension and obesity. South Med. J. 1985;78:841-844.

284 Ling WH, Hanninen O. Shifting from a conventional diet to an uncooked vegan diet reversibly alters fecal hydrolytic activities in humans. J. Nutr. 1992;122:924-930.

285 Donaldson M. S. Metabolic vitamin B12 status on a mostly raw vegan diet with follow-up using tablets, nutritional yeast, or probiotic supplements. Ann. Nutr. Metab. 2000;44:229-234.

286 Agren JJ, Tormala ML, Nenonen MT, Hanninen OO. Fatty acid composition of erythrocyte, platelet, and serum lipids in strict vegans. Lipids. 1995;30:365-369.

287 Fontana L, Shew JL, Holoszy JO, Villareal DT. Low bone mass in subjects on a long-term raw vegetarian diet. Arch Intern Med 2005 Mar 28;165(6):684-9.

288 Koebnick C, Strassner C, Hoffmann I, Leitzmann C. Consequences of a long-term raw food diet on body weight and menstruation: results of a questionnaire survey. Ann Nutr Metab 1999;43:69-79.

289 Ibid.

290 Wrangham RW, Jones JH, Laden G, Pilbeam D, et al.. The raw and the stolen: cooking and the ecology of human origins. Current Anthropology 1999;40(5):567-594.

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activity, only that they don’t. People have many reasons for not engaging in physical activity, and some deliberately avoid it. References to the habits of contemporary hunter-gatherers have the same weakness. The fact that these people eat meat doesn’t tell us that they can’t live or maintain health without eating meat, it only indicates that they do eat meat. They might do this as a choice (just as many people choose to eat donuts), or because they inhabit regions (e.g. the Arctic) where no other choice is possible. The fact that people choose something never provides evidence that their choice is the only one possible or the best for their health.

Nevertheless, this frequently cited study deserves some attention because it reveals some interesting findings pertinent to the claim that stone age humans couldn’t sustain health on diets composed of raw fruits and vegetables.

Koebnick et al.291 reported that “complete data sets were evaluated of 513 persons (216 men and 297 women).” However, they also state that “The diet groups were classified as meat eaters (n=253), vegetarians (n=184) and vegans (n=135)”, amounting to only 472 subjects. Koebnick et al. do not explain why 41 subjects having “complete data sets” were excluded in the diet groupings.

According to Koebnick et al., the subjects consumed an average of 90% of their diet as raw food, primarily fruits and vegetables, and the average duration of raw diet was about 3.7 years. As stated more than half of the subjects of this study ate meat. They did not report what proportion of the raw food consumed by the meat-eating subjects consisted of raw meat.

Koebnick et al. provided no detailed information about the habitual food choices or energy intakes of any of the subjects, but noted that 49% of the subjects engaged in regular fasting, ranging in duration from one day to several weeks “at least once per year.” Since fasting restricts energy intake, the absence of clear data on frequency and duration of fasting and its relation to the various degrees of raw food consumption, body weight and menstruation confounds the results, making it impossible to make any reliable conclusions about the energy sufficiency of a diet based on raw foods.

The mean BMIs for men and women in this study were 20.7 and 20.1 (Table 8.3), with little deviation from the mean. Since BMI is only a ratio of height to weight, it does not reliably indicate body composition or health risks. One can have an “underweight” BMI yet have a high body fat level (via replacement of lean mass with fat mass) and one can have an “overweight” BMI yet have a low body fat level (as found in athletes with extraordinary muscle mass). Nevertheless, any BMI in the range 18.5 to 24.9 is defined as normal; hence, these raw food dieters had, on average, normal BMIs.

Further, 78% of males and 70% of females had normal BMIs. Among those eating 90-99% raw diets, 74% had normal BMI, and among those eating 100% raw, 67% had normal BMIs. In all groups of raw dieters, ranging from 70% to 100% raw diet, no less than 67% of subjects had normal BMI. Also, among subjects eating 80-89% or 90-99% raw diet, greater proportions of subjects (79% and 74%,

291 Koebnick et al.. Consequences of a long-term raw food diet on body weight and menstruation: results of a questionnaire survey. Ann Nutr Metab 1999;43:69-79.

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respectively) had normal BMI than among subjects eating only 70-79% raw diets (70%), contradicting the hypothesis that increasing the proportion of raw food in the diet makes body weight maintenance more difficult. The average BMI in the 90-99% raw group was above 20.0, and in the 100% raw group, above 19.0; both in the normal range. Although the latter falls on the low side, we already noted that in this study the subjects’ body mass displayed very little deviation from the mean.

Table 8.3: Classification of BMI and distribution of relative body weight in relation to gender and amount of raw food consumed (%), from Koebnick et al. 1999.

Classification BMI kg/ male female 70-79% 80-89% 90-99% 100% m2

Severe underweight <16 0.4 1.5 1.3 0.8 0.8 1.9

Moderate underweight 16.0-16.9 2.2 4.1 2.5 0.8 3.4 6.8

Mild underweight 17.0-18.4 12.1 19.3 11.4 11.9 17.8 22.3

Normal weight 18.5-24.9 78.3 69.6 69.6 79.4 73.5 67.0

Overweight 25.0-29.9 6.1 3.8 12.7 4.0 4.2 1.0

Obesity 30.0-39.9 0.0 1.2 2.5 0.8 0.4 0.0

Severe obesity ≥40.0 0.0 0.0 0.0 0.0 0.0 0.0

Missing data 0.9 0.6 0.0 2.4 0.0 1.0

n 230.0 342.0 79.0 126.0 264.0 103.0

Source: Koebnick et al.. Consequences of a long-term raw food diet on body weight and menstruation: results of a questionnaire survey. Ann Nutr Metab 1999;43:69-79.

Koebnick et al. also reported that vegans had no significantly higher odds of underweight or amenorrhea than vegetarians or meat eaters. Far from showing that no human can maintain a normal weight on a raw plant-based diet, this study found that, regardless of animal food intake, more than two thirds of raw dieters have a normal BMI, despite engaging in an unknown frequency and duration of fasting.

If as Ben-Dor et al. and others propose, plant foods impose some special energy intake ceiling in comparison to animal foods, and humans eating raw diets must eat animal flesh to maintain body weight and fertility, then vegans should have had a greater risk of underweight and amenorrhea than meat eaters, but they did not.

Koebnick et al. also found that among these subjects “the BMI increased slowly with the duration of raw food diet consumption.”292 This suggests that modern humans raised on a diet consisting largely of cooked foods and low in fresh fruits and vegetables may go through a learning and adaptation period when adopting a raw food diet; during which time they figure out how to eat to maintain weight. For

292 Koebnick et al., Ann Nutr Metab 1999;43:69-79. 74.

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people eating plant-based diets, this would include learning what proportion of the diet to devote to foods that vary in energy density from less than 0.2 kcal/g (e.g. lettuce) to more than 5.0 kcal/g (seeds and nuts).

Whether a long-term raw food dieter becomes underweight or not depends dramatically on how she chooses to compose her diet and how often she engages in fasting. The energy density of a raw diet will vary widely depending on what foods are used as staples. Two kilograms each of raw lettuce, bananas, dates, or almonds will provide approximately 340, 1800, 5500, and 11,000 kcal, respectively. Surprisingly, Koebnick et al. do not even mention these basic facts in their discussion of their findings. Since a high proportion of all groups in the Koebnick et al. study maintained normal BMIs, and BMI also increased with time eating raw food, it seems likely that food choices, diet composition and dietary energy intake varied with duration of raw diet experience and between the normal and underweight subjects. Unfortunately, Koebnick et al. did not report collecting any data on or accounting for this very important variable, again making it impossible to make any broad conclusions about “raw food diet” and risk of underweight or amenorrhea.

Koebnick et al. reported that compared to men, women raw food dieters had a twofold increased risk of underweight on average, and a stepwise increase in risk with increased raw food consumption. They ventured no explanation for the discrepancy between male and female risk, but it begs explanation. Males generally have a greater body mass and energy requirement and therefore should have more difficulty than females maintaining body mass on a raw diet if a raw diet is intrinsically low in nutrient or energy density. Since as I just noted, raw foods vary widely in energy density, the fact that males had a lower risk of underweight in this study suggests that females had a more restrictive approach to raw food diet than males, either restricting total food intake or specific, high energy density foods. Again, Koebnick et al. failed to collect or report the detailed food intake data that would reveal why some individuals, particularly men, eating raw food diets maintained normal or even overweight BMI, while others, particularly women, did not.

Koebnick et al. commented that “Amenorrhea is also observed with eating disorders like bulimia and anorexia.” Females make up the vast majority (~90%) of individuals involved in eating disorders.293

“Women experience more food-related conflict than men do, in that they like fattening foods but perceive that they should not eat them...Women experience more dissatisfaction with their body weight and shape than men do” and, unlike men, start practicing food intake and energy restriction at early ages.294

“Women typically view themselves as heavier than they actually are and desire a thinner figure...with more reporting dissatisfaction with their bodies than men in the same BMI category...Research suggests that men tend to be more satisfied than women with their body size

293 Fairburn CG, Harrison PJ. Eating disorders. The Lancet 2003 Feb 1;361(9355):407-416.

294 Rolls BJ, Federoff IC, Guthrie JF. Gender differences in eating behavior and body weight regulation. Health Psychol 1991;10(2):133-42. Abstract.

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or weight, even if they are overweight...For men, body size does not appear to affect their self perceptions or body image as much as it does for women, which may account for discrepancies between the sexes in weight-control behaviors.”295

Accumulated research suggests that, regardless of diet type, women are more likely than men to restrict their food intake, particularly of foods perceived as energy-dense or “fattening.” Women in general, and particularly those engaged in eating disorders, may select raw food diet as a deliberate method of food and energy intake restriction; these women may also gravitate toward what seems to them the most restrictive approach, namely 100% raw. Since apparently many women perceive themselves as overweight, even when they are not, those involved in raw foods – whether engaged in eating disorders or not – may overly restrict the energy-dense raw plant foods (e.g. nuts, seeds, fruits). Further, women receive social encouragement to eat small portions, whereas society expects men to “eat like a man” i.e. large portions.

This well established data predicts a higher incidence of underweight among female than male raw food dieters, due to deliberate food intake restriction. This suggests that deliberate energy restriction by female subjects probably confounds Koebnick et al.’s link between high intake of raw foods to underweight and amenorrhea. The fact that a majority of subjects in this study engaged in fasting, the most severe form of deliberate energy restriction, increases the probability that some or all of the underweight subjects in this study practiced other forms of deliberate food intake and energy restriction. Koebnick et al. did not report any data that would clarify this issue, making it impossible to exclude the possibility that the underweight individuals in their study population engaged in deliberate food intake restriction, again making it impossible to make any broad conclusions about humans’ ability to maintain health on raw plant foods.

Therefore, while Koebnick et al. did find that among their raw dieter population a higher intake of raw foods was associated with a greater risk of underweight and disturbances of menstrual function, since they did not control for diet composition, energy intakes, deliberate non-fasting food restriction, and frequency and duration of fasting, they did not establish any meaningful connection between “raw food diet” and either underweight or amenorrhea. Their data does not support their stated conclusion that “The main reason for a low BMI for raw food dieters is the consumption of a strict raw food diet” because they failed to recognize or account for the potential wide variation in the nutrient contents of a strict raw food diet determined by conscious choice. Put pointedly, their data does not support the conclusion that all possible permutations of plant-based raw food dieting result in significant dietary energy restriction, underweight, or sub-fecundity in modern humans. Therefore, it does not provide evidence for a raw plant food ceiling for humans.

In another study of the same German raw food population, Koebnick et al. reported that the vegan raw food dieters they surveyed consumed an average of only 1.9 kg total food supplying only 1887 kcal per

295 Millstein RA, Carlson SA, Fulton JE, et al.. Relationships Between Body Size Satisfaction and Weight Control Practices Among US Adults. Medscape J Med 2008;10(5):119.

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day, or about 1.0 kcal/100g food.296 This suggests a low intake of energy dense fruits like dates (2.8 kcal/g) or nuts and seeds (around 5.5 kcal/100g). Active women of child-bearing age generally require 2000 to 2500 kcal daily, and active men require 2500 to 3000 kcal daily. The population studied by Koebnick et al. probably had a low intake of total food and energy dense foods, which would explain their tendency to very low body mass. Again, this fails to support a conclusion that humans can’t meet their energy requirements on a raw food diet, only that those in this population failed to do so.

Of interest, Fontana et al. studied a smaller population of U.S. plant-based raw food dieters with an average of 3.6 years of experience and found that they also had a mean BMI in the normal range.297 In this study, men had a mean body weight of 65 kg, and women 54 kg; men had a mean body fat percentage of 13 and women 24. These body fat levels indicate that these raw food subjects had good physical fitness; neither men nor women had too little body fat. Meanwhile, the control subjects had male and female BMIs of 26 and 25 and body fat percentages of 21 and 34, respectively. Thus, among the controls, the men and women had body fat percent levels defined as average and obese, respectively, and both had BMIs defined as overweight. Fontana et al. found that the control subjects had greater bone density than the vegan raw food dieters, but we expect heavier people to have greater bone mass than lighter weight subjects, because bone adapts to greater loads by increasing in density (Wolff’s Law). Although once again not an appropriate trial, merely a survey of a population, Fontana et al.’s findings do not support the “raw food ceiling” and “plant food ceiling” claims of Ben-Dor et al..

Plant-Food Ceiling Part 3: Simian Diet Trials

We have no controlled clinical trials testing the hypothesis that modern humans must eat cooked starches or animal flesh to maintain health, weight, and fecundity. However, we do have two studies that come very close to the mark, and neither supports the idea that human dentition or gastrointestinal physiology imposes the plant food ceilings proposed by Ben-Dor et al..

In one of these, Jenkins et al. (1997) compared the effects of a simian diet composed entirely of non- starchy vegetables, fruits, and nuts (edible raw) to a control diet containing cooked starches and animal products.298 Subjects were allowed but not required or encouraged to cook the foods in the simian diet. Cooking would not have had much effect on the digestibility of the foods in the simian diet because it included only whole plant foods that humans can consume in raw form.

When eating the vegetable diet, subjects consumed an average of 2.6 kg food daily – 1.8 kg vegetables, 0.7 kg fruits, and 0.1 kg nuts – providing 2300 kcal and 64 g fiber. Thus they consumed 0.7 kg/d more food than the subjects in Koebnick et al. (2005). Jenkins et al. advised subjects who lost more than 0.5

296 Koebnick C, Garcia AL, Dagnelie PC, et al.. Long-term Consumption of a Raw Food Diet is Associated with Favorable Serum LDL Cholesterol and Triglycerides but Also with Elevated Plasma Homocysteine and Low Serum HDL Cholesterol in Humans. J Nutr 2005 Oct 1;135(10):2372-2378.

297 Fontana et al.. Arch Intern Med 2005 Mar 28;165(6):684-9.

298 Jenkins DJA, Popovich DG, Kendall CWC, et al.. Effect of a Diet High in Vegetables, Fruit, and Nuts on Serum Lipids. Metabolism 1997 May;46(5):530-537.

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kg in the first week on the vegetable diet to eat more fruits and nuts in the second week to prevent weight loss.299 The vegetable diet included 60 to 120 g/day of nuts, and provided an average of only 25% of energy as fat, compared to 29% in the control diet. When on the control diet providing only 29 g fiber, they consumed 2318 kcal/d. Thus, these subjects had similar energy intakes on the high vegetable diet and the low vegetable diet, despite the former having twice as much fiber as the latter. If the simian dieters had consumed 1.4 kg fruits, 1.0 kg vegetables, and 0.2 kg nuts, they would have obtained a greater total energy intake while consuming the same mass of food.

During the vegetable diet period, subjects lost an average of 0.5 kg, which was not significantly different from the control weight change (–0.3 kg). Jenkins et al. (1997) reported “The vegetable diet was well tolerated, although participants noted increased flatulence.” This controlled trial provides evidence that modern humans probably can obtain adequate energy from a 100% raw plant food diet despite our small molars and without burdening our gut with any “avalanche of fiber.”

Jenkins et al. (2001) studied the effects of a very high fiber diet composed entirely of cultivated fruits, vegetables, and nuts that can be eaten raw and providing 55 g fiber per 1000 kcal in modern humans.300 All subjects consumed each of three diets – the very high fiber diet, a starch-based lacto-vegetarian diet, or a lacto-ovo low fat therapeutic diet – for two weeks at a time in a randomized crossover design. When eating the very high fiber diet, the subjects consumed an average of 5.1 kg of food daily (range, 3.6 to 6.3 kg) supplying an average of 2706 kcal301 and 149 g fiber. In comparison, when eating the starch-based and low-fat therapeutic diets they consumed an average of 1.9 kg (range, 1.5 to 2.4 kg) and 2.0 kg (1.4 to 2.4 kg) of total food daily. This data shows clearly that modern humans can sustain intakes of more than 2 kg of fibrous plant food daily.

Although Jenkins et al. attempted to get subjects to eat enough to maintain weight (range, 2400 to 2700 kcal), subjects tended to lose weight on all diets, high and low fiber alike.302 The subjects started with an average BMI of 25, defined as overweight. BMIs ranged from 21 (normal) to 32 (obese), so some subjects probably had ample excess adipose. All diets provided less than 24% of energy from fat, contributing to a negative fat balance despite high energy intakes.

When eating the very high fiber, 100% plant-based diet, subjects consumed more total food (5.1 kg) and kcalories (2705) than when eating a lacto-ovo “low-fat therapeutic diet” (2509 kcalories, 2 kg of total daily food, and 10 g fiber per 1000 kcal). Consistent with this, when eating the very high fiber vegetable diet, subjects lost less weight than when eating the low fiber “therapeutic” diet (0.4 kg and 0.6 kg, respectively). Apparently modern humans with small molars and guts can consume similar amounts of energy from a very high fiber diet as from a relatively low fiber diet. In this study, subjects consumed

299 Good advice for the underweight German raw food dieters studied by Koebnick et al. (1999 and 2005).

300 Jenkins DJA, Kendall CWC, Popovich DG, et al.. Effect of a Very-High-Fiber Vegetable, Fruit, and Nut Diet on Serum Lipids and Colonic Function. Metabolism 2001 April;50(4):494-503.

301 An uncanny resemblance to Ben-Dor et al.’s calculated 2705 kcal energy expenditure for H. erectus!

302 Jenkins et al.. Metabolism 2001 April;50(4):494-503

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2.8 times as much total plant food (by weight) and 50% more energy than consumed by the raw food dieters studied by Koebnick et al. (2005).303

Table 8.4 compares the food and energy intakes Koebnick et al. (2005) reported for raw food dieters to those Jenkins et al. reported for subjects consuming largely raw simian diets in two different studies. The data from Jenkins et al. suggests strongly that the raw food dieters studied by Koebnick et al. had restricted food and energy intake for reasons other than the bulk or fiber content of the food. As suggested above, factors may have included fasting, eating disorders, avoidance of energy-dense fruits or nuts, and deliberate restriction for body weight control.

Table 8.4: Food mass, fiber, and energy intakes reported in Koebnick et al.’s survey of vegan raw food dieters versus Jenkins et al.’s two trials of a simian diet.

Study Total food Fiber (g) Energy intake (kcal) Dietary Energy consumption (kg) Density (kcal/g)

Koebnick et al., raw 1.8 59.0 1887.0 1.0 vegan group

Jenkins et al. vegan 2.6 64.0 2300.0 0.9 simian diet, 1997

Jenkins et al. vegan 5.1 149.0 2700.0 0.4 simian diet, 2001

Apparently modern human teeth and guts can process diets very high in fiber-rich plants, and probably can obtain adequate nutrients to maintain body mass and consequently, fecundity. It seems that we lack evidence to support the hypothesis that humans can’t, and ancient humans couldn’t, obtain adequate energy from a diet consisting entirely of a sufficient quantity of raw plant foods. Furthermore, we have good reason to believe that African H. erectus/ergaster – the branch that gave rise to modern humans – had control of fire and hence was able to utilize both cooked and raw plant foods. As discussed in Chapter 1, a hypothetical diet providing 60% of weight as cooked starchy plant foods would have provided H. ergaster with about 20% more energy than a diet providing 60% of weight as raw meat.

Small Intestine Length and Obesity

The relative length of the human small intestine compared to that of animals biologically adapted to eating flesh might help us explain why several studies have reported that humans eating diets lacking animal flesh, eggs, and milk tend to maintain a healthier body mass throughout life.

Among U.S. Seventh Day Adventists, “Mean BMI was lowest in vegans (23.6 kg/m2) and incrementally higher in lacto-ovo vegetarians (25.7 kg/m2), pesco-vegetarians (26.3 kg/m2), semi-vegetarians (27.3 kg/

303 Koebnick et al.. J Nutr 2005 Oct 1;135(10):2372-2378.

SMALL INTESTINE – 121

m2), and nonvegetarians (28.8 kg/m2).”304 In that population, only the vegans had an average BMI in the healthy range, whereas all other groups had average BMIs indicating overweight or obese, and the prevalence of overweight or obesity increased directly with the increased variety and amount of animal flesh in the diet.

In the EPIC-Oxford project, vegans had the lowest average BMI305 and the slowest rate of weight gain, despite the fact that many vegans typically eat energy-dense processed foods like oils, sugars, sweets, and flour products.306 In a Belgian population, people reporting a higher intake of animal protein and lower intake of plant protein had a higher body mass than those with lower intake of animal protein and higher intake of plant protein.307 In the U.S., meat consumption associated with both obesity and central abdominal obesity.308

Simply, the human has a long small intestine with a great surface area for absorption, adapted to maximizing nutrient absorption from plant foods having a high water and fiber content, low caloric density, and low percentage of fat. Humans can only absorb 85 to 90 percent of the fats in whole nuts and seeds,309 whereas we can absorb nearly 100% of dietary animal fat or refined oils.310 When presented with fiber-free, easily digested animal flesh or refined plant oils, the very long human small intestine probably absorbs more fat than actually required. Thus, when eating animal flesh (or refined plant oils), we have a greater likelihood of a positive fat balance (more fat assimilated than expended), which will result in a gain of body fat mass unless counterbalanced by deliberate (and difficult) restriction of food and energy intake.

Further, animal flesh provides only protein and fat, and the body very efficiently stores any excess dietary fat as body fat; whereas most plant foods contain very little fat and consist primarily of carbohydrate, which the body only very rarely converts to body fat, primarily when subjected to extreme

304 Tonstad S, Butler T, Yan R, and Fraser GE. Type of Vegetarian Diet, Body Weight, and Prevalence of Type 2 Diabetes. Diabetes Care. 2009 May; 32(5): 791–796.

305 Spencer EA, Appleby PN, Davey GK, Key TJ. Diet and body mass index in 38 000 EPIC-Oxford meat-eaters, fish-eaters, vegetarians, and vegans. Int J Obesity (2003);27:728-34.

306 Rosell M, Appleby P, Spencer E, and Key T. Weight gain over 5 years in 21, 966 meat-eating, fish-eating, vegetarian, and vegan men and women in EPIC-Oxford. International Journal of Obesity (2006) 30, 1389–1396.

307 Lin Y, Bolca S, Vandevijvere S, et al.. Plant and animal protein intake and its association with overweight and obesity among the Belgian population. British Journal of Nutrition 2011;105:1106-1116.

308 Wang Y, Bevdoun MA. Meat consumption is associated with obesity and central obesity among US adults. Int J Obes (Lond). 2009 June; 33(6): 621–628.

309 Mattes RD, Dreher ML. Nuts and healthy body weight maintenance mechanisms. Asia Pac J Clin Nutr 2010;19(1): 137-141.

310 Rumpler WV, Baer DJ, Rhodes DG. Energy available from corn oil is not different that that from beef tallow in high- or low-fiber diets fed to humans. J Nutr 1998 Dec 1;128(12):2374-2382.

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overfeeding of highly refined carbohydrates at levels generally possible only in a metabolic ward.311, 312 Under normal (not forced) feeding conditions, particularly when eating bulky, fiber-rich whole plant foods, dietary fat makes the major contribution to the positive fat balance required to produce an increase in body fat stores.313

Finally, the mammalian gut has taste receptors which sense nutrients ingested, and when in contact with carbohydrates it releases gastro-intestinal peptides which transmit a signal of carbohydrate ingestion to the brain via the vagus nerve.314 This signal appears to induce satiation. Consequently, when animal products displace plant products, the reduced total intake of and gut exposure to glucose and fructose may result in less satiation than when consuming a plant based diet.

311 Flatt JP. Issues and Misconceptions About Obesity. Editorial. Obesity (2011);19(4): 676–686.

312 Hellerstein MK. No common energy currency: de novo lipogenesis as the road less traveled.. Am J Clin Nutr 2001 Dec; 74(6):707-708.

313 Swinburn B and Ravussin E. Energy balance or fat balance? Am J Clin Nutr 1993;57(suppl): 766S-71S.

314 Rasoamanana R, Darcel N, Fromentin G, Tomé D. Nutrient sensing and signaling by the gut. Proceedings of the Nutrition Society(2012);71:446-455.

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9: Cecum and Appendix

The Cecum

The cecum (Latin: caecum) consists of a blind pouch found just past the end of the ileum (the last part of the small intestine).

Animals that consume large amounts of highly fibrous material such as grass and leaves have very large cecums. For example, the horse has a cecum measuring approximately four-feet long, which can hold up to 40 quarts of food and fluid.315 It houses symbiotic fermentative microbes that break down fibrous material not digested in the small intestine.

Flesh-eating animals also have cecums:

“In the dog, the cecum is a coiled appendage located distal to the ileocecal valve, while in the cat the cecum is not as coiled (Stevens and Hume, 1995).”316

According to Snipes, cats have a conspicuously small and macroscopically relatively undifferentiated cecum in comparison to most plant-eating animals. “Microscopically (light, scanning and transmission electron microscopy), however, it is characterized by an abundance of goblet cells and enterocytes rich in organelles, suggestive of functional activity.”317 Thus, the cecum probably has some as yet undetermined function in cats.

Gray’s Anatomy describes the human cecum as follows:

“The Cecum (intestinum cæcum) (Fig. 1073), the commencement of the large intestine, is the large blind pouch situated below the colic valve. Its blind end is directed downward, and its open end upward, communicating directly with the colon, of which this blind pouch appears to be the beginning or head, and hence the old name of caput cæcum coli was applied to it. Its size is variously estimated by different authors, but on an average it may be said to be 6.25 cm. in length and 7.5 in breadth.”318

According to Milton, the human cecum resembles that of other apes:

315 Ohio State University. Horse Nutrition. Bulletin 762-00.

316 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 5.

317 Snipes RL. Anatomy of the cecum of the cat. Anat Embryol (Berl) 1984;170(2):177-66.

318 Gray H. Anatomy of the Human Body, 20th Edition. Thoroughly Revised and Re-Edited by Warren H Lewis. Philadelphia: Lea and Febiger, 1918. New York: Bartleby.com, 2000. 2h. The Large Intestine. Retrieved on September 17, 2013 from http://www.bartleby.com/107/249.html

125

“All hominoids (apes and humans), in keeping with their descent from a common ancestor, show the same basic gut anatomy consisting of a simple acid stomach, a small intestine, a small cecum terminating in an appendix, and a markedly sacculated colon.”319 [Italic added]

Primatologists believe that comparative anatomical studies of the primates have established that the primitive, ancestral primate gut had a large cecum and little or no appendix. Generally, as one surveys the primate family, the length of the cecum (relative to the colon)

“…decreases as one traverses the primate phylogenetic tree from monkeys to humans. Concurrently, the size of the appendix increases. The appendix is mostly absent in prosimians and New World monkeys, yet they have a large caecum. In Old World monkeys the appendix is more recognizable, and it is well-developed in the anthropoid apes, which lack the large cellulose-fermenting caecum found in their ancestors and other primates....”320 [Italic added]

Some people have argued that our small cecum indicates adaptation to a meat-rich diet. However, since all anthropoid apes have small cecums and consume plant-based diets, the fact that humans have a relatively small cecum does not provide unequivocal evidence of adaptation to any significant quantity of dietary animal tissues. It more likely represents adaptation to a diet based on botanical fruits, which have a higher digestible sugar, protein, or fat concentration than the leafy plant foods upon which primates who have larger cecums depend.

The Appendix

Attached to the cecum, all anthropoid primates and some monkeys have an appendix:

“A vermiform appendix is not unique to humans. It is found in all the hominoid apes, including humans, chimpanzees, gorillas, orangutans, and gibbons, and it exists to varying degrees in several species of New World and Old World monkeys.”321

The appendix consists of “a developmental derivative and evolutionary vestige of the end of the much larger herbivorous caecum.”322

Besides primates, the rabbit, capybara, and wombat also have appendixes. All of these species eat plant- based diets. Neither cats nor dogs have an appendix. To my knowledge, no animal primarily adapted to a meat-based diet has an appendix.

319 Milton K. Nutritional characteristics of wild primate foods. Nutrition 1999;15 (6):488-98.

320 Theobald D. The vestigiality of the human vermiform appendix. The Talk Origins Archive, April 19, 2007.

321 Ibid.

322 Ibid.

126 – HUMAN NUTRITIONAL ADAPTATIONS

The human appendix secretes an alkaline fluid containing amylase, eripsin, and mucin.323 As already noted, the sole purpose of the enzyme amylase consists of starch digestion. Eripsin digests peptides (present in all whole plant foods), and mucins contribute to the mucus lining of the intestine. Only whole plant foods contain starch, so the fluid secreted by the appendix appears adapted to a plant-based diet.

Summary

Since all of the anthropoid apes (orangutans, gorillas, and chimpanzees) have reduced cecums and a vermiform appendix, these gut features probably represent an adaptation to a reduced dependence on highly fibrous plant parts (like leaves) and an increased dependence on plant tissues that are rich in digestible sugars, starches, or fats, and possibly lower in fiber, such as (in the case of the anthropoid apes) fruits, nuts, seeds, and tender leaves.

In short, when considered in relation to the rest of human physiology, the human cecum and appendix have characteristics expected for a primate that specializes in eating botanical fruits, and their proportions and characteristics do not provide any unequivocal evidence that humans have genetically adapted to eating flesh.

323 Milton K. Primate diets and gut morphology: Implications for Hominid Evolution. In Harris M (ed.), Food And Evolution: Toward a Theory of Human Food Habits, Temple University Press, 1989. 100

CECUM and APPENDIX – 127

10: Colon

For carnivores, like cats and dogs, more than 95% of ingested food (meat and fat) is assimilated, and what remains contains no fiber and little water. Since the flesh-eating animal ingests relatively large amounts of fats (compared to a plant-eating animal), it must secrete large amounts of bile to digest those fats. Bile acids have cytotoxic, genotoxic, mutagenic, and tumor promoting effects on colon tissue, particularly when in high concentration, such as in low fiber, animal-based diets.324, 325 Red meat also provides haem (heme) iron, which generates carcinogenic N-nitroso compounds (NOC).326 To minimize the negative effects of bile acids and haem iron on the colon, an animal adapted to eating flesh and fat benefits from a short colon with as little surface area as possible.

In contrast, plant-eating animals ingest foods providing large amounts of fiber and water but relatively little fat. Since the primary function of the colon consists of extracting water from the material remaining after digestion and absorption, and whole plant matter contains more fiber and water than animal matter, the colon of an animal well-adapted to eating plant materials must have greater length and surface area than that of a carnivore, to produce a relatively solid feces.

As with the small intestine, it seems unlikely that natural selection could produce a colon equally well- adapted to processing residues from both high-fat flesh and high-fiber/high-water plants. A colon short enough to ensure a fecal transit rapid enough to minimize exposure to bile acids and haem iron would be too short to extract enough water from fibrous plant food residues, resulting in a loss of valuable water in wet feces. On the other hand, a colon long enough to allow enough time for extracting enough water from a significant intake of fibrous plant food residues would extract too much water from the residues of meat, resulting in dry, compact feces that the animal would have difficulty expelling. A relatively long colon would probably not move a meat-eater’s feces through fast enough to provide optimal protection from haem iron and the bile acids.

Comparing Colons

Dogs with a body length of 0.75 m have a colon length of about 0.6 m; cats with a body length of 0.5 m have a colon length of about 0.4 m.327 Thus, in dogs and cats, the large intestine measures 80% of the torso.

324 Debruyne PR, Bruyneel EA, Li X, et al.. The role of bile acids in carcinogenesis. Mutation Research 2001;480-481:359-369.

325 Nagengast FM, Grubben MJAL, van Munster IP. Role of Bile Acids in Colorectal Carcinogenesis. European J of Cancer 1995; 31(7/8): 1067-1070.

326 Cross AJ, Pollock JRA, Bingham SA. Haem, not Protein or Inorganic Iron, Is Responsible for Endogenous Intestinal N- Nitrosation Arising from Red Meat. Cancer Res 2003 May 15; 63: 2358.

327 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 5.

129

In the horse, “The colon or large intestine is about 12 feet long,”328 making it about twice as long as the horse torso (abut six feet).

According to Gray’s Anatomy, the human colon measures about 1.5 meters (about 59 inches) in length.329 Since the average human torso (base of neck to end of tailbone) measures about 0.54 to 0.64 m (small female and average male, respectively), the human colon measures about 2.3 to 2.5 times the length of the torso, making its relative length more similar to that of the horse than that of the dog or cat. Relative to body length, the human colon measures about 3 times as long as that of the cat or dog.

The human colon “is haustrated throughout almost it entire length, like that of most apes and many monkeys.”330 Only a few non-primate species have a fully haustrated (sacculated) colon. These include the horse and the pig, both of which have primarily herbivorous diets and gut morphology. In contrast, no carnivorous marsupial, nor any member of either the Insectivora or Carnivora order (the latter of which includes omnivorous hypo- and mesocarnivores), has a haustrated colon.331

A haustrated colon has more surface area for a given length compared to a non-haustrated colon, so that an animal with a haustrated colon has more tissue surface area exposed to the passing contents than a colon without haustrations. This makes a haustrated colon optimum for extracting fluid from bulky fiber-rich plant remains to produce a relatively solid excrement. In contrast, such a colon would extract too much fluid from the drier, low fiber remains of a meat-based diet, resulting in a compact dry stool that the colon muscles would have difficulty propelling to the anus, leading to constipation. Haustrations also increase the amount of tissue exposed to potential toxins – such as bile acids or haem iron – thus increasing the risk of tissue poisoning. In other words, natural selection would only favor haustrations in an animal that specializes in eating a plant-based diet, and would favor a short, smooth- walled colon in any animal that specializes in eating flesh.

In sum, the human colon does not have characteristics appropriate for and found in the colons of animals biologically adapted to flesh-eating, and has the features appropriate for and typically found in animals biologically adapted to plant-based diets.

Intestinal Ecology

Human intestinal flora differs from that of canines and felines in species and proportions. Specifically, certain strains of bifidobacteria form a very important part of human colonic flora, but cats and dogs do not harbor these strains, and have very little or no bifidobacteria:

328 Ohio State University. Horse Nutrition. Bulletin 762-00.

329 Gray H. Anatomy of the Human Body, 20th Edition. Thoroughly Revised and Re-Edited by Warren H Lewis. Philadelphia: Lea and Febiger, 1918. New York: Bartleby.com, 2000. XI. Splanchnology. 2h. The Large Intestine. Retrieved September 18, 2013 from http://www.bartleby.com/107/249.html

330 Stevens CE and Hume ID. Comparative Physiology of the Vertebrate Digestive System. Cambridge University Press, 1995. 76.

331 Ibid., 93.

130 – HUMAN NUTRITIONAL ADAPTATIONS

“There are currently about 30 known Bifidobacterium species. The Bifidobacterium species that inhabit the human intestinal tract are rather distinct from those that inhabit the intestines of animals (Mitsuoka, 1984). The representative species of human origin include B. longum, B. breve, B. infantis, B. bifidum, B. adoltescentis and B. pseudocatenulatum. Representatives of animal-derived species include B. pseudolongum, B. thermophilus and B. animalis. Species of animal origin are never isolated from the human intestinal tract and human origin species are almost never found in animal intestines.”332

“The most significant aspect of the canine microflora is the much lower level of bifidobacteria found in canines than in other animals. The feline colonic flora (Fig. 3) is even less well characterized (12), and the bifidobacteria levels are probably even lower than in canines. In fact, bifidobacteria are only intermittently isolated from felines.”333

Humans host intestinal microbial populations of the same types found in chimpanzees,334 a species clearly adapted to a plant-based diet.

Koeth et al. reported that the intestinal microbiota found in humans habitually consuming animal flesh converts dietary choline (found in greater amounts in animal flesh than plants), phosphatidylcholine, and L-carnitine (a substance found only in flesh) into trimethylamine (TMA), which then gets metabolized to trimethylamine-N-oxide (TMAO), which promotes atherosclerosis.335 In contrast, the microbiota present in the guts of human long-term vegans (more than 5 years without meat consumption) displayed “virtually no capacity to generate TMAO.”

This indicates that, in humans, meat consumption favors the growth of colon microbiota that produce substances toxic to the vascular system, and promotes atherosclerosis (Chapter 16). This does not happen in animals physiologically adapted to consumption of flesh. For example, despite having a flesh-based diet, canines (omnivores/ mesocarnivores) do not develop atherosclerosis (Chapter 16), so either they do not harbor the same TMAO-producing bacteria as humans, or they have immunity to the toxic effects of TMAO.

332 Ishibashi N, Yaishima T, Hayasawa H. Bifidobacteria: their significance in human intestinal health. Mal J Nutr 1997; 3: 149-159.

333 Rastall RA. Bacteria in the Gut: Friends and Foes and How to Alter the Balance. J. Nutr. August 1, 2004; 134(8): 2022S-2026S.

334 Pappas S. What do Chimps and Humans Have in Common? Gut Bacteria. From: Science on NBCNews.com, updated 11/13/2012 3:30:35 PM ET. http://www.msnbc.msn.com/id/49809192/ns/technology_and_science-science/ %23.UK2RXYVD30A

335 Koeth RA, Wang Z, Levison BS, et al.. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nature Medicine 2013 April 7, Advance Online Publication. doi:10.1038/nm.3145.

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Flora, Fiber, and Fats

Animals adapted to a plant-based diet have symbiotic relationships with microbes capable of converting dietary fiber into short-chain fatty acids (SCFA), which serve as fuel for the colon and thereby contribute to total energy intake. Surprising to some, dogs (mesocarnivores) have hindgut microflora that ferment fibers to SCFAs, and dog colons use these as an energy source contributing about 7 percent of energy requirements.336 In vitro studies also suggest that cats also harbor microflora that produce SCFAs from fibers and probably obtain similar energy value from the process as dogs.337

Some evidence indicates that SCFAs also promote water reabsorption from the colon in both dogs and humans.338

Humans’ symbiotic colonic microflora convert fiber to SCFAs and these provide fuel to human colon cells. The significant contribution of colonic fermentation of fiber to energy requirements and energy conservation is evident in people who have had surgical removal of the colon. These individuals “have been shown to weigh 4 kg less than age- and height- matched controls (26) with similar energy intake (33); the loss of both the large intestine and the ability to conserve energy may be a major factor contributing to this difference.”339

According to the Food and Nutrition Board of the Institute of Medicine: “While it is still unclear as to the energy yield of fibers in humans, current data indicate that the yield is in the range of 1.5 to 2.5 kcal/ g....”340 Since non-human primates depend on the same fermentation process for extraction of energy from fiber, the energy yield of fibers for humans probably does not differ from that of gorillas or chimps.

“Studies in humans have indicated that dietary fiber is 35-100% fermentable, depending on the fiber type, with 80% fermentation of leafy vegetables (e.g. cabbage).”341 This data suggests that human colonic microflora excel at fermenting fibers found in leaves and fruits, a pattern expected for a large- bodied primate that primarily eats botanical fruits supplemented by green leaves. Recall also that human intestinal immune cells require I3C from cabbage family vegetables for activation (Chapter 8).

336 Subcommittee on Dog and Cat Nutrition, Committee on Animal Nutrition, National Research Council. Nutrient Requirements of Dogs and Cats. National Academies Press, 2006. 62.

337 Ibid., 62.

338 Subcommittee on Dog and Cat Nutrition, Nutrient Requirements of Dogs and Cats. NAP, 2006. 62.

339 McNeil NI. The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 1984 Feb;39(2):338-342.

340 Food and Nutrition Board of the Institute of Medicine. Dietary Reference Intakes for Energy, etc. National Academies Press, 2005. 349.

341 Popovich DG, Jenkins DJA, Kendall CWC, et al.. The Western Lowland Gorilla Diet has Implications for the Health of Humans and other Hominoids. J Nutr 1997 Oct 1;127(10):2000-2005.

132 – HUMAN NUTRITIONAL ADAPTATIONS

In humans consuming conventional, low fiber diets (20 g/d) with little from fruits and green vegetables, fermentation of fiber contributes 5 to 10% of energy requirements (mean, 7.5%), similar to the pig,342 which has a hindgut specialized for fiber fermentation. In pigs, the energy available as SCFA from hindgut fermentation increases with the concentration of fiber in the diet; at dietary fiber concentrations of 77 g/kg and 240 g/kg dry matter, pigs obtained 7 and 18% of total available dietary energy, respectively, from fiber fermentation.343 For reference, assuming that humans consume 1.5 to 2 kg food daily, and 80% of this weight consists of water, the fiber concentration of a diet supplying only 20 g/d is 50 to 70 g/kg dry matter. .

Since humans consuming 150 g fiber per day from fruits and vegetables show a 3-4 fold increase in fecal SCFAs compared to people consuming only 25 g fiber per day,344 and 95 to 99 percent of SCFAs produced in the hindguts of mammals get absorbed,345 as with pigs, we expect that humans consuming more than 20 g fiber daily probably get much more than 10% of their energy from fiber fermentation:

“Dietary fiber intakes in Africa are up to seven times higher than in the United Kingdom (36). The amount of fiber and other carbohydrate in the stool is unknown, but it is likely that a substantial proportion of the fiber will be metabolized to short-chain fatty acids, and for these people, the energy made available is likely to be proportionately higher.”346

Based on the above data humans requiring 3000 kcal daily and consuming 20 g/d fiber would therefore obtain 150 to 300 kcal per day from fiber fermentation. That amounts to 28 to 56% of the energy requirements of the human brain (540 kcal/d347). Humans consuming 80 to 100 g fiber daily (240 g/kg dry matter) on plant-based diets rich in green vegetables and fruits probably produce 2-3 times as much SCFA and obtain as much as 18% of their energy, possibly more, from colonic fiber fermentation. For people expending 2500 to 3000 kcal daily (active young women and men respectively), that would amount to 450 to 540 kcal per day , or 83 to 100% of the brain’s energy requirements. It appears that fiber fermentation probably can in humans provide nearly as much energy to the gut as required by the brain, allowing the body to direct an energy-equivalent amount of digestible sugars away from the gut, to the brain.

342 McNeil NI. The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 1984 Feb;39(2):338-342.

343 Anguita M, Canibe N, Pérez JF, Jensen BB. Influence of the amount of dietary fiber on the available energy from hindgut fermentation in growing pigs: Use of cannulated pigs and in vitro fermentation. J Anim Sci 2006 Oct;84(10):2766-2778.

344 Jenkins et al.. Effect of a Very-High-Fiber Vegetable, Fruit, and Nut Diet on Serum Lipids and Colonic Function. Metabolism 2001 April;50(4):494-503.

345 Subcommittee on Dog and Cat Nutrition, Nutrient Requirements of Dogs and Cats. NAP, 2006. 62.

346 McNeil NI. The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 1984 Feb;39(2):338-342.

347 Herculano-Houzel S (2011) Scaling of Brain Metabolism with a Fixed Energy Budget per Neuron: Implications for Neuronal Activity, Plasticity and Evolution. PLoS ONE 6(3): e17514. doi:10.1371/journal.pone.0017514

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In folifrugivorous gorillas, colonic fermentation of fiber provides 30-60% of total energy requirements.348 The gorilla primarily feeds on leaves, which consist largely of fiber, and has a large colonic surface area, so we expect him to depend more on fiber fermentation than a primarily frugivorous species, which would depend more on digestion of sugars, fats, and proteins in botanical fruits.

Thus, in humans, colonic microbial fermentation of fiber plays a role as significant as in the pig, which scientists classify as a hindgut fermenter, and it ferments the types of fibers found in tender leaves better than many other types. Further, it can play a very important role in human total energy economy and contribute substantially to provision of the energy requirements of the gut, allowing the body to divert other resources (glucose) to the brain. The human intestinal system including the colon and its symbiotic microbes have the features expected of a species that specializes in consuming whole botanical fruits supplemented by vegetables, particularly leaves.

Colon Health

If humans have a colon adapted to a plant-based diets, we should find that people eating plant-based diets have easier fecal elimination and better colon health. Animals adapted to carnivory (e.g. felines, canines) have daily bowel movements whether they consume plants (fiber) or not. If humans have a lower frequency of bowel movement or increased risk of colon disorders when consuming animal flesh than when not, this supports the conclusion that the human colon has not adapted to dietary animal flesh, unlike the feline or canine colon.

In 1925, Kuczynski reported that the Kirghiz nomads who lived almost exclusively on grass-fed animal products suffered “habitual constipation.”349

Sanjoaquin et al. reported that Europeans consuming vegan diets were 2.5 times more likely to have a daily bowel movement than meat-eaters.350 In this study, people who ate all types of animal flesh (behavioral omnivores) had the lowest frequency of bowel movement, followed in ascending order by people who ate fish flesh but not other types, people who ate lacto-ovo vegetarian diets, and people who ate vegan diets (no animal products), who had the highest frequency of bowel movements. Thus, in this population, consumption of animal products may have reduced frequency of bowel movement in a dose- response fashion.

348 Popovich et al.. The Western Lowland Gorilla Diet has Implications for the Health of Humans and other Hominoids. J Nutr 1997 Oct 1;127(10):2000-2005.

349 Bernstein FL, Burton C, Healey D. Soviet Medicine: Culture, Practice, Science. Northern Illinois University Press, 2010. 75.

350 Sanjoaquin et al.. Nutrition and lifestyle in relation to bowel movement frequency: a cross-sectional study of 20 630 men and women in EPIC–Oxford. Public Health Nutrition 7(1):77-83. doi:10.1079/PHN2003522.

134 – HUMAN NUTRITIONAL ADAPTATIONS

Similarly, Davies et al. reported that vegans had the shortest intestinal transit time and the most frequent defecation, compared to vegetarians and behavioral omnivores.351 This study data suggests that any type of animal food in the diet may reduce the frequency of bowel movement in humans, whereas no type of animal food decreases bowel movement frequency in healthy dogs or cats.

Crowe et al. reported that Europeans (British) consuming vegetarian diets have a lower risk of diverticular disease than those consuming flesh.352 In this study, people who ate all types of animal flesh and people who ate fish flesh but not land animal flesh had similar risk for diverticular disease; vegetarians (consumers of milk and eggs) combined with vegans (no animal product) had a 31 percent lower risk of the disease compared to flesh-eaters; and vegans had a 72 percent reduced risk compared to flesh-eaters. Vegetarians and vegans also had a reduced risk of diverticular disease after adjustment for fiber intake; indicating that animal food intake increases the risk of the disease even if one consumes fiber in quantities similar to people eating plant-based diets. This data indicates that all animal foods (flesh, milk, and eggs) increase the risk of diverticular disease in humans, possibly in a dose-response fashion, and supports the conclusion that the human colon remains adapted to a plant-based diet and has not specifically adapted to consumption of animal products.

In a clinical trial, Jenkins et al. compared the effects on colon health of a very high fiber “simian” diet composed entirely of vegetables, fruits, and nuts (fiber, 55g/1000 kcal) to those of a whole cereal and legume, lacto-vegetarian starch-based diet (fiber, 19g/1000 kcal) and a low-fiber, low-fat diet (fiber, 10 g/1000 kcal).353 When on the simian diet, people produced the largest daily fecal output (906 g), compared to the starch diet (279 g) and the low-fat diet (172 g). The simian diet also produced the greatest daily elimination of potentially harmful bile acids (1.1 g, 0.5 g, and 0.7 g for simian, starch, and low-fat diets, respectively), but had the lowest fecal concentration of bile acids (1.2, 2.0, and 4.0 mg/g wet weight, simian, starch, and low-fat, respectively). The simian diet produced a 3 to 4 fold increase in fecal SCFAs compared to the low-fat diet. Besides serving as an energy source and facilitating water reabsorption, SCFAs have anti-cancer properties. People on the simian diet also reduced their LDL by 33% within one week, similar to the effect of first-generation statin drugs. Jenkins et al. concluded that the simian fruit-and-vegetable diet simultaneously reduced the risk factors for cardiovascular disease and possibly colon cancer.

Summary

The human colon closely resembles that of species known to consume plant-based diets, not only in length, structure and function, but also in symbiotic flora and fermentation of fiber. Colonic

351 Davies GJ, Crowder M, Reid B, Dickerson JWT. Bowel function measurements of individuals with different eating patterns. Gut 1986;27:164-169.

352 Crowe FL, Appleby PN, Allen NE, Key TJ. Diet and risk of diverticular disease in Oxford cohort of European Prospective Investigation into Cancer and Nutrition (EPIC): prospective study of British vegetarians and non-vegetarians. BMJ 2011 Jul 19;343:d4131. doi: 10.1136/bmj.d4131.

353 Jenkins DJA, Kendall CWC, Popovich DG, et al.. Effect of a Very-High-Fiber Vegetable, Fruit, and Nut Diet on Serum Lipids and Colonic Function. Metabolism 2001 April;50(4):494-503.

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fermentation of fiber in humans can contribute significantly to total energy supplies, and a very high fiber diet probably enables colonic flora to produce enough SCFAs to significantly offset the energy requirements of the brain. A whole-foods plant-based diet consisting primarily of fruits, vegetables, and nuts appears to produce the most healthful colonic function. These findings support the conclusion that the human colon remains adapted to a plant-based diet.

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Seminal Vesicles

The human male reproductive system includes seminal vesicles. No animal adapted to a primarily flesh- based diet has seminal vesicles.354

Placenta

The anthropoid apes including humans have a discoid placenta, a villous interdigitation between mother and fetus, and a hemochorial membrane separating mother and fetus. Other species with a discoid placenta include the rabbit, hare, guinea pig, rat, mouse, and beaver, which eat plant-based diets, and bats (frugivorous and insectivorous) and moles, but none of these have a villous interdigitation. Cats, dogs, and other members of the Carnivora order have zonary placentas, labyrinth interdigitation, and an endothelialchorial membrane separating mother and fetus. Members of the Arteriodactyl order, including pigs, sheep, cows, and goats have diffuse or cotyledonary placentas.355 Rather than take space here to give a lengthy explanation of the differences referred to by these technical terms, I refer any reader interested in the details to the reference given.

Morning Sickness

If a species must eat animal flesh to survive or successfully reproduce, then the females of that species would not very likely have an aversion to eating flesh during pregnancy. Neither cats nor dogs experience an aversion to eating flesh during pregnancy.

However, among humans, women often have a strong aversion to consumption of animal products during pregnancy. Cross-cultural data indicates that morning sickness primarily occurs in among women in populations consuming animal-based diets and rarely occurs in populations that have plant- based diets356:

“A cross-cultural analysis using the Human Relations Area Files revealed 20 traditional societies in which morning sickness has been observed and seven in which it has never been observed. The latter were significantly less likely to have animal products as dietary staples and

354 Dixon A. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Humans. Oxford University Press, Jan 26, 2012. P. 321.

355 Benirschke K. Comparative Placentation. http://placentation.ucsd.edu/introfs.html

356 Sherman PW, Flaxman SM. Nausea and vomiting of pregnancy in an evolutionary perspective. Am J Obstet Gynecol 2002;186:S190-7.

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significantly more likely to have only plants (primarily corn) as staples than the 20 societies in which morning sickness occurred.”357

The aversion to animal products during pregnancy probably improves reproductive fitness due to the fact that animal flesh carries pathogens that could terminate a pregnancy, as well as highly available iron that supports growth of pathogens, and (as shown in Chapter 7 above) humans lack the stomach acidity required to kill those pathogens:

“Animal products may be dangerous to pregnant women and their embryos because they often contain parasites and pathogens, especially when stored at room temperatures in warm climates. Avoiding foodborne microorganisms is particularly important to pregnant women because they are immunosuppressed, presumably to reduce the chances of rejecting tissues of their own offspring (Haig 1993). As a result, pregnant women are more vulnerable to serious, often deadly infections. We hypothesize that morning sickness causes women to avoid foods that might be dangerous to themselves or their embryos, especially foods that, prior to widespread refrigeration, were likely to be heavily laden with microorganisms and their toxins. The alternative hypotheses that morning sickness is (i) an epiphenomenon of mother-offspring genetic conflict or hormones associated with viable pregnancies, or (ii) an indicator to potential sexual partners and kin that the woman is pregnant, resulting in reduced sexual behavior and increased nepotistic aid, were not well supported. Available data are most consistent with the hypothesis that morning sickness serves an adaptive, prophylactic function.” 358

“Immunosuppression during pregnancy makes the mother vulnerable to pathogens. Because meat is the principal source of ingestible pathogens, pregnancy raises the costs of meat eating. Natural selection has crafted a mechanism involving changes in nausea susceptibility and olfactory perception that reduces meat consumption during pregnancy. Evidence is presented showing that the luteal phase is marked by both immunosuppression and changes in nausea susceptibility and olfaction; meat consumption may be reduced during this period, suggesting a mechanism similar to pregnancy sickness. Constraints on compensatory increases in meat consumption outside of the luteal phase explain why women eat less meat than men. Meat is the principal target of acquired aversions. Women possess more aversions than men, suggesting that prophylactic mechanisms sometimes result in longstanding dietary changes. Reproductive immunosuppression explains many aspects of dietary behavior and sheds light on factors that may have contributed to gender-based divisions of labor during hominid evolution.”359

The fact that women experience aversion to and sickness from eating animal flesh during pregnancy provides evidence that natural selection favored the reproduction of humans who have the ability to

357 Flaxman SM, Sherman PW. Morning sickness: a mechanism for protecting mother and embryo. Q Rev Biol. 2000 Jun; 75(2):113-48.

358 Ibid.

359 Fessler DM. Luteal phase immunosuppression and meat eating. Riv Biol. 2001 Sep-Dec;94(3):403-26.

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consume completely plant-based diets during pregnancy and have fewer pregnancy complications when not eating animal flesh. This suggests that meat consumption may impair human reproductive ability and therefore Darwinian fitness.

Fertility

“Fitness, according to Darwin, means the capacity to survive and reproduce.”360 The greater the capacity to reproduce healthy children over a lifespan, the greater the potential Darwinian fitness.

Species biologically adapted to meat consumption have their greatest fertility when eating meat, and lose fertility in the absence of meat consumption.

“Carnivorous diets are associated with higher basal rates of metabolism, faster growth rates, and higher fecundity in carnivorans. Consequently, if ecological conditions, such as an already high diversity of predators, do not inhibit the evolution of hypercarnivory, mesocarnivorous species are expected to evolve in that direction.”361

If an animal experiences a reduction in fertility or impairment of reproductive functions in a dose– response to consumption of meat or other animal products, this strongly suggests maladaptation to the consumption of animal flesh. If humans are mesocarnivorous, as described by leading advocates of animal-based (low carbohydrate, or paleolithic) diets, humans should clearly have higher fertility when eating animal-based diets, and show signs of evolving in the direction of hypercarnivory, i.e., the more flesh in the diet, the more fertile.

On the other hand, a species biologically adapted to a plant-based diet will have its greatest reproductive fertility when eating plants. If a given species shows improvements in fertility when consuming increased amounts of fruits and vegetables or other plant foods or plant-based nutrients, this strongly suggests adaptation to a plant-based diet.

Generally and for some years birth rates in nations with low animal protein consumption have exceeded rates in nations with high meat or fat consumption. In 1952 Josué de Castro reported in his book The Geography of Hunger the data in Table 11.1.362 This 1952 data predates the release of the birth control pill (first marketed in 1960) so we can’t attribute these differences to use of the contraceptive pill in industrialized nations. It also predates the widespread use of hormones in livestock production. It suggests that, in humans, animal protein intake may impair fertility.

360 Demetrius L, Ziehe M. Darwinian fitness. Theoretical Population Biology 2007; 72: 323-345.

361 Van Valkenburgh B. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47(1): 147-163.

362 William RJ. Nutrition Against Disease. Pitman, 1971: 141. Citing DeCastro J. The Geography of Hunger. Little, Brown, 1952.

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Table 11.1: Dietary animal protein and birth rate (From de Castro, 1952)

Nation Dietary animal protein (g/day) Birth Rate (per 100,000)

Formosa 4.7 45.6

Malay States 7.5 39.7

India 8.7 33.0

Japan 9.7 27.0

Yugoslavia 11.2 25.9

Greece 15.2 23.5

Italy 15.2 23.4

Bulgaria 16.8 22.2

Germany 37.3 20.0

Ireland 46.7 19.1

Denmark 59.1 18.3

Australia 59.9 18.0

United States 61.4 17.9

Sweden 62.6 15.0

Source: William RJ. Nutrition Against Disease. Pitman, 1971: 141. Citing DeCastro J. The Geography of Hunger. Little, Brown, 1952.

This data seems to show that human fertility declines in a dose-response fashion as animal protein intake increases. However, it does not rule out confounders such as income, female social status, and other social factors. Nevertheless, a number of late 20th and early 21st century studies have linked consumption of animal protein to reproductive disorders that would reduce fertility and hence, reproductive fitness.

Animal Flesh and Female Infertility

Chavarro et al. prospectively studied the effect of intake of animal or vegetable protein on ovulatory fertility in 18,555 married women having no initial history of infertility.363 They found that the multi- variate adjusted relative risk of ovulatory infertility increased by 39 percent when comparing the highest to lowest animal protein intake. Further, “consuming 5% of total energy intake as vegetable protein rather than as animal protein was associated with a more than 50% lower risk of ovulatory infertility.”

363 Chavarro JE, Rich-Edwards JW, Rosner BA, Willet WC. Protein intake and ovulatory infertility. Am J Obstet Gynecol 2008 Feb: 198(2): 210.el–210.e7.

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The addition of one serving of meat (red meat, chicken, turkey, processed meat, or fish) per day, while holding total energy intake constant, correlated with a 32 percent greater risk of ovulatory infertility. Increasing animal protein intake by 5 percent at the expense of carbohydrates increased the risk of infertility by 18 percent, while increasing vegetable protein intake by 5 percent in the same fashion reduced risk by 50 percent. In this study, increased animal protein intake increased the risk of infertility in women greater than 32 years of age but not those less than 32. This study provides additional evidence that consumption of animal flesh reduces the long-term ovulatory fertility of women, a major blow to their Darwinian fitness.

Barr et al. found that vegans who had avoided eating flesh for at least 2 years had a higher proportion of normal ovulatory cycles than did nonvegetarians (75% vs. 62%).364 Barr et al. found that the vegan women they studied had no anovulatory cycles over a six month period, while among the lactovegetarians 7 of every 100 cycles produced no ovum, and among those with the highest variety and intake of animal protein (nonvegetarians), 15 of every 100 cycles produced no ovum. In this study, as the dose of animal protein increased, so did the impairment of ovulation in direct proportion, and only women eating no animal products had ovulation on every cycle. This study provides more evidence that consumption of animal flesh impairs human fertility in a dose-response fashion.

Hill et al. found that when they fed a Western diet (40 percent of calories from fat, and 65 percent of protein from animal products) to premenopausal South African women accustomed from weaning to a “vegetarian” diet supplying 15 percent of calories from fat and “mainly plant protein,” they experienced multiple deleterious hormonal changes.365 These included increases in testosterone, follicle stimulating hormone (FSH), and prolactin, and a decrease in estrogen. The changes observed “may be associated with anovulatory cycles, amenorrhea, and infertility” since studies (cited in this paper) have shown that these symptoms occur in conjunction with relatively small increases in testosterone, prolactin, or FSH, or decreases in estrogen. The changes in testosterone and estrogen found in this study suggest that consumption of animal products may have a masculinizing effect on women. Elevated testosterone occurs in women affected with polycystic ovary syndrome, a disorder characterized by impaired ovulation and fertility.

In addition, in a case-control study involving 1008 Italian women, Parazzini et al. found that women with the highest intake of red meat had a risk of endometriosis twice that of women with the lowest intake, while women with the highest intake of green vegetables (spinach/other greens, crucifers, green and red salads, zucchini, and artichokes) or fruits (citrus, apple, peach, melon, strawberries/cherries,

364 Barr SI, Janelle KC, Prior JC. Vegetarian vs nonvegetarian diets, dietary restraint, and subclinical ovulatory disturbances: prospective 6-mo study. Am J Clin Nutr 1994;60:887-94.

365 Hill P, Garbaczewski L, Helman P, et al.. Diet, lifestyle, and menstrual activity. Am J Clin Nutr 1980; 33: 1192-1198. The 15% fat figure is in Table 1, p 1193.

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banana and pear) had, respectively, thirty and sixty percent the risk of those with the lowest intakes of those whole plant foods.366 Endometriosis typically causes infertility.367

Together, these studies suggest that female fertility may decrease in dose-response to consumption of animal flesh or milk, and improve in response to intake of fruits and green vegetables, a pattern expected for an animal with a physiology dependent upon a diet composed of fruits and vegetables but contrary to what we would expect if natural selection had favored the reproduction of primarily carnivorous humans.

High Protein Diets Potentially Toxic To Fetus

In a summary of studies involving use of high protein supplements in pregnant women, Rush stated that “it is clear that high-density protein supplements are consistently associated with depression, rather than increase, in mean birthweight.”368

Sloan et al. similarly reported that women eating higher protein diets (average, 106 g/d) and low protein diets (average, 42 g/d) during gestation both had lower birth weight infants (71 g and 77 g lower, respectively) compared to women eating moderate amounts of protein (average, 68 g/d). Multiple regression analyses showed a decline in birth weights when protein intakes exceeded about 70 g/d.369 These findings are consistent with several reviews of prospective, controlled trials that found that women who ingested sufficient energy and high levels of dietary or supplemental protein consistently showed low infant birth weight.

Excessive protein intake results in the metabolism of excess amino acids to ammonium, which circulates in the blood until the liver can convert it to urea. Rudman et al. found that the human liver has a limited ability to detoxify ammonium produced by high protein flesh-based diets, such that a protein intake of 3.2 g/kg per day (175 g for a 55 kg/120 lb woman) or greater leads to incremental increases in blood ammonium,370 which would increase ammonium delivery to the placenta.

Using a murine model, Lane and Gardner found that “the presence of ammonium at very low concentrations, as low as 18.8 uM, during development from the zygote to the blastocyst stage has significant detrimental effects on embryo physiology,” including difficulties establishing implantation,

366 Parazzini F, Chiaffarino F, Surace M, et al.. Selected food intake and risk of endometriosis. Hum Reprod 2004; 19(8): 1755-1759.

367 Bulletti C, Coccia ME, Battistoni S, Borini A. Endometriosis and infertility. J Assist Reprod Genet. 2010 August; 27(8): 441–447.

368 Rush D. Effects of Changes in Protein and Calorie Intake during Pregnancy on the Growth of the Human Fetus. In: Enkin M, Chalmers I, eds. Effectiveness and Satisfaction in Antenatal Care, Volume 81. Cambridge University Press, 1982: 100.

369 Sloan NL, Lederman SA, Leighton J, Himes JH, Rush D. The effect of prenatal dietary protein on birth weight. Nutrition Research 2001 Jan-Feb; 21(1-2): 129-139.

370 Rudman D, DiFulco TJ, Galambos JT, et al.. Maximal Rates of Excretion and Synthesis of Urea in Normal and Cirrhotic Subjects. J Clin Invest 1973 September; 52(9):2241-2249. PMC333026

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reduced fetus size, and delayed development. They concluded that “it is essential that in culture of the mammalian embryo, conditions are used that result in only minimal production of ammonium in the medium, thereby maintaining normal embryo function.”371 This suggests the possibility that natural selection favored reproduction of women who have the common pregnancy aversion to animal protein discussed earlier in this chapter as a protection against ammonium intoxication of any developing embryo.

As discussed briefly in the discussion of locomotion above (Chapter 4), African wild game animals typically have very little body fat. Consequently, African wild game flesh provides about 75 percent of its energy as protein. One hundred grams of wild antelope meat provides about 114 kcal and 22 g of protein. Eight hundred grams (~1.5 lb.) of this meat would provide a pregnant woman with 176 grams of protein, a dose probably toxic to the embryo she carried, but only 912 kcal, about 1600 kcal short of her energy requirements.

However, Sloan et al. reported finding decreased birth weights in women eating greater than 70 grams of protein per day,372 suggesting that excess dietary protein may exert adverse reproductive effects at levels well below the amount (3.2 g/kg) required to reach the liver’s maximal rate of urea synthesis. Since a basic diet of fruits, vegetables, legumes, nuts, and seeds can supply a woman with 50 to 60 grams of dietary protein, this would suggest that adding just 10 to 20 grams of animal protein to a diet (the amount present in 1 to 3 ounces of flesh, 1 to 3 eggs, or 10 to 20 ounces of cow milk) may have adverse effects on pregnancy outcomes.

According to the data from De Castro (Table 11.1) the birth rate in Formosa was twice that of Greece and three times that of Sweden. The animal protein intakes of these three nations (5, 15, and 63 g) represent intakes of (a) less than one, (b) two, and (c) nine ounces of flesh, respectively. Thus, De Castro’s data also suggests that as little as 1 ounce of animal flesh in the diet may markedly reduce female fertility, remarkably consistent with the findings of Sloan et al..

This data all supports the conclusion that natural selection did not prepare the female reproductive system for the high protein intake that would occur if humans had a nutritional dependence on consumption of animal flesh, eggs, or milk. It casts considerable doubt on the hypothesis that a meat- based diet drove human evolution, and supports the hypothesis that a cooked starch-based diet fueled human evolution.

Meat and Male Infertility

Researchers have also found links between consumption of animal flesh and male infertility, and consumption of fruits and vegetables and greater male fertility.

371 Lane M, Gardner DK. Ammonium Induces Aberrant Blastocyst Differentiation, Metabolism, pH Regulation, Gene Expression and Subsequently Alters Fetal Development in the Mouse. Biology of Reproduction 2003; 69; 1109–1117.

372 Sloan et al.. The effect of prenatal dietary protein on birth weight. Nutrition Research 2001 Jan-Feb; 21(1-2): 129-139.

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Mendiola et al. found that Spanish men having generalized abnormalities of sperm density, movement, and morphology consumed more full-fat milk products, eggs, pork, chicken, cold cuts, and organ meats but less lettuce, tomatoes, apricots, and peaches, compared to healthy controls.373 In a more detailed analysis they also found that healthy, fertile controls had significantly higher intakes of carbohydrates, fiber, folate, vitamin C, and lycopene (all plant-based nutrients) and lower intakes of proteins and total fat (the nutrients dominant in animal products). Semen quality was positively associated with lycopene, folate, and vitamin C intake.374

Ekenazi et al. found that non-smoking men with the highest intakes of vitamin C, vitamin E, and beta- carotene had higher sperm counts, greater sperm motility, and greater sperm concentration than men with lowest intakes of these nutrients found in fruits and vegetables.375

Some researchers believe that consumption of red meat may adversely affect male fertility by serving as sources of estrogens and xenoestrogens remaining in the flesh as a consequence of the use of hormones as growth promoters.376 However, estrogens naturally occur in all animal flesh, milk, and eggs, and the estrogen residues in meat from cattle treated with exogenous hormones do not differ significantly from those in meat from cattle not fed hormones.

According to Doyle,377 four studies have found that muscle meat from an untreated steer provides estradiol in a range of 2.8-14.4 pg/g. Two other studies found estradiol at concentrations of 12 pg/g in liver, and 12.6 pg/g in kidney. Doyle also cites an FAO report finding that meat from implanted steers had 9.7 pg/g estradiol at 15 days after implantation, and 7.3 pg/g at 61 days after implantation. In short, the levels of estradiol in hormone-treated meat falls in the normal range found in meat from untreated cattle. Doyle comments:

“Estradiol levels in edible tissues of implanted cattle are usually significantly higher than in controls but the increases are small, in the ng/kg range. The greatest increases reported in an FAO report on estradiol residues were 0.002, 0.0065, 0.005, and 0.0084 mg/kg for implanted bulls, steers, heifers, and calves, respectively. These increases are well below the FDA recommended limits listed in the table on p. 2 and well below estradiol concentrations in muscles of pregnant heifers (0.016 to 0.033 mg/kg).”

373 Mendiola J, Torres-Cantero AM, Moreno-Grau JM, et al.. Food intake and its relationship with semen quality: a case- control study. Fertil Steril 2009 Mar;91(3):812-8.

374 Mendiola J, Torres-Cantero AM, Vioque J, et al.. A low intake of antioxidant nutrients is associated with poor semen quality in patients attending fertility clinics. Fertil Steril 2010 Mar 1;93(4):1128-33.

375 Eskenazi B, Kidd SA, Marks AR, et al.. Antioxidant intake is associated with semen quality in healthy men. Hum. Reprod. 2005 April; 20 (4): 1006-1012.

376 Swan SH, Liu F, Overstreet JW, Brazil C, Skakkebaek NE. Semen quality of fertile US males in relation to their mother’s beef consumption during pregnancy. Hum Reprod 2007;22(6):1497-1502.

377 Doyle E. Human Safety of Hormone Implants Used to Promote Growth in Cattle: A Review of the Scientific Literature. Food Research Institute, University of Wisconsin Madison, WI 53706. fri.wisc.edu/docs/pdf/hormone.pdf

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Similarly, Hartmann et al. examined the “Natural occurrence of steroid hormones in food.”378 Using gas chromatography-mass spectrometry, they measured the levels of twelve steroids occurring in market- sourced meats, milk products, plants, yeast, and alcoholic beverages, including both naturally occurring and residues of additional hormones used in production. They tested beef (bull, steer, heifer), veal, pork, poultry, eggs, fish, and plants (potatoes, wheat, rice, soybeans, haricots beans, mushrooms, olive oil, safflower oil, and corn oil). They found that “Residues of steroid hormones in the tissues of calves, steers and heifers treated with estradiol and/or testosterone or progesterone are in the same order as in untreated cattle.”379

They also found significant levels of active steroids in milk products, eggs, and poultry. Based on common consumption patterns, milk products provide most of the naturally occurring dietary estrogens and progesterones in typical diets:

“Meat does not play a dominant role in the daily intake of steroid hormones... The main source of estrogens and progesterone are milk products (60-80%).”380

As for health effects of these hormones in foods, Hartmann et al. compared the intake of hormones from diet from all sources to natural human hormone production levels, concluding that the food contents of steroids are insignificant compared to endogenous production:

“These values [amounts provided by diet] are far exceeded by the human steroid production (Table 10). Children, who show the lowest production of steroid hormones, produce about 20 times the amount of progesterone and about 1000 times the amount of testosterone and estrogens that are ingested with food on average per day. It has further to be taken into consideration that about 90% of the ingested hormones are inactivated by the first-pass-effect of the liver. This leads to the conclusion that no hormonal effects, and as a consequence no tumor promoting effects, can be expected from naturally occurring steroids in food.”381

This suggests that the endogenous hormone production of a pregnant woman would have more effect on any male embryo she carried than would any hormones she ingested from foods. Based on their data, Hartmann et al. concluded:

“More effects on human beings can be expected from exposure to phytoestrogens, which occur in plants in high amounts, or by environmental chemicals with hormonal or hormone blocking

378 Hartmann S, Lacorn M, and Stienhart H. Natural occurrence of steroid hormones in food. Food Chemistry 62(1);7-20.

379 Ibid.

380 Ibid.

381 Hartmann S, Lacorn M, and Stienhart H. Natural occurrence of steroid hormones in food. Food Chemistry 62(1);7-20.

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activity such as some pesticides, polychlorinated biphenyls or dioxins, which are widespread in food and water.”382

Due to bioaccumulation, animal products generally do serve as the primary sources of pesticides and other chemicals that may affect fertility. However, animal products serve as the only dietary sources of cholesterol, and the principal dietary sources of saturated fats for most people. As documented below in Chapter 16, dietary cholesterol and saturated fats increase blood lipids in humans. As noted above in discussion of the effects of animal protein on female fertility, dietary animal products may adversely influence endogenous hormone production. Some research suggests that elevated blood lipids may adversely affect testicular function.

Padrón et al. found a link between high blood lipids (total lipoproteins and triglycerides) and poor semen quality. Most men with high blood lipids showed abnormal spermiograms, and infertile men who had no sperm in their semen had higher mean lipid levels and a greater incidence of lipid abnormalities than fertile controls. Padrón et al.’s correlation studies suggested an association between high blood lipid levels (cholesterol and/or triglycerides) and both poor semen quality and higher levels of follicle stimulating hormone (FSH). They believed that their studies “suggest that high lipid levels exert adverse direct effects at the testicular level.”383

Ergun et al. similarly reported finding a significant correlation between increased serum VLDL or triglyceride with decreased sperm motility, impaired seminal parameters, and problems with spermatogenesis.384

Attaman et al. studied men attending a fertility clinic and found that men with the highest total fat intake had a 43% lower total sperm count and 38% lower sperm concentration than men having the lowest total fat intake, and the association was driven by saturated fat intake from animal sources.385

Jensen et al. studied 701 young Danish men and reported that those with the highest intake of dietary saturated fats had impaired sperm concentration and count:

“A significant dose-response association was found, i.e., saturated fat intake above the recommended 10% was associated with a reduced sperm count and concentration. Men with the highest decile percentage of energy from saturated fat had an ~60% lower sperm concentration and total sperm count compared with men with the lowest decile intake. In addition, the percentage of spermatozoa with normal morphology was lower among men with a high

382 Ibid.

383 Padrón RS, Más J, Zamora R, et al.. Lipids and testicular function. Int Urol Nephrol 1989;21(5):515-9. Abstract. PMID: 2613482

384 Ergun A, Kose SK, Aydos K, Ata A, Avci A. Correlation of seminal parameters with serum lipid profile and sex hormones. Arch Androl 2007 Jan-Feb;53(1):21-3. Abstract. PMID: 17364460

385 Attaman JA, Toth TL, Furtado J, et al.. Dietary fat and semen quality among men attending a fertility clinic. Hum Reprod 2012; 0(0): 1-9. doi: 10.1093/humrep/des065

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percentage of energy from monounsaturated fat...The lower semen quality among men with a higher percentage of energy from saturated fat was not due to a higher total energy intake because adjustment for total energy did not change the findings.”386

This latter study holds special interest because Denmark does not allow the use of exogenous hormones in livestock.

Together, these studies suggest that animal products may exert adverse effects on male fertility by route of ingestion of excessive saturated fats, and elevation of serum lipids and FSH levels, factors independent of chemical contamination of animal products. Since evidence accumulated over the course of the past 100 years has led to the conclusion that dietary cholesterol and saturated fats increase serum lipids and the risk for cardiovascular disease in humans (Chapter 16), we can expect to find that these also produce adverse effects in other body systems.

Humans generally ingest animal protein with animal fat. Animal protein raises serum lipid levels (Chapter 16), and also may lead to increased blood levels of ammonium, as discussed above. It remains possible that high animal protein intake produces elevations of blood ammonium that interfere with male reproductive function such as spermatogenesis.

Taken together, the data discussed herein provide evidence that consumption of animal flesh has a negative impact while consumption of fruits and vegetables has a positive effect on the human male reproductive system. This pattern supports the hypothesis that human evolution was powered by a plant-based diet, and casts doubt on the hypothesis that human evolution was primarily fueled by an animal-based diet.

Summary

Humans have reproductive system characteristics significantly different from those of flesh-eating animals. We have evidence indicating that humans consuming the most animal products have reduced fertility in comparison to those consuming little or no animal products, while humans consuming the most fruits and vegetables or plant-derived nutrients have increased fertility in comparison to those consuming the least fruits and vegetables or plant-derived nutrients. We also have evidence of plausible mechanisms by which the consumption of animal protein and cholesterol may impair human reproductive capacity. In other words, we have evidence indicating that humans eating plant-based diets have Darwinian fitness superior to those eating animal-based diets. This strongly suggests that humans have a reproductive system naturally selected for a diet based on botanical fruits and vegetables with very little or no intake of animal flesh, eggs, or milk.

386 Jensen TK, Heitmann BL, Jensen MB, et al.. High dietary intake of saturated fat is associated with reduced semen quality among 701 Danish men from the general population. AJCN 2013;97:411-18.

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12: Protein Requirements

As discussed in Chapter 2, as a general rule, when a species evolves on a diet containing a large excess of a required nutrient, natural selection will favor the reproduction of individuals who have the ability to quickly metabolize and detoxify the excess of that nutrient. In contrast, when a species evolves on a diet containing a limited amount of a required nutrient, natural selection will favor the reproduction of members of that species who can minimize the need for that nutrient. Therefore, if a species has mechanisms that increase the metabolism, detoxification, and elimination of a particular nutrient, we know that its ancestors had a large supply of that nutrient; and if a species has mechanisms that allow it to minimize the use of that nutrient, we know that its ancestors had a limited supply of that nutrient.

Natural Selection of Protein Requirements

In the context of a total diet, since every mammalian cell requires glucose as a fuel source, if a species evolves on a diet supplying more amino acids and protein than absolutely required for tissue repair, but insufficient intake of glucose, natural selection will favor the survival of individuals who can very efficiently and automatically convert excess amino acids to glucose. On the other hand, if a species evolves on a diet supplying large amounts of glucose but limited protein, natural selection will favor the survival of individuals who can efficiently recycle amino acids while utilizing diet-derived glucose as fuel.

Animals biologically adapted to diets rich in high-protein animal flesh and low in carbohydrates from plant foods have high basal protein requirements because throughout their evolution they relied upon protein as a source of glucose. As explained by Carpenter:

“….carnivores must always have had a higher proportion of their energy intake from protein. Free-living deer, rabbits, and field mice, for example, all preyed on by carnivores, have given analyses indicating that at least 30% and as much as 75% of the potential energy that they provide is in the form of protein…Most studies have indicated that adult cats need to receive ~20% of their energy as protein. When fed diets of lower protein content, cats appear unable to reduce their rate of catabolism of circulating amino acids and they continue to be in negative nitrogen balance. Of course, the ability to make such reductions would have been of no value to the cat family during its evolution. The important thing was that they should be able to deaminate the very large quantity of amino acids ingested each day and, for the most part, needed only as fuel. I do not believe that it could be argued that cats truly have a greater need for protein than the grain-eating species. They simply have had a constant need to break down a greater quantity and to detoxify and eliminate the free ammonia that is released.”387

To grow and reproduce, individuals of any species must have the ability to maintain health on the lowest chronic protein intake commonly encountered when eating the foods to which the species has adapted.

387 Carpenter K. Protein requirements of adults from an evolutionary perspective. Am J Clin Nutr 1992;55:913-7.

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Probably each species has a minimum protein requirement reflecting the lowest habitual level of chronic protein consumption of its lineage.

For example, if a species occupies a niche in which it habitually eats foods which provide it with about 40 to 50 grams of protein daily when eaten in amounts sufficient to meet energy needs, natural selection will favor the reproduction of those individuals who can maintain health and fertility on the lowest chronic daily intake of protein, namely, 40 grams of protein. As a result, over a long period of time the species will consist almost exclusively of individuals who can adapt successfully to a diet that provides 40 grams of daily protein.

Human Protein Requirements

Human milk provides only 1% protein by weight yet supports the most rapid lean tissue growth phase in the life span. It seems highly unlikely that adults at any stage of life or engaged in any activity would require a net protein intake proportionally greater than what human milk provides to infants. However, since human milk protein has a very high digestibility compared to whole plant foods, and infants have a hormonal condition that makes them much more efficient at protein utilization than adults, weaned humans may require a somewhat greater gross amount of dietary plant protein in order to obtain a net intake similar to human breast milk.

An adult consuming 2400 kcal from a diet with the protein content of mother’s milk would ingest only 35 g of protein in a day. Experiments have determined that humans generally require only about 0.65 g/ kg bodyweight as protein, and that 0.8 g/kg bodyweight will cover the needs of 98 percent of the population.388 The Food and Nutrition Board of the National Academy of Sciences has stated:

“Available evidence does not support recommending a separate protein requirement for individuals who consume complementary mixtures of plant proteins.”389

On this basis the average 70 kg (154 lb.) man or 55 kg (121 lb.) woman consuming a plant-based diet would require only 56 g or 44 g of daily dietary protein, respectively.

In contrast to these recommendations, some researchers have suggested that people eating plant-based diets may require 1.0 g/kg bodyweight due to the lower digestibility of plant proteins.390 In this case a 70 kg man and 55 kg woman would need 70 g and 55 g daily dietary protein, respectively.

388 Rand WM, Pellett PL, Young VR. Meta-analysis of nitrogen balance studies for estimating protein requirements in healthy adults. Am J Clin Nutr January 2003; 77(1):109-127.

389 Food and Nutrition Board. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients). The National Academies Press, 2005. 662.

390 Kniskern MA, Johnston CS. Protein dietary reference intakes may be inadequate for vegetarians if low amounts of animal protein are consumed. Nutrition. 2011 Jun;27(6):727-30.

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However, in the 2005 edition of Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients) the Food and Nutrition Board of the National Academies stated that the lower digestibility of plant proteins does not increase protein requirements:

“Plant proteins are generally less digestible than animal proteins; however, digestibility can be altered through processing and preparation. Therefore, consuming a varied diet ensures an adequate intake of protein for vegetarians.”391

Data from free living populations may cast some doubt on claims that people eating plant-based diets have higher dietary protein requirements than flesh-eaters. Some populations in New Guinea have maintained nitrogen balance and health on diets containing only 20 to 25 g protein daily, just 3% of total energy, primarily from sweet potatoes containing only 1-2% protein (wet weight).392, 393 Medical personnel described them as “lean, physically fit, and in a good nutritional state;” 76 percent of the men achieved ‘good’ or ‘superior’ scores on the Harvard Pack Test of physical fitness, and scores did not fall with age.394 Some evidence suggests that these people may obtain some of their required protein from symbiotic colonic flora, raising the possibility that people consuming diets very high in plant foods providing fermentable carbohydrates have a lower dietary requirement for protein.395

Based on this evidence it seems likely that human metabolism evolved in response to a habitual diet that generally supplied in the vicinity of 1.0 g (0.8 to 1.2 g) protein/kg body weight, with some of this possibly coming from intestinal flora, while meeting total energy requirements largely with carbohydrate. Physically active individuals will naturally consume more total food, and so long as they consume whole foods, they will consume additional protein as a matter of course. I will discuss this further below.

391 Food and Nutrition Board, NAS. Dietary Reference Intakes for...(Macronutrients). NAP, 2005. 662.

392 Oomen HAPC. Interrelationship of the human intestinal flora and protein utilization. Proceedings of the Nutrition Society, December 1970; 29(2): 197-206. doi:10.1079/PNS19700046

393 Sinnett P, Whyte M. Papua New Guinea. In: Western Diseases: Their emergence and prevention. Ed. by H. Hubert Carey Trowell and Dennis Parsons Burkitt. Harvard University Press, 1981. 174.

394 Sinnett PF, Whyte HM. Epidemiological studies in a total highland population, Tukisenta, New Guinea: Cardiovascular disease and relevant clinical, electrocardiographic, radiological and biochemical findings. J Chron Dis 1973; 26:265-290.

395 Oomen, op. cit.

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Plant-Based Protein

Human protein requirements match the protein delivery of a plant-based diet. As shown in Table 12.1, many plant foods have a protein density similar to or greater than human milk, and any diet providing sufficient energy from any single plant food, or any common mix of raw vegetables, legumes, nuts, seeds, and fruits, can provide well more than 50 g of protein.

Table 12.1: Protein in human milk and non-animal foods. Food Protein, % dry weight Protein, % wet weight Protein, g per 2400 kcal Milk, human 8 1 35 Yeast, nutritional 53 N.A. 340 Spinach 30 3 300 Lettuce, romaine 24 1 174 Peas, green, raw 24 8 160 Kale 25 4 156 Pumpkin seeds 32 30 130 Tomatoes 20 1 120 Oats, dry 18 17 102 Wheat, dry 15 15 90 Almonds 22 21 90 Onions 11 1 66 Corn, sweet, raw 10 3 60 Carrots 8 1 54 Potatoes 9 2 54 Rice, brown, boiled 7 1 48 Oranges 8 1 42 Bananas 4 1 30 Apples 2 0 12 Source: USDA Food Nutrient Database

Many people believe that plant foods all lack some of the essential amino acids. In fact, excluding some sweet fruits, most single plant foods consumed in adequate quantity to meet caloric needs will supply adequate amounts of all essential amino acids.396 Studies using single plant foods such as potatoes or wheat to supply protein to malnourished children have demonstrated that these foods provide all the essential amino acids in adequate amounts to support growth and development equal to milk protein if

396 McDougall J. Plant Foods Have a Complete Amino Acid Composition. Circulation 2002;105:e197. McDougall J. Misinformation on Plant Proteins. Circulation 2002;106:e148.

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consumed in adequate quantities to meet energy requirements.397 Based on these and other experiments, Millward, one of the leading authorities on human protein requirements, has stated:

“….we can reasonably safely conclude that, with the exception of some starchy roots, plant- based diets available in most parts of the world are capable of providing adequate protein for all ages.

“….it is clear that meat-free, largely plant-based diets available in developed countries can supply protein in the amount and quality adequate for all ages. In developing countries the protein issues relate mainly to low protein levels in some staples (taro, yams and cassava etc.), but cereal-based diets, especially those based on wheat and maize, supply protein levels considerably above the requirement level.”398

Assuming a requirement of 0.65 to 1.0 g/kg bodyweight, a 70 kg moderately active adult male with a energy requirement of about 2800 to 3000 kcalories daily would need 46 to 70 g of protein daily. Tables 12.2 and 12.3 display the protein and amino acid contents of a plant-based diet consisting entirely of fresh fruits, vegetables, nuts, and seeds.

Table 12.2: Protein content of a 2800 kcal raw plant-based diet for a 70 kg male. Food Measure Kcal Protein (g) Oranges 4 whole (2-7/8” dia) 274 5 Bananas 6 med (7” to 7-7/8”) 630 8 Apples 4 med (3” dia) 378 2 Grapes 2 cups 208 2 Kale, raw 4 cups 131 9 Tomatoes 4 med (2-3/5” dia) 89 4 Avocados, California 1 fruit w/o skin or seed 227 3 Lettuce, romaine 1/2 head 53 4 Pumpkin seeds 2 oz (28 g) 316 17 Corn, sweet, white, raw 2 cups kernels (308 g) 249 10 Peas, green, fresh, raw 2 cups (145 g) 235 16 Total 2793 79 Calculated using USDA data and Cronometer (www.cronometer.com).

By any standard discussed above, this diet supplies adequate energy and protein (1.1 g/kg) and surpasses all essential amino acid requirements for a 70 kg (154 lb.) moderately active male. A larger or more

397 Millward DJ. The nutritional value of plant-based diets in relation to human amino acid and protein requirements. Proceedings of the Nutrition Society, May 1999;58(2): 249-260. doi:10.1017/S0029665199000348

398 Ibid.

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active individual would consume more food to meet his higher energy requirements and would as a matter of course also consume a larger absolute amount of protein (see next section). Increasing the kcaloric proportion of leafy greens, legumes, grains, seeds, and nuts while decreasing that of fleshy fruits (particularly avocado) can easily augment the proportion of energy derived from protein if so desired. Please note that I used only foods edible raw in this menu only to illustrate the point; I do not intend this as a prescription to consume only raw foods or an endorsement of strictly raw food diets.

Table 12.3: Amino acid delivery of diet in Table 12.2 Amino acid Amount (g) Percent of recommended value Cystine 0.7 268.0 Histidine 2.1 310.0 Isoleucine 2.9 213.0 Leucine 5.3 199.0 Lysine 3.8 185.0 Methionine 1.1 166.0 Phenylalanine 3.5 408.0 Threonine 2.7 263.0 Tryptophan 0.9 314.0 Tyrosine 2.0 235.0 Valine 3.6 205.0 Calculated using USDA data and Cronometer (www.cronometer.com).

Plant-Based Protein For Athletes

The Food and Nutrition Board of the National Academies found no compelling evidence for a higher protein requirement for physically active individuals:

“In view of the lack of compelling evidence to the contrary, no additional dietary protein is suggested for healthy adults who undertake resistance or endurance exercise.”399

Regarding athletes eating plant-based diets, the American College of Sports Medicine (ACSM) has claimed:

399 Food and Nutrition Board, NAS. Dietary Reference Intakes for...(Macronutrients). NAP, 2005. 661.

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“Because plant proteins are less well digested than animal proteins, an increase in intake of about 10% protein is advised (15). Therefore, protein recommendations for vegetarian athletes approximate 1.3 to 1.8 g/kg/day (52).”400

To support the claim that plant-based athletes need 10% more protein than meat-eaters, the ACSM refers (by note 15) to the National Academies Press publication, Dietary Reference Intakes: The Essential Guide to Nutrient Requirements.401 I was unable to find any support for that claim in that text. In fact, there you will find the following two statements:

“However, vegetarian diets that include complementary mixtures of plant proteins can provide the same quality of protein as that from animal proteins. Available evidence does not support recommending a separate protein requirement for individuals who consume complementary mixtures of plant proteins.”402

“However, since compelling evidence of additional need is lacking, no additional dietary protein is suggested for healthy adults who undertake resistance or endurance exercise.”403

In discussing foods, Dietary Reference Intakes (2006) makes no mention of lesser digestibility, although it does make the incorrect claim that plant proteins “tend to be deficient in one or more of the indispensable animo acids,” 404 a claim that does not fit the facts, shown in the previous section.

The ACSM’s range for the protein requirements of plant-based athletes lacks precision, suggesting that requirements may vary by as much as 38%. It suggests that a 70 kg man eating a plant-based diet could need anywhere from 91 g to 126 g of protein daily, but offers no method by which an individual can determine his/her requirement within this range, except to suggest that the lower end of this range applies to endurance athletes and the upper end to strength and speed athletes.

Phillips reviewed research investigating the protein turnover and requirements of people involved in strength sports.405 He found that while some studies suggest that athletes involved in resistance training or strength sports have greater protein requirements than sedentary individuals, others have “suggested that exercise results in a more economic use of protein and may actually reduce protein

400 American Dietetic Association, Dietitians of Canada, American College of Sports Medicine, et al.. American College of Sports Medicine position stand: Nutrition and athletic performance. Journal of the American Dietetic Association 2009;109(3):509-527.

401 Otten J, Hellwig J, Meyers L, eds. Dietary Reference Intakes: The Essential Guide to Nutrient Requirements. National Academies Press, 2006.

402 Ibid., 150.

403 Ibid.

404 Ibid, 151.

405 Phillips SM. Protein requirements and supplementation in strength sports. Nutrition 2004 Jul 1;20(7):689-695.

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requirements.”406 In addition, he reports that the studies indicating elevated requirements (~1.5 g/kg/ day) involved individuals unaccustomed to resistance training, whereas studies of experienced trainees (more than 12 days of training) have found lower requirements (~1.05 g/kg/day). In his estimation:

“After an initiation phase of any resistance training program and the initial adaptation to the performance of exercise are over, it is hard to reconcile that resistance-trained athletes would have markedly elevated protein requirements.”407

Phillips also notes that for athletes seeking positive nitrogen balance, “Landmark studies have clearly demonstrated that energy intake may be as, if not more, important than protein intake in determining nitrogen balance.”408

“What these early, elegantly designed studies showed was that, even when no protein is consumed, increasing energy intake improves nitrogen balance. Conversely, even when consuming relatively high protein intakes, positive nitrogen balance was not possible until energy balance was positive; however, exercise modified this relation and actually increased nitrogen balance, even in the face of a deficit in energy balance.”409

Finally, Phillips notes that “In terms of macronutrients that support nitrogen retention, isoenergetic substitutions of fat for carbohydrate have clearly shown that carbohydrate is protein sparing.”410 In other words, a high protein intake provides little benefit to athletes unless accompanied by a high carbohydrate intake.

This indicates that humans have a naturally selected requirement for plants, the primary sources of carbohydrates, to support positive protein balance. It also suggests that our ancestral diet more reliably supplied carbohydrate than fat (otherwise, natural selection would have favored reproduction of humans for whom dietary fat would be more protein-sparing than carbohydrate). Hence plants, particularly legumes in combination with high protein leaves, are the ideal protein sources for humans engaged in sports training because they combine carbohydrate with protein, whereas animal flesh (except for milk products) lacks the carbohydrate required to support a positive nitrogen balance.

Phillips believes that “a ‘safe’ level of protein intake for strength-trained athletes is 1.33 g/kg/d”411 but notes that this estimate is based on nitrogen balance studies, which have serious flaws. As noted by Phillips and the Food and Nutrition board, studies showing positive nitrogen balances at protein intakes

406 Ibid., 694.

407 Ibid., 693.

408 Ibid., 692.

409 Ibid.

410 Ibid.

411 Ibid., 694.

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greater than 1.1 g/kg predict very large increases in lean body mass, on the order of 300 g/day, in those eating the higher protein diets, but those increases did not take place, and, in fact, subjects eating adequate protein diets usually had improvements in strength and muscle mass similar to those eating additional protein.412, 413

Carbohydrate, not protein or fat, provides the fuel to support resistance training or other high intensity activities. Therefore, resistance training athletes would need additional protein only to support repair and accrual of muscle mass. One pound of muscle tissue (75% water) contains about 114 g of protein. Adding one pound of muscle to the body in the course of a month (12 pounds in a year, a relatively high rate of gain) therefore requires consumption of only 4 additional grams of protein daily above basal (sedentary) requirements. Assuming some additional need for repair of tissue damaged by training, we can double this to 8 g daily.

At the beginning of the month, a 70 kg (154 lb.) male would require 64 g of protein daily (56 g basal, plus 4 g/d to repair training-induced damage and 4 g/d to support the lean mass gain), and at the end of the month, now weighing 70.5 kg, his requirement would be 64.4 g/d. If he continued this for 12 months, at the end of the year he would weigh 75.5 kg (166 lb.) and his daily protein requirement would be 68.4 g. It seems likely that a daily protein intake of 1.0 to 1.1 g/kg would at any point in this process probably more than suffice for accrual of lean mass up to the individual’s genetically determined potential, provided that he maintained an adequate total carbohydrate intake throughout.

Tarnopolsky reported on the protein requirements for endurance athletes.414 Tarnopolsky emphasized that adequate carbohydrate (plant food) intake prevents use of protein for fuel during endurance exercise. This indicates again that natural selection has produced a human muscle metabolism dependent upon plant foods. According to Tarnopolsky:

“For the well-trained endurance athlete training 4 to 5 d/wk for longer than 60 min, there appears to be a very modest increase in dietary protein requirements of only 20% to 25% [i.e. 1.0 g/kg/d]. for the top sport elite endurance athlete, the increase in dietary protein intake may be up to 1.6 gPRO/kg/d.”415

The “top sport elite endurance athletes” include Tour de France cyclists and others who may train 10 to 12 hours per week or more. Needless to say, these people do not represent the energy or protein requirements of human ancestors engaged in normal activities of daily living. These athletes would need very high total food energy intakes to support their training, such as 4000 kcal per day. A plant- based diet can easily meet their increased needs.

412 Ibid., 692.

413 Food and Nutrition Board, NAS. Dietary Reference Intakes for...(Macronutrients). NAP, 2005. 661.

414 Tarnopolsky M. Protein Requirements for Endurance Athletes. Nutrition 2004;20(7):662-68.

415 Ibid.

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Regardless of training status (novice or experienced), a plant-based athlete can easily obtain a more than adequate protein intake. For example, 50 slices of whole wheat bread supplies 4032 kcal and 199 g of protein; 35 cups of green peas provides 4110 kcal and 275 g of protein; respectively, for a 70 kg athlete, 2.8 and 3.9 gPRO/kg, intakes 1.8 and 2.4 times the level that Tarnopolsky identifies as adequate for the elite endurance athlete. A 50:50 mix of these two foods would provide the athlete with 237 g protein, or 3.4 g/kg for a 70 kg individual, more than double the maximal protein requirement of an elite endurance athlete according to Tarnopolsky.

Similarly, an 80 kg strength athlete would require at least 3000 kcal per day. Twenty-six cups of raw green peas provides 3054 kcal, 204 g protein, and all essential amino acids in amounts 4 to 7 times requirements of sedentary individuals; 10 cups of oats provides 3070 kcal, 107 g protein, and all essential amino acids in amount 2.5 to 13 times the requirements for a sedentary individual. Peas and oats, as single food sources, provide 2.6 and 1.34 g PRO/kg bodyweight for an 80 kg individual eating 3000 kcal per day. A 50:50 mix of these two foods would provide 3062 kcal and 155 g protein, amounting to 1.9 g/kg for an 80 kg athlete, well exceeding the 1.33 g/kg level that Phillips suggested might serve as the optimum for strength athletes.

I have chosen simple examples to illustrate this point. A more varied diet can provide similar or greater levels of energy and protein so long as it emphasizes legumes, green leafy vegetables, seeds, and nuts.416 I have provided an example from my own diet in Table 12.4. Without intention, on October 10, 2013 I obtained 120 g of protein (1.7 g/kg) from my plant-based diet. Notice also that on this day, I consumed 3.2 kg of total food, more than double what Brand-Miller and Holt considered an amount that a human would require virtually the whole day to consume (Chapter 7). In fact on this day I spent 8 hours in my office seeing patients, and devoted no more than 1.5 hours consuming my meals and snacks.

416 Fuhrman J and Ferreri DM. Fueling the vegetarian (vegan) athlete. Curr Sports Med Rep 2010;9(4):233-241.

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Table 12.4: A high protein plant-based diet that I consumed on October 10, 2013.

Food Quantity (g) Kcal Protein (g)

Beans, pinto, boiled 1.5 cups (257) 367 23

Ezekial 4:9 sprouted grain tortilla 1 tortilla (57) 150 6

Lettuce, romaine 0.5 head (313) 53 4

Corn, sweet, yellow, raw 1 cup (145) 125 5

Orange juice, raw 1 cup (248) 112 2

Mangos, raw 1.5 cup (248) 149 2

Raspberries 1 cup (123) 64 2

Lentils, boiled 2 cups (396) 459 36

Bananas, raw 5 medium (590) 525 6

Soymilk 2 cups (486) 199 14

Oats, regular, dry 1 cup (81) 307 11

Raisins 0.25 cup (41) 123 1

Kale, raw 3 cups (201) 98 9

Totals 3186 g 2731 121

Calculated using www.cronometer.com

Wild Plants Could Satisfy Human Protein Needs

Eaton et al. reported that the set of wild plant foods they used to estimate the nutrient intakes of paleolithic foragers provided 129 kcal and 4.1 g protein per 100 g.417 Brand-Miller and Holt give values of 167 and 6, respectively, for 829 wild plant foods available to Australian Aborigines.418

Using the figures from Eaton et al.., a 70 kg male H. erectus requiring 2705 kcal per day (as suggested by Ben-Dor et al.419) could have obtained 86 g of protein, or 1.23 gPRO/kg from a plant-based diet consisting of wild foods. Using the figures from Brand-Miller and Holt, this individual could have obtained 97 g of protein, or 1.39 g PRO/kg from a wild plant-based diet. These levels exceed all of the recommendations given above for people eating plant-based diets and engaged in normal activities of

417 Eaton and Konner. Paleolithic Nutrition. NEJM 1985 Jan 31;312(5):283-289. Table 2.

418 Brand-Miller and Holt. Australian Aboriginal plant foods. Nutrition Research Reviews 1998;11:5-23.21.

419 Ben-Dor et al.. Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

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daily living, including those that recommend an increased intake due to lower plant-protein digestibility. They also exceed the levels recommended for experienced endurance and strength athletes (about 1.1. g/ kg, as discussed above), by 12% and 26%, plenty to cover any increased need due to lower digestibility of plant foods.

These figures assume that foragers ate equal portions of the various foods included in the two data sets. Some of those have higher and some lower protein contents. We don’t know the full complement of plant foods available to stone age hominins, nor their nutritional compositions. Stone age hominins may have preferred and consumed higher proportions of plants that had higher protein levels than the average of either of these data sets. Nevertheless, this data does not support any claims that stone age hominins could not meet their protein requirements eating plant-based diets. On the contrary, the data suggests that stone age hominins could have easily obtained adequate protein from wild plants alone so long as they obtained adequate total food intake.

Methionine and Cystine

Presumably, the amino acid composition of human milk arose from natural selection of the mix that best supports human health, growth, and development. Humans have a dietary requirement for the sulfur- containing amino acids methionine and cysteine. Our cells can use methionine to produce cysteine, so dietary intake of cysteine reduces the methionine requirement. Foods provide cysteine primarily in the form of cystine, the dimer of cysteine.

Human milk provides 0.3 mg of methionine per kcalorie, and methionine and cystine each make up about 2 percent of the total protein, producing a 1:1 ratio of these two amino acids. Animal proteins supply a greater amount of methionine per kcal, and generally tend to have a higher methionine-to- cysteine ratio, in comparison to both human milk and plant foods (Table 12.5).

The 7 animal foods listed in this table have an average of 3.5 mg methionine (Met) per kcalorie, or about 11 times that of human milk. The 14 plant foods have an average of 0.8 mg Met/kcal, or about 3 times that of human milk. The animal and plant proteins have mean Met/Cys ratios of 2.3 and 1.3, respectively. This means that as the proportion of animal foods in the total diet increases, the methionine dose increases and the cysteine dose decreases, and as the proportion of plant foods increases, the methionine dose decreases and the cysteine dose increases. As shown in Table 12.3, the menu in Table 12.2 has a Met/Cys ratio of 0.61. In short, the methionine and cysteine contents of plant proteins or plant based diets generally more closely resemble those of human milk than do those of animal proteins or animal based diets.

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Table 12.5: Methionine and cystine in animal and plant proteins

Food Met (mg/kcal) Met (mg/g protein) Cys (mg/g protein) Met/Cys

Animal Proteins

Cow milk 1.3 25 6 4

Salmon 4.5 29 11 3

Chicken 5.2 28 13 2

Lamb 2.3 25 12 2

Pork, loin 5.0 26 12 2

Beef, round 3.9 26 13 2

Egg, chicken 2.6 29 21 1.4

Human milk 0.3 21 19 1

Plant Proteins

Corn (fresh) 0.8 16 8 2

Peas (fresh) 1.0 15 6 2.5

Lettuce, cos or romaine 0.8 13 5 2.6

Spinach 2.2 19 12 1.6

Lentils 0.7 8 13 0.6

Corn (dried) 0.5 21 14 1.5

Wheat 0.7 15 23 0.7

Oats 0.8 19 24 0.8

Kale 0.6 9 12 0.8

Peas (dried) 0.7 12 28 0.5

Soybean (dried) 1.3 13 16 0.8

Orange 0.4 20 10 2.0

Banana 0.1 8 9 0.9

Date 0.1 10 28 0.4

Source: Calculated from USDA data provided by Cronometer.com.

PROTEIN REQUIREMENTS – 161

The body can only produce cysteine from methionine via a path that involves production of an intermediate compound called homocysteine (Hcy), but it can’t convert cysteine into methionine or Hcy by any path. It appears that we benefit by obtaining cysteine directly from the diet because this reduces the conversion of Met to Hcy. Dietary studies have linked the absolute amount of dietary methionine (Met) and Met-derived Hcy to reduced lifespan and age-related diseases.420 Dietary Met restriction without kcalorie restriction extends lifespan in Drosophila and rodents,421 and selectively blocks cancer proliferation in humans because malignant cells have a greater Met dependency and requirement than normal cells.422 Met-derived Hcy promotes atherosclerosis,423 serves as a risk factor for cancer and a potential tumor marker,424 and may contribute to diabetic neuropathy,425 hypertension,426 and osteoporosis.427 Evidence from epidemiological, experimental, and clinical trials indicates that diets rich in animal flesh, and therefore Met, promote atherosclerosis, cancer, diabetes, hypertension, osteoporosis, and neurological diseases, while plant-based diets prevent, stall, or reverse these diseases.428, 429

Pamplona and Barja discuss the various lines of evidence suggesting that excess dietary methionine derived from dietary animal protein promotes premature aging in humans:

“Interestingly, we have recently found that methionine is the only amino acid present in heart intracellular proteins that strongly correlates with mammalian MLSP [maximum life span], and that this correlation is negative [81] (Fig. 2). Moreover, protein methionine content is also lower in tissues of long-lived birds than in short-lived mammals of similar body size [82] and [131]. Thus, the longer the life span of a species, the lower is its tissue protein methionine content. Many other recent investigations also point to a relationship between methionine and aging [132], [133], [134] and [135]. In addition, excessive methionine dietary supplementation

420 Schloss JV. On the Origin of Western Diet Pathologies. Nature Precedings 07/2010; DOI:http://hdl.handle.net/10101/npre. 2010.4641.1.

421 Grandison RC, Piper MDW, Partridge L. Amino acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 2009 Dec 24; 462:7276.

422 Cellarier E, Durando X, Vasson MP, et al.. Methionine dependency and cancer treatment. Cancer Treatment Reviews 2003;29:489-499.

423 McCully KS. Homocysteine, vitamins, and vascular disease prevention. Am J Clin Nutr 2007 Nov;86(5):1563S-1568S.

424 Wu LL, Wu JT. Hyperhomocysteinemia is a risk factor for cancer and a new potential tumor marker. Clinica Chimica Acta 2002 Aug 1;322(1):21-28.

425 Wile DJ, Toth C. Association of Metformin, Elevated Homocysteine, and Methylmalonic Acid Levels and Clinically Worsened Diabetic Peripheral Neuropathy. Diabetes Care 2010 Jan 1:33(1):156-161.

426 Stehouwer CDA, van Guldener C. Does Homocysteine Cause Hypertension? Clin Chem Lab Med 2003;41(11): 1408-1411.

427 Herrmann M, Widmann T, Herrmann W. Homocysteine - a newly recognized risk factor for osteoporosis. Clin Chem Lab Med 2005; 43(10):1111-1117.

428 Campbell TC. Dietary protein, growth factors, and cancer. Am J Clin Nutr 2007 June; 85(6):1667.

429 Campbell TC, Campbell TM II. The China Study: starling implications for diet, weight loss, and long term health. Dallas, TX: BenBella Books, Inc, 2005.

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damages many vital organ systems and increases tissue oxidative stress. Thus, methionine supplementation increases plasma hydroperoxides and LDL-cholesterol [136], raises iron and lipid peroxidation, conjugated dienes, and cholesterol in rat liver [137] and [138], is hepatotoxic and alters liver antioxidants like SOD, catalase, GSH-peroxidase and GSH in rats [137], [139] and [140], increases liver oxidative stress [140], raises plasma, heart and aortic homocysteine levels leading to angiotoxicity and mitochondrial degeneration in arterial smooth muscle cells [136], [140] and [141] and accelerated aging of rat vascular system [142], induces hypertension and coronary disease [140] and [143], decreases vitamin E levels in liver and heart [136], and possibly speeds up brain aging [139]. The high methionine content of the Western diet may also predispose human beings to cardiovascular disease [139]. Interestingly, similar negative effects of methionine supplementation have been described in rats fed high protein (50%) and high methionine (2%) diets for 2 years [142]. High protein diets (50% protein for 1 week), and casein- rich compared to soybean-rich diets, increase plasma protein carbonyls and are cholesterolemic and atherogenic in rats [136] and [144], which is interesting because casein has higher methionine content than soybean protein, and because protein oxidation seems to play a role in atherosclerosis and other degenerative diseases [145].”430

This information suggests that long-lived species, such as humans, require low tissue concentrations of methionine to achieve their long life spans. This would explain why human milk has a relatively low methionine concentration. It seems that natural selection favored the reproduction of long-lived humans having low tissue concentrations of methionine by route of consuming a plant-based diet, and the diseases of civilization arise in humans who eat an animal-based, methionine-rich diet discordant with this genetic endowment.

Taken together, the information in this section all points to humans having a protein metabolism adapted to a diet having a low absolute amounts of methionine and relatively high amounts of cysteine, similar to human milk. A diet of whole plant foods has this characteristic. It also suggests that humans have a protein metabolism poorly adapted to diets containing significant quantities of animal flesh and its constituent proteins.

Summary

In summary, humans display a clear metabolic adaptation to a protein intake and dietary amino acid profile similar to what a strictly plant-based diet can provide, and do not have the type of obligatory amino acid oxidation pattern found in species adapted to diets containing significant amounts of animal flesh.

430 Pamplona R, Barja G. Mitochondrial oxidative stress, aging and caloric restriction: The protein and methionine connection. Bioenergetics 2006 May-Jun:1757(5-6):496-508.

PROTEIN REQUIREMENTS – 163

13: Vitamin C, Uricase, and Uric Acid

All animals adapted by natural selection to eating flesh as a principal part of the diet produce their own vitamin C, a nutrient very poorly supplied by most animal flesh. They also produce an enzyme, uricase, which metabolizes uric acid to less toxic compounds. Vitamin C and uricase both reduce the accumulation of uric acid in the blood.

Unlike other mammals, humans and other primates cannot produce vitamin C, due to a genetic mutation that occurred 30 to 40 million years ago.71 We do not produce ascorbic acid for lack of activity of one enzyme, L-gulonolactone oxidase, present in other species. Only a species that specialized in consuming a diet rich in fruits and vegetables could tolerate this mutation, since nuts, seeds, animal flesh, fat, and eggs are all poor sources of vitamin C.

If humans had the same ability to produce vitamin C as found in non-primates, our liver would make two to four grams of it daily.431 A free-living primate similar in size to a human would consume from wild raw fruits and vegetables approximately two to six grams of vitamin C daily,432 roughly equivalent to what our liver would produce if it had the required enzyme. This suggests that our pre-human ancestors could thrive without the ability to produce vitamin C because their diet of fruits and vegetables provided the physiologically appropriate amount (along with uncounted synergistic factors). It also raises the question as to whether our physiology may require an intake of fruits and vegetables (not isolated ascorbic acid) capable of supplying as much as two to four grams of ascorbic acid daily.433 A diet must consist largely or exclusively of vegetables and fruits to obtain more than 500 mg of vitamin C daily.

Also unlike other mammals, humans and other primates lack uricase, an enzyme that metabolizes uric acid, due to knock-out of the uricase-coding gene 10 to 15 million years ago.434 Primates lacking this enzyme would have a toxic accumulation of uric acid in the blood, leading to gout, if they weren’t eating adequate fruits and vegetables rich in vitamin C, which reduces uric acid concentrations.435

431 Stone I. The Natural History of Ascorbic Acid in the Evolution of the Mammals and Primates and Its Significance for Present Day Man. Orthomolecular Psychiatry, 1972; 1 (2 and 3): 82-89.

432 Milton K. Nutritional characteristics of wild primate foods: Do the diets of our closest living relatives have lessons for us? Nutrition 1999; 15(6): 488-498.

433 Trials have not found benefit to supplementing the diet with high doses of isolated ascorbic acid for any particular condition and probably never will; while some trials suggest harm. High vitamin C intake among non-human primates serves as a marker for high intake of vegetables and fruits supplying a myriad of synergistic nutrients. Beneficial effects can only arise from ingesting the whole foods, not single isolated chemicals, because our physiology adapted to the complexes found in whole foods, not to isolated chemicals.

434 Johnson RJ, Andrews P, Benner SA, and Oliver W. The Evolution of Obesity: Insights from the Mid-Miocene. Trans Am Clin Climatol Assoc. 2010; 121: 295–308.

435 Huang, H.-Y., Appel, L. J., Choi, M. J., Gelber, A. C., Charleston, J., Norkus, E. P. and Miller, E. R. The effects of vitamin C supplementation on serum concentrations of uric acid: Results of a randomized controlled trial. Arthritis and Rheumatism (2005); 52 (6): 1843–1847.

165

Natural selection may have favored reproduction of primates lacking uricase activity because higher uric acid levels can raise blood pressure. A diet consisting of fruits and vegetables provides very large amounts of potassium and vitamin C, but very little sodium; whereas animal tissues provide little vitamin C and larger amounts of sodium relative to potassium (Table 13.1). A diet with a high ratio of potassium to sodium tends to reduce blood pressure; and a diet with a high ratio of sodium to potassium tends to increase blood pressure. Those mutant frugivorous primates who had lost the uricase-coding gene may have had an advantage of more optimal blood pressure by maintaining higher levels of uric acid in the face of very high intake of vitamin C and potassium.90

Table 13.1: Potassium:Sodium Ratio (K:Na) in Common Plant and Animal Tissues (100 g Portions) Food Potassium (K), mg Sodium (Na), mg K:Na Ratio Banana 358 1 358 Wheat, whole, flour 363 2 180 Orange 166 1 166 Apple 107 1 107 Rice, brown, cooked 154 2 75 Potato, white, raw 421 6 70 Avocado 507 8 63 Tomato 237 5 47 Lettuce 247 8 30 Sweet potato, baked 475 36 13 Chicken, ground, raw 522 60 8 Salmon, Chinook, raw 352 74 5 Beef, grass fed, raw 289 68 4 Cow milk 132 43 3 Chicken egg, raw 114 125 0.9 Source: USDA, Cronometer.com

Loss of uricase has other metabolic consequences. Elevated serum uric acid also appears to promote general inflammation,436 increase the risk of cardiovascular disease,437 and facilitate the storage of body fat.90

Animal flesh provides purines, which feed the production of uric acid, but essentially no vitamin C. Animals well-adapted to eating flesh produce both uricase and vitamin C in their own tissues. Since

436 Shi Y. Caught red-handed: uric acid is an agent of inflammation. J Clin Invest. 2010 June 1; 120(6): 1809–1811.

437 Leyva F, Anker SD, Godsland IF, et al.. Uric acid in chronic heart failure: a marker of chronic inflammation. European Heart Journal (1998); 19 (12): 1814-1822.

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both uricase and vitamin C reduce uric acid levels, these abilities allow them to eat meat-rich diets without suffering gout, cardiovascular disease, high blood pressure, inflammation, and obesity.

Thus, primates including humans have a metabolism specifically adapted to plant foods low in purines and sodium, but high in vitamin C and potassium; and poorly adapted to animal flesh, which richly supplies sodium and purines, but poorly supplies vitamin C and potassium. Humans and other apes have naturally selected metabolic systems geared to increase blood pressure as an adaptation to a plant-based diet that drives blood pressure down. If you take away the fruits and vegetables, or add sodium- and purine-rich foods (like animal flesh) these systems continue to drive blood pressure up, producing so- called ‘essential’ hypertension. Among Caucasian Adventists, vegans had the lowest risk of hypertension, followed by lacto-ovo vegetarians, partial vegetarians, and omnivores.438 This suggests that every replacement of plant food with animal food increases the risk of hypertension.

On the one hand, it appears that the loss of uricase may have helped human ancestors thrive on a primarily frugivorous diet. On the other hand, it also made the primate lineage (including modern humans) physiologically dependent on a plant-based diet rich in vitamin C and potassium to maintain safe levels of uric acid to prevent high blood pressure, obesity, chronic inflammation, and cardiovascular disease.

Gout In Traditional Meat-Based Cultures

“Traditional” populations eating diets composed largely of wild or grass-fed animal products seem to have had a propensity to suffer gout. In 1925, Kuczynski reported that the Kirghiz nomads who lived almost exclusively on grass-fed animal products frequently suffered gout.439 Inupiat Eskimos have a prevalence rate of gout similar to those of the general U.S. population.440 Lane describes gout as “a common illness among the Mongols”441 who lived on flesh and milk from free-ranging grass-fed animals.

In Europe and the U.S.A. prior to the 20th century, almost all animal flesh consumed came from wild or grass-fed animal products. Medical letters and textbooks from the 18th and 19th centuries consistently reported that gout occurred rarely or never in people eating plant-based diets but frequently in people eating animal-based diets, and that a plant-based diet reliably cured the disease.

438 Pettersen BJ, Anousheh R, Fan J, Jaceldo-Siegi K, Fraser GE. Vegetarian diets and blood pressure among white subjects: results from the Adventist Health Study-2. Public Health Nutr 2012 Oct; 15(10): 1909-1916.

439 Bernstein FL, Burton C, Healey D. Soviet Medicine: Culture, Practice, Science. Northern Illinois University Press, 2010. 75.

440 Boyer GS, Lanier AP, Templin DW. Prevalence rates of spondyloarthropathies, rheumatoid arthritis, and other rheumatic disorders in an Alaskan Inupiat Eskimo population. J Rheumatol 1988 Apr;15(4):678-83.

441 Lane G. Daily Life in the Mongol Empire. Greenwood Press, 2006. 137

VITAMIN C, URICASE, AND URIC ACID – 167

A 1792 “Dissertation on the Gout” states: “The most proper means of prevention seems to be (unless your exercise is strong and laborious) to eat sparingly of animal food; together with a proper quantity of vegetables.”442

In an 1821 medical text, Thomas states:

“The use of animal food and other analogous aliments tends to diminish the quantity of urine at the same time that it increases the proportion of uric acid, whereas a vegetable diet has the contrary effect.”443

“Men who are employed in constant bodily labour, or who live much upon vegetable food, as well as those who make use of wine and other fermented liquors very sparingly, are not often afflicted with the gout.”444

“A full diet of animal food, ragouts, and rich sauces, with a free use of spirituous and fermented liquors, particularly of wines abounding with tartar, together with indolence and inactivity, are the causes which give rise to corpulency and a full habit of body; hence the frequency of gout among the rich.”445

“Gout, when in the system, and not regularly formed, requires an excess of animal food to drive it to the extremities.”446

“While the vigour of the system still remains unimpaired, either by intemperance or frequent attacks of gout, and abstinence from animal food may be entered upon with safety, in order to prevent a recurrence of the disease.”447

In an 1823 text on gout, Wilson states: “A constant, full, or excessive diet of animal food has also a powerful tendency to excite gout, in persons predisposed to its attacks.”448

In an 1840 medical textbook, Budd states:

442 Author unknown. Dissertation on the Gout. The Gentleman’s Magazine, and Historical Chronicle 1792 April. 312.

443 Thomas R. The Modern Practice of Physic, Exhibiting the Character, Causes, Symptoms, Prognostics, Morbid Appearances, and Improved Method of Treating the Diseases of All Climates, 7th Ed.. London: Longman, 1821. 772.

444 Ibid., 198.

445 Ibid., 199.

446 Ibid., 210-211.

447 Ibid., 217.

448 Wilson C. Observations on gout and rheumatism, including an account of a speedy, safe, and effectual remedy for those diseases. 3rd Ed. London: Underwood, 1823. 33.

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“Gout has in all times been observed to affect chiefly the rich and well-fed members of society...”449

“Several influential circumstances prevail in the mode of life of gouty persons; namely, high feeding, especially great consumption of animal food... During a long and extensive professional connection with a large rural district, we never knew an instance of gout among agricultural labourers, who of course form the great mass of the population; gout was not uncommon among tradesmen, but still more frequent in the class of gentlemen and opulent farmers.

“That the quantity of animal food consumed by agricultural labourers is comparatively very small, must be well known to persons who have lived in the country; and we believe that this circumstance has considerable share in procuring for that class their singular exemption from gout. It is nearly established that large consumption of animal food tends to produce the lithic acid diathesis; a condition so often associated with gout, that more than one author has been led to consider these forms of disease as essentially connected. In advancing the opinion that large consumption of animal food is a cause of gout, we are glad to avail ourselves of the support of one of the most distinguished physiologists of our day. Muller, in commenting on Magendie’s experiments on food, says, ‘These experiments have thrown some light on the causes and mode of treatment of gout and calculous disorders. The subjects of these diseases are generally persons who live well and eat largely of animal food...By diminishing the proportion of azotised substances in the food, the gout and gravelly deposits may be prevented.’ ”450, 451

In a 1907 textbook on gout, Luff states: “The subjects of gout are generally persons who live well and consume a large amount of animal food.”452

This literature provides evidence that, prior to the widespread practice of feeding grains to livestock, physicians had already established that consumption of animal flesh promotes and a plant-based diet prevents or cures gout.

Contemporary Diet-Gout Research

In 1998, Kullich et al. reported that 97% of 300 patients with hyperuricemia also had elevated serum cholesterol (>200 mg/dl), 87% had elevated LDL, and 69% had elevated VLDL. Kullich et al. treated all patients with “a special low-cholesterol, low-triglyceride and low-purine dietetic regimen” i.e. a

449 Budd W. Gout. In: Tweedie A, ed. The Library of Medicine: A System of Practical Medicine, comprised in a series of original dissertations. Vol. 5. London: Whittaker and Co.,1840. 206.

450 Ibid., 218.

451 Garrod AB. A Treatise on Gout and Rheumatic Gout (rheumatoid Arthritis). Longmans., 1876. 229.

452 Luff AP. Gout: Its Pathology, Forms, Diagnosis and Treatment. New York: Wm Wood and Co., 1907. 242.

VITAMIN C, URICASE, AND URIC ACID – 169

reduced intake of animal products. After four weeks of this program, all lipid levels and serum urate concentrations reduced significantly.453

In 2003 Lyu et al. reported that in a Taiwanese population, those in the highest tertile of plant protein consumption (a significant portion from soy products) had a 46% reduced risk of gout, while those in the highest tertile of animal fat consumption had a 34% increased risk of gout.454 Those in the highest tertile of fiber (i.e. whole plant food) consumption had a 62% reduced risk of gout. The authors concluded that “Fruit and vegetables, which are rich in dietary fiber, folate, and vitamin C, are protective against gout.”

A 2004 study of U.S. men found that those with the highest intake of animal flesh had a 41% greater risk of gout than those with the lowest intake; whereas men with the highest intake of plant proteins had a 27% decreased risk compare to those with the lowest intake.455

A 2005 study of U.S. men and women found that those with the highest intake of total animal flesh had a serum uric acid level 0.48 mg/dl greater than those with the lowest intake.456

A 2008 study of Taiwanese men and women found no association between serum urate levels and animal flesh consumption.457 The authors noted that the average total protein intake in Taiwan is only 85 to 90% of that in American and numerous European countries.458 Further, Taiwan has a total per capita meat consumption of about 79 kg, compared to 127 kg in the U.S.459 Per capita, Taiwanese and Americans obtain about 540 kcal and 900 kcal daily from non-fish livestock products, respectively.460 The authors of this study did not identify the low and high intakes defining the lower and upper quartiles of animal flesh consumption in this Taiwanese population, but the relatively low total intake of animal flesh in this population suggests a possible low variance in high vs. low consumers (see comments on Villegas et al. below), which would make it difficult to detect a relationship (if everyone is consuming a relatively similar amount of meat, there would likely be very little metabolic difference between high and low consumers).

453 Kullich W, Ulreich A, Klein G. [Changes in uric acid and blood lipids in patients with asymptomatic hyperuricemia treated with diet therapy in a rehabilitation procedure]. [Article in German]. Rehabilitation (Stuttg). 1989 Aug;28(3):134-7. Abstract.

454 Lyu LC, Hsu CY, Yeh CY, et al.. A case-control study of the association of diet and obesity with gout in Taiwan. Am J Clin Nutr 2003 Oct;78(4):690-701. Table 4.

455 Choi HK, Atkinson K, Karlson EW, et al.. Purine-Rich Foods, Dairy and Protein Intake, and the Risk of Gout in Men. N Engl J Med 2004 March 11;350:1093-1103.

456 Choi HK, Liu S, Curhan G. Intake of Purine-Rich Foods, Protein, and Dairy Products and Relationship to Serum Levels of Uric Acid. Arthritis and Rheumatism 205 Jan;52(1):283-89.

457 Yu KH, See LC, Huang YC, et al.. Dietary Factors Associated with Hyperuricemia in Adults. Sem Arth and Rheum 2008 Feb;37(4):243-50.

458 Ibid., 246.

459 FAO. The state of food and agriculture, 2009. 136.

460 Ibid., 141.

170 – HUMAN NUTRITIONAL ADAPTATIONS

As noted above, previous research in Taiwan did find a link between saturated fat consumption and gout, but also found whole plant foods protective. Therefore, it may be that in Taiwan the consumption of whole plant foods by consumers of animal flesh obscures the effect of consuming animal flesh. This last study did find that beer intake increased the risk of elevated serum urate, which raises the question whether beer intake covaries with animal flesh intake in this population as it probably does in the U.S..

A 2008 study of 5,003 subjects from 5 cities in China found a higher prevalence of hyperuricemia and gout among residents of the more economically developed urban areas “as manifested by the increase of daily consumption of meat and seafood.”461 These authors also found that overweight or obesity, hypertension, and abnormal triglycerides all “were highly associated with higher prevalence of hyperuricemia.” All of these phenomena have been associated with animal flesh consumption. For example, as noted above, among Caucasian Adventists, vegans had the lowest risk of hypertension, followed by lacto-ovo vegetarians, partial vegetarians, and omnivores.462

In a 2011 study of Chinese men, Villegas et al. found that protein from animal sources was significantly associated, while protein from plant sources was inversely related, with prevalence of hyperuricemia.463 In this study, fish intake drove the association between animal protein and high serum urate; other meat did not have an association. Similar to Taiwan, China has a relatively low total meat consumption of approximately 60 kg annually per capita464 and of this about one-quarter consists of fish.465 In 2010, the top Chinese rural and urban consumers of fish consumed 5 and 2 times more than the bottom consumers in each region, respectively.466 However, the Chinese consuming the most pig, cow, and mutton flesh only consumed about 50 percent more than the bottom consumers.467 While the top Chinese consumers of bird flesh consumed about 3 times as much as the bottom consumers,468 the 2006 total annual per capita urban consumption of bird flesh was about 25% lower than consumption of fish, at only 8 vs. 13 kg respectively.469 In comparison, in the U.S. in 2006, total per capita chicken consumption alone was

461 Miao Z, Li C, Chen Y, et al.. Dietary and lifestyle changes associated with high prevalence of hyperuricemia and gout in the Shandong coastal cities of Eastern China. J Rheumatol 2008 Sep;35(9):1859-64. Abstract.

462 Pettersen BJ, Anousheh R, Fan J, Jaceldo-Siegi K, Fraser GE. Vegetarian diets and blood pressure among white subjects: results from the Adventist Health Study-2. Public Health Nutr 2012 Oct; 15(10): 1909-1916.

463 Villegas R, Xiang YB, Elasy T, et al.. Purine-rich foods, protein intake, and the prevalence of hyperuricemia: The Shanghai Men’s Health Study. Nutr Metab Cardiovasc Dis 2012 May:22(5):409-16.

464 FAO, op. cit.

465 Zhou Z, Tian W, Wang J, et al.. Food Consumption Trends in China, April 2012. Report submitted to the Australian Government Department of Agriculture, Fisheries, and Forestry. http://www.daff.gov.au/__data/assets/pdf_file/ 0006/2259123/food-consumption-trends-in-china-v2.pdf

466 Ibid., 31.

467 Ibid., 15, 16, 38.

468 Ibid., 24, Figure 2.5, 2010 data.

469 Ibid., 15, Table 2.5 b.

VITAMIN C, URICASE, AND URIC ACID – 171

40 kg, and total bird consumption was 48 kg, 6 times that of urban Chinese.470 A relatively low variance between low and high consumers of mammals’ flesh and a relatively low consumption of bird flesh compared to fish flesh in this population probably will make it difficult to consistently detect a relationship between land animal flesh consumption and hyperuricemia.

A 2013 study of elderly women in suburban Guangzhou, Guangdong province, China, reported that animal flesh consumption was “strongly associated with a higher prevalence of hyperuricemia.471

At least two other 21st century studies have shown that consumption of animal flesh increases the risk of gout.472, 473 Of these, the one in which fruit intake and flesh consumption appears inversely related also found increasing consumption of fruit to protect against gout; men who averaged greater than two pieces of fruit daily had 50% less risk than those who ate less than one-half piece of fruit daily.474 These findings seem predictable from the nature of human metabolism of uric acid.

However, other studies have suggested that increasing fruit consumption, including fruit juices, increases the risk of gout. Most likely this paradox arises from processing of fruits and consuming them in conjunction with a diet rich in meats. Processing fruits to juices or otherwise reduces their vitamin C content, and consuming high amounts of fructose-rich but vitamin C-poor fruit juices (and refined sugars) along with high amounts of animal flesh rich in purines but lacking vitamin C would increase uric acid levels.

In 2013 Schmidt et al. reported that vegans in the EPIC-Oxford Cohort had the highest serum urate concentrations, followed by meat eaters, fish eaters, and lactovegetarians, with concentrations descending in that order.475 Since in this study, when you exclude the vegans, the pattern indicates that reductions in animal food intake result in reductions in urate levels, the higher levels in vegans appear paradoxical.

Schmidt et al. suggested that “the higher concentrations among vegans might be due to their lack of consumption of dairy products” which all other groups consumed. In this study and others, dairy or calcium intake has inversely correlated with serum urate levels, and vegans in this study had low

470 USDA and The National Chicken Council. Per Capita Consumption of Poultry and Livestock, 1965 to Estimated 2014. Retrieved October 12, 2013 from http://www.nationalchickencouncil.org/about-the-industry/statistics/per-capita- consumption-of-poultry-and-livestock-1965-to-estimated-2012-in-pounds/

471 Xiong Z, Zhu C, Qian X, et al.. Serum uric acid is associated with dietary and lifestyle factors in elderly women in suburban Guangzhou in Guangdong province of south China. J Nutri Health Aging 2013 Jan;17(1):30-4. Abstract.

472 Pokharel K, Yadav BK, Jha B, Parajuli K, Pokharel RK. Estimation of serum uric acid in cases of hyperuricaemia and gout. JNMA J Nepal Med Assoc. 2011 Jan-Mar; 51(181):15-20. Abstract.

473 Williams PT. Effects of diet, physical activity and performance, and body weight on incident gout in ostensibly healthy, vigorously active men. Am J Clin Nutr May 2008; 87(5): 1480-1487.

474 Ibid.

475 Schmidt JA, Crowe FL, Appleby PN, et al.. Serum Uric Acid Concentrations in Meat Eaters, Fish Eaters, Vegetarians, and Vegans: A Cross-Sectional Analysis in the EPIC-Oxford Cohort. PLoS One 2013;8(2):e56339.

172 – HUMAN NUTRITIONAL ADAPTATIONS

calcium intakes (570 mg/d). We have some evidence that dairy consumption and calcium levels may affect serum urate levels.476 However, calcium supplementation has not reduced serum urate in an intervention study done in New Zealand,477 but the baseline calcium intake of the average non-vegan New Zealander man is about 850 mg,478 more than 50% higher than among vegans in the EPIC-Oxford cohort. It remains possible that the low calcium intake in the vegans of the EPIC-Oxford cohort contributes to their elevated urate levels. Even though low intakes of total animal protein and adequate vitamin D status may reduce calcium requirements,479 I recommend that people eating plant-based diets aim for calcium intakes of at least 800 mg per day as a minimum, since this seems to represent the minimal short-term human requirement for calcium,480 and the calcium intakes of wild leaf-eating primates far exceed this on a mg/kg bodyweight basis.481

Schmidt et al. did not consider the possibility that low cobalamin (B12) status in the vegans may have contributed to their elevated urate levels. Some studies suggest a correlation between elevated homocysteine levels, which can arise from B12 deficiency, and elevated uric acid.482, 483, 484, 485 In the EPIC-Oxford cohort, only 19% of vegans regularly took a B12 supplement, and not surprisingly, 52% tested B12 deficient and another 21% showed B12 depletion; these people also had elevated homocysteine (Hcy) levels and “would be expected to have a higher risk of developing clinical symptoms related to vitamin B12 deficiency.”486

476 Dalbeth N, Horne A, Gambel GD, et al.. The effect of calcium supplementation on serum urate: analysis of a randomized controlled trial. Rheumatology 2009;48(2):195-97.

477 Ibid.

478 Australian Ministry of Health. Nutrient Reference Values for Australia and New Zealand: Calcium. Retrieved October 12, 2013 from http://www.nrv.gov.au/nutrients/calcium.htm.

479 Nordin BEC. Calcium requirement is a sliding scale. Am J Clin Nutr 2000;71(6):1381-83.

480 Hunt CD and Johnson LK. Calcium requirements: new estimations for men and women by cross-sectional statistical analyses of calcium balance data from metabolic studies. Am J Clin Nutr 2007 Oct;86(4):1054-63.

481 Milton K. Nutritional characteristics of wild primate foods. Nutrition 1999;15 (6):488-98.

482 Lassier-Cacan S, Xhignesse M, Piolot A, et al.. Plasma total homocysteine in health subjects: sex-specific relation with biological traits. Am J Clin Nutr 1996 Oct;64(4):587-93.

483 Uehara SK, Rosa G. Association of uricemia with biochemical and dietary factors in human adults with metabolic syndrome genotyped to C677T polymorphism in the methylenetetrahydrofolate reductase gene. Nutr Hosp 2011 Mar-Apr; 26(2):298-303.

484 Uehara SK, Rosa G. Association of homocysteinemia with high concentrations of serum insulin and uric acid in Brazilian subjects with metabolic syndrome genotypes for C677T polymorphism in the methylenetetrahydrofolate reductase gene. Nutr Res 2008 Nov;28(11):760-6. Abstract.

485 Malinow MR, Levenson J, Giral P, et al.. Role of blood pressure, uric acid, and hemorheological parameters on plasma homocyst(e)ine concentration. Atherosclerosis 1995 April;114(2):175-83. Abstract.

486 Gilsing AMY, Crowe FL, Lloyd-Wright Z, et al.. Serum concentrations of vitamin B12 in British male omnivores, vegetarians, and vegans: results from a cross-sectional analysis of the EPIC-Oxford cohort study. Eur J Clin Nutr 2010 Sep; 64(9):933-39.

VITAMIN C, URICASE, AND URIC ACID – 173

Cobalamin supports the cells’ use of folate to synthesize DNA from its precursors, thymidine and purines. A deficiency of B12 traps folate in a form that the cells can’t use. In this case, folate can not participate in DNA synthesis. Logically, then, in a folate-sufficient but cobalamin-deficient individual (this would characterize a majority of vegans) this could lead to an underutilization and accumulation of purines, which the body would then metabolize to uric acid. It seems possible that this or some not yet determined relationship between vitamin B12, serum Hcy and urate accounts for the elevated serum Hcy and urate in the vegans in this study.

In 1929, Riddle reported that patients with pernicious anemia (B12 deficiency) have abnormally high values for uric acid in the blood and urine during treatment.487 Riddle hypothesized that the destruction of large numbers of red blood cell nuclei which accompanies the rapid maturation of the cells, and an increase in general nuclear metabolism throughout the body, may contribute to the increased uric acid levels during recovery from megaloblastic anemia.

Fox et al. also reported that megaloblastic anemia caused by low vitamin B12 status induces alterations in purine metabolism in humans, and supplementation with the vitamin may increase uric acid levels.488

“Within 3 to 5 days of vitamin therapy, temporally related to the reticulocyte response of a peak value of 21 percent, the plasma uric acid increased in all patients except 1. The mean peak increase was 50 percent over pre-therapy values.”

The Mayo Clinic recommends cautious use of B12 supplementation in patients with a history of gout or elevated uric acid levels “as the correction of megaloblastic anemia with vitamin B12 may precipitate gout in susceptible individuals.”489 The textbook Medicine states:

“The megaloblastic anemia in pernicious anemia responds dramatically to intramuscular injections of cobalamin...A reticulocytosis begins after 72 hours, the serum uric acid rises, and hypokalemia may develop as the new blood cells incorporate potassium.”490

It seems clear that there exists an as yet incompletely clarified relationship between vitamin B12 status, Hcy and uric acid levels. Since excluding the almost universally B12-deficient vegans from the EPIC- Oxford cohort data suggests that removing animal flesh from the diet reduces serum urate levels, it seems very likely that the vegans did not exhibit the expected lowest levels of urate because of either B12 or calcium deficiency.

487 Riddle MC. The endogenous uric acid metabolism in pernicious anemia. J Clin Invest 1929;8(1):69-88.

488 Fox IH, Dotten DA, Marchant PJ. Alterations of human purine metabolism in megaloblastic anemia. In: M.M. Muller et al.. (eds.), Purine Metabolism in Man–II. Plenum Press, 1977. 249

489 Mayo Clinic. Vitamin B12. Retrieved October 12, 2013 from http://www.mayoclinic.com/health/vitamin-B12/NS_patient- vitaminb12/DSECTION=safety.

490 Fishman MC (ed.). Medicine. Lippincott Williams and Wilkins, 2004. 367.

174 – HUMAN NUTRITIONAL ADAPTATIONS

I urge all people who adopt a plant-based diet to regularly use B12 supplements and ensure their calcium intake with appropriate food choices (as discussed in Appendix B) to avoid this issue.

Summary

Humans lack the enzymes that produce vitamin C and uricase, whereas all carnivorous animals produce vitamin C and uricase. The lack of these enzymes makes humans poorly adapted to consumption of animal flesh. A rather large body of evidence indicates that humans who consume animal flesh have a propensity to elevated uric acid levels and an increased risk of gout. This data contradicts the hypothesis that adaptation to an animal-based diet drove human evolution, and supports the hypothesis that human evolution was powered by a plant-based diet.

VITAMIN C, URICASE, AND URIC ACID – 175

14: Complexion Preference

In many animal species, including humans, carotenoids derived from plants provide coloration of flesh and feathers, and also appear to play key roles in support of immunity and fertility.

“Carotenoid supplementation is associated with improved development of the immune system in human children (Alexander et al. 1985), whereas individuals infected with HIV and malaria have reduced carotenoid levels (Friis et al. 2001). Carotenoid levels may also affect spermatogenesis in boars (Chew 1993), and women who failed to conceive during in vitro fertilization had unusually fluctuating carotenoid levels in their follicular fluid (Schweigert et al. 2003). Brightly colored carotenoid-based ornaments are displayed by many bird and fish species, the size and brightness of which reflect aspects of health and condition. Male greenfinches with brighter yellow breast feathers showed stronger humoral immune responses to a novel antigen (Saks et al. 2003). Male and female yellow-eyed penguins with more saturated yellow eye ornamentation produced more offspring per season (Massaro et al. 2003). Researchers have demonstrated mate choice based on the brightness of carotenoid ornaments in greenfinches (Eley 1991), yellow- eyed penguins (Massaro et al. 2003), and goldfinches (MacDougall and Montgomerie 2003).”491

Experiments have shown that when people are given the choice between various skin colors, they rate as most healthy and attractive a complexion that has both 1) a redness reflecting good skin vascularization and blood oxygenation, and 2) a bright yellowness reflecting skin enrichment with carotenoids derived from fruits and vegetables.492, 493

Complexion, Vascularization, Oxygenation, and Diet in Humans

Factors that increase skin redness in humans include increased skin vascularization and increased blood oxygenation.494 Factors associated with increase skin vascularization in humans include physical fitness and, in women, increased estrogen levels; conditions known to decrease skin vascularization include hypertension and diabetes type 2.495 Increased aerobic fitness increases blood oxygenation; cardiac or

491 Stephen ID, Law Smith MJ, Stirrat MR, Perrett DI. Facial Skin Coloration Affects Perceived Health of Human Faces. International Journal of Primatology 2009; 30 (6): 845-857.

492 Ibid.

493 University of Nottingham (2011, January 12). Eating vegetables gives skin a more healthy glow than the sun, study shows. ScienceDaily. Retrieved September 19, 2013, from http://www.sciencedaily.com/releases/ 2011/01/110111133224.htmform_372.replyids=2andform_363.replyids=2andform_346.userid=215andform_346.replyids=92 61

494 Stephen et al., op. cit..

495 Ibid.

177

respiratory illness decreases blood oxygenation to such an extent that the complexion appears dull and blue.496

In nonhuman primates, increased skin redness signals reproductive fitness:

“Increased facial skin redness, due to increased skin blood perfusion, has been linked to increased testosterone in male rhesus macaques (Rhodes et al. 1997), and increased estrogen levels and fertility have been linked with increased redness of anogenital skin in female rhesus macaques (Czaja et al. 1977; Dixson 1983). Both of the reddened areas attract preferential visual attention from the opposite sex (Waitt et al. 2003, 2006). Facial redness is also associated with higher testosterone levels and dominance rank in male mandrills (Setchell and Dixson 2001) and reproductive status in female mandrills (Setchell et al. 2006); female mandrills prefer to mate with brightly colored males (Setchell 2005). Facial redness in male mandrills may therefore be an honest signal, demonstrating the bearer’s ability to bear the burden of the immune suppression caused by increased testosterone levels (Folstad and Karter 1992; cf. Setchell et al. 2009).”497

Thus, on a Darwinian basis it seems likely that facial redness in humans also signals reproductive fitness, and that people find individuals who have a well-vascularized complexion perfused by oxygen- rich blood more attractive because this type of complexion signals a healthy physiology and sexual ability.

In humans, the conditions associated with decreased vascularization and oxygenation, and dull, unattractive complexion–hypertension, type 2 diabetes, cardiac and respiratory diseases–are linked to consumption of animal milk and flesh containing saturated fat and cholesterol.

Among Caucasian Adventists, vegans had the lowest risk of hypertension, followed by lacto-ovo vegetarians, partial vegetarians, and omnivores.498 In the Adventist Health Study, regardless of BMI, and after adjustment for lifestyle factors, vegans had the lowest risk of type 2 diabetes, followed by lacto-ovo vegetarians, pesco-vegetarians, semi-vegetarians, and non-vegetarians in that order (i.e. nonvegetarians had the highest risk).499 Again among Adventists, men who never consumed meat had the lowest risk of ischemic heart disease.500 People with lower intakes of vitamin C, carotenoids, vitamin E, magnesium, and omega-3 fatty acids provided by fruits, leafy vegetables, nuts, and seeds have increased

496 Ibid.

497 Ibid.

498 Pettersen BJ, Anousheh R, Fan J, Jaceldo-Siegi K, Fraser GE. Vegetarian diets and blood pressure among white subjects: results from the Adventist Health Study-2. Public Health Nutr 2012 Oct; 15(10): 1909-1916.

499 Tonstad S, Butler T, Yan R, Fraser GE. Type of Vegetarian Diet, Body Weight, and Prevalence of Type 2 Diabetes. Diabetes Care 2009 May; 32(5):791-96.

500 Fraser GE. Associations between diet and cancer, ischemic heart disease, and all-cause mortality in non-Hispanic white California Seventh-day Adventists. Am J Clin Nutr September 1999; 70(3): 532s-538s.

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risks for obstructive lung diseases.501 In three European countries, middle aged men with greater intake of fruits and vegetables had better pulmonary function.502 In Japan, among young adult women, increasing meat intake was associated with increased risk of allergic rhinitis.503

In humans, consumption of saturated fats from animals increases blood viscosity and propensity to clot, which decreases blood perfusion and thus oxygenation of tissues.504 Both dietary saturated fats and dietary cholesterol raise LDL cholesterol which promotes atherosclerosis,505 which by narrowing vessels also decreases blood flow and oxygenation of tissues, creating chronic low-grade ischemia. These factors contribute to a dull, bluish, or pasty-white complexion – which I will call the cholesterol complexion–associated with cardiac and respiratory diseases. (Look for it among adherents of milk- and flesh-based diets.)

In contrast, animal-free, low-fat, plant-based diets reduce blood cholesterol, triglycerides, and viscosity and prevent and reverse atherosclerosis,506, 507 thus increasing blood oxygenation and perfusion and improving complexion.

This implies that most people would describe well-nourished people who eat a plant-based diet with little or no animal protein, saturated fat, and cholesterol as having a more attractive complexion than those who eat large amounts of flesh, fat, eggs, and milk with little fruits and vegetables.

Summary

In summary, humans have a natural attraction to and preference for the facial complexion associated with cardiovascular health and consuming a carotenoid-rich, low fat, plant-based diet containing little or no animal flesh. Since other primates subsisting on plant-based diets show similar preferences, we can conclude that natural selection also favored the reproduction of humans who had and preferred the carotenoid complexion in comparison to the cholesterol complexion. The supports the hypothesis that human evolution was powered by a plant-based diet, not an animal-based diet.

501 Romieu I, Trenga C. Diet and obstructive lung diseases. Epidemiol Rev (2001) 23 (2): 268-287.

502 Tabak C, Smit H, Rasanen L, et al.. Dietary factors and pulmonary function: a cross sectional study in middle aged men from three European countries. Thorax 1998 November; 54(11):1021-1026.

503 Miyake Y, Tanaka K, Okubo H, Sasaki S, Arakawa M. Dietary meat and fat intake and prevalence of rhinoconjunctivitis in pregnant Japanese women. Nutr J 2012; 11: 19.

504 Miller GJ. Effects of diet composition on coagulation pathways. Am J Clin Nutr 1998;67(suppl):542S–5S.

505 National Heart, Lung, and Blood Institute, National Cholesterol Education Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (ATP III) Final Report.

506 Esselstyn CB Jr. et al.. A Strategy to Arrest and Reverse Coronary Artery Disease: A 5 -Year Longitudinal Study of a Single Physician's Practice. The Journal of Family Practice 1995 December; 41(6): 560-68.

507 Esselstyn CB Jr. Updating a 12 -Year Experience With Arrest and Reversal Therapy for Coronary Heart Disease. Am J of Cardiology 1999 August 1; 84:339-341.

COMPLEXION PREFERENCE – 179

15: Vitamins A & B-12

To reiterate the general principle, if an organism subsists on a diet with a low availability of a certain essential nutrient, it needs mechanisms for increasing absorption and retention of that nutrient, to prevent deficiency. On the other hand, if an organism subsists on a diet with a very high availability of a certain essential nutrient, posing a danger of toxicity, then it needs mechanisms for reducing absorption, detoxifying, and eliminating that nutrient.

Thus, if an organism has mechanisms for increasing absorption and retention of a nutrient, or limited mechanisms for detoxifying or eliminating excesses of a potentially toxic nutrient, we can deduce that it evolved in an environment that had limited supplies of that nutrient. On the other hand, if an organism has mechanisms for limiting the absorption of a nutrient, or for detoxifying or eliminating a potentially toxic nutrient, we can deduce that it evolved in an environment that had excessive supplies of that nutrient.

Comparing Human Carotenoid Metabolism To Flesh-Eating Animals

Humans can convert ß-carotene from plants into retinol/vitamin A, and, provided adequate vegetables and fruits, can derive all their vitamin A requirements from plants.508 Dogs apparently can convert carotene to retinol in sufficient amounts to reverse vitamin A deficiency,509 but cats do not do the conversion at all and require preformed dietary retinol.510

A study of thirteen species found that serum and brain tissue concentrations of carotenoids positively correlated with maximum life span potential, and humans had the highest carotenoid levels as well as the longest potential lifespan.511 Due to a mutation, humans have lower activity of the enzyme that converts ß-carotene into retinol when compared to shorter-lived species.512 Retinol did not correlate with maximum life-span, suggesting that it plays little or no role in prevention of age-related diseases.513

Thus it seems that humans may have a specific genetic mutation that maximizes the use of carotenes from plants to provide protection against age-related diseases, particularly cancer, thus supporting

508 Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (2001). National Academies Press, 2001. 119-120.

509 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 197.

510 Ibid, 199.

511 Cutler RG. Carotenoids and retinol: their possible importance in determining longevity of primate species. PNAS, December 1, 1984; 81(23): 7627-7631.

512 Ibid.

513 Ibid.

181

humans’ extraordinary longevity among primates.514 Apparently natural selection favored the reproduction of human ancestors who habitually consumed a diet composed largely or primarily of fruits and vegetables, the primary dietary sources of carotenes.

Some people have suggested that humans require animal-source retinol, claiming that some research shows that some humans have such a low rate of conversion of ß-carotene to retinol that they can’t meet their retinol needs without consuming it directly. However, in the two studies frequently cited, no subjects had a deficient vitamin A status and all subjects consumed cod liver oil providing 1250 IU of retinol every other day throughout the study.515, 516 This confounds the results because the body tightly regulates conversion of ß-carotene to retinol, and limits the conversion when the body has stored retinol, to prevent retinol overdose. In other words, it appears that the authors either lacked this knowledge or deliberately designed the study to produce the false impression that some people do not have sufficient ability to convert ß-carotene to retinol.

The Institute of Medicine Food and Nutrition Board has stated that humans can meet their retinol requirements from plants alone provided that they consume adequate quantities of carotenoid-rich fruits and vegetables supplying at least 15,000 mcg of ß-carotene daily.517 Considering that just one sweet potato (about 100 kcalories) supplies almost 11,000 mcg and one large carrot (30 kcalories) supplies 7200 mcg of ß-carotene, a person eating a fruit- and vegetable- rich plant-based diet supplying 2000 kcalories can easily consume 30,000 to 60,000 mcg of ß-carotene daily. In 2010, a panel of experts in ß- carotene metabolism also affirmed that humans can meet their daily requirement for retinol exclusively from ß-carotene rich plant foods if they consume adequate amounts of fruits and vegetables.518

Of interest, de Pee et al. found that orange-colored fruits rich in carotenoids (papaya, mango, and pumpkins) increase serum concentrations of retinol and ß-carotene in humans more effectively than dark-green, leafy vegetables or carrots.519 In this study, people converted fruit ß-carotene to vitamin A more than twice as effectively as vegetable ß-carotene. This suggests that human ancestors may have depended more upon botanical fruits (including squashes and pumpkins) than vegetables for carotenoid intake, since if human ancestors had relied upon green vegetables for vitamin A, natural selection would have favored the reproduction of individuals who could more efficiently meet vitamin A need by eating

514 Ibid.

515 Hickenbottom SJ, Follett JR, Lin Y, et al.. Variability in conversion of β-carotene to vitamin A in men as measured by using a double-tracer study design. Am J Clin Nutr 2002 May;75(5):900-907.

516 Lin Y, Dueker SR, Burri BJ, et al.. Variability of the conversion of ß-carotene to vitamin A in women measured by using a double-tracer study design. Am J Clin Nutr 2000 June;71(6):1545-1554.

517 Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (2001). National Academies Press. 119-120.

518 Grune E, Lietz G, Palou A, Ross AC, Stahl W, Tang G, Thumham D, Yin S, Biesalski HK. ß-Carotene is an Important Vitamin A Source for Humans. J Nutr 2010 December; 140(12):2268S-22-85S.

519 de Pee S, West CE, Permaesih D, et al.. Orange fruit is more effective than are dark-green, leafy vegetables in increasing serum concentrations of retinol and ß-carotene in schoolchildren in Indonesia. Am J Clin Nutr 1998 Nov;68(5):1058-1067.

182 – HUMAN NUTRITIONAL ADAPTATIONS

vegetables than fruits. As previously noted, many of the 101 edible USOs found in African grasslands belong to the Curcurbitaceae family which also produces carotenoid-rich starchy squashes and pumpkins.520

Although the amounts of fruits and vegetables required to meet vitamin A requirements are unusually large in comparison to conventional Western diets, they are small in comparison to the quantities of fruits and vegetables consumed by non-human primates of comparable body size (i.e. chimpanzees and gorillas) or some contemporary human tribes. The people of Papua New Guinea obtain more than 90 percent of their dietary energy from sweet potatoes. A young, active woman in this tribe consuming 1520 kcalories from sweet potatoes daily (only about 60 percent of her daily energy requirements) would obtain about 15,740 mcg retinol activity equivalents (RAE), approximately 22 times her daily requirement (700 mcg RAE/day). This provides more than enough ß-carotene to satisfy both the requirement for retinol and the maintenance of high serum levels of carotenoids associated with prevention of age-related diseases.

Perhaps not incidentally, the people of Papua New Guinea eating their traditional sweet potato diet had a very low incidence of age-related diseases.521

Comparing Human Retinol Metabolism To Flesh-Eating Animals

Carnivorous and omnivorous animals regularly consume the liver of their prey. Animal liver provides large amounts of retinol. For example, a 100 gram portion of pork liver provides 24,500 IU of retinol, more than double the level the Food and Nutrition Board of the Institute of Medicine identified as the Tolerable Upper Level for retinol intake.522

In humans, an acute overdose of retinol can cause blurred vision, nausea, vomiting, vertigo, increased pressure inside the skull, and headaches; and a chronic overdose of retinol can cause birth defects, liver abnormalities, and possibly bone loss.523

Children have developed symptoms of retinol toxicity from eating chicken liver and various supplements providing about 4800 IU vitamin A daily.524 An increased incidence of birth defects has

520 Ibid., 569.

521 Sinnett P, Whyte M. Papua New Guinea. In: Western Diseases: Their emergence and prevention. Ed. by H. Hubert Carey Trowell and Dennis Parsons Burkitt. Harvard University Press, 1981. 174.

522 Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (2001). National Academies Press, 2001. 143.

523 Whitney EN, Rolfes SR. Understanding Nutrition, 10th edition. Thomson Wadsworth, 2005. 372-73.

524 Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (2001). National Academies Press, 2001. 132.

VITAMINS A & B-12 – 183

been found in women consuming 15,000 IU of retinol daily.525 Some people have developed liver tissue abnormalities (fibrosis) consuming as little as 5050 IU of retinol daily over a ten year period.526 (Eating 100 g of beef liver once weekly equates to 4492 IU daily.) The US National Library of Medicine contains numerous case reports of individuals developing liver cirrhosis or fibrosis from chronic ingestion of retinol.527

Based on a body of this type of evidence showing severe, irreversible adverse effects of excess retinol ingestion, the Institute of Medicine’s Food and Nutrition Board has recommended that adults not consume more than 10,000 IU (3000 mcg) of retinol daily.528 That works out to a tolerable dose of about 40 to 60 mcg retinol per kilogram of bodyweight. Given that some individuals have developed fibrosis by consuming as little as 5050 IU daily (above), the tolerable chronic dose may actually lie somewhere below 20 to 30 mcg per kg of bodyweight.

In contrast, animals adapted to eating flesh have much greater tolerance for retinol. Puppies and pregnant bitches can consume 15,000 mcg retinol per kilogram of bodyweight, and adult dogs can tolerate 64,000 mcg retinol per kilogram of bodyweight, without adverse effects.529 The omnivorous/ mesocarnivorous canines thus can ingest more than 300 times more retinol than humans without adverse effects.

Analysis of the femur of a young female H. erectus dated to 1.7 mya suggests that she died from an overdose of retinol.530 This shows that regular consumption of animal liver and retinol would have exerted a natural selection in favor of any individuals having higher tolerance of retinol.

The fact that modern humans have such a low tolerance for retinol compared even to the relatively omnivorous dog supports the conclusion that natural selection did not favor the reproduction of humans having the equipment required for successful adaptation to a flesh-based, mesocarnivorous diet as consumed by wild canines and recommended to people by “paleo diet” advocates.

Moreover, as discussed in Chapter 3, animals biologically adapted to eating flesh, such as dogs and cats, thoroughly enjoy eating liver without cooking or condiment. In contrast, many people find just the thought of eating liver repulsive. Among U.S. readers of AOL Food, a poll found that liver is the most

525 Ibid. 138.

526 Ibid. 134.

527 PubMed.gov. http://www.ncbi.nlm.nih.gov/pubmed?linkname=pubmed_pubmedandfrom_uid=17151585 Gathered June 6, 2013.

528 Ibid. 143.

529 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 199.

530 Smithsonian National Museum of Natural History. KNM-ER 1808. What does it mean to be human? Retrieved October 18, 2013 from http://humanorigins.si.edu/evidence/human-fossils/fossils/knm-er-1808 .

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hated food.531 A survey in Britain also found liver among the ten most hated foods, along with snails, tripe (intestines), oysters, squid, anchovies, cockles, kidneys, black (blood) pudding, and olives.532

If humans had a dietary requirement for retinol, which only liver and eyeballs supply in significant amounts, this would have arisen from human ancestors having a dietary dependence on consumption of raw liver or eyeballs for vitamin A, and this would have favored the reproduction of humans who relished raw liver and eyeballs without cultural influence, resulting in a modern human population wherein, regardless of cultural education, most or all people would enjoy eating raw liver or eyeballs. The fact that liver can rank on two different polls as one of the most hated foods among modern humans provides evidence that natural selection did not favor human dependence on liver or retinol as a source of vitamin A.

The fact that almost no one recommends or even considers eating eyeballs (raw or cooked) to get vitamin A also provides strong evidence that human ancestors did not rely on consumption of eyeballs to satisfy their vitamin A requirements.

Human Vitamin B12 Metabolism Compared to Flesh-Eating Animals

Many authors suggest that animal foods serve as the only and original dietary source of vitamin B12, and that our dietary requirement for it indicates that humans must eat animal flesh (i.e. are obligate carnivores). In fact, only microbes produce vitamin B12.

“Cobalamin, the preferred name for the family of derivatives familiarly known as vitamin B12, is unique among the vitamins in that it is synthesized only by certain microorganisms. Whenever cobalamins occur in nature, they are the result of synthesis by bacteria or other microorganisms in the rumen, intestine, soil, or sewage. All animals, including dogs and cats, ultimately depend on microbially synthesized cobalamin.”533

Dogs, cats, and humans all produce intrinsic factor (IF) to facilitate the absorption of cobalamin. In humans, only the stomach mucosa produces IF, while in dogs and cats, the stomach lacks or has weak production of IF.534 In dogs, the pancreas produces the bulk of IF, while in cats, only the pancreas produces IF.535

531 http://about-food.livejournal.com/76665.html

532 London B. Fussy food nation: Tripe, black pudding, cockles and olives top poll of Britain’s most hated foods. Mail Online, 17 August 2012.

533 National Research Council (U.S.) Ad Hoc Committee on Dog and Cat Nutrition. Nutrient requirements of dogs and cats. National Academies Press, 2006. 225.

534 Ibid., 226.

535 Ibid.

VITAMINS A & B-12 – 185

Animal flesh, particularly liver, contains considerably more vitamin B12 than typically consumed parts of plants. An animal biologically adapted to eating flesh would have a frequent supply of cobalamin, but one biologically adapted to eating plants would have infrequent intake of small amounts of B12. Thus, we would expect that an animal biologically adapted to eating plants would have a highly conservative metabolism of B12.

Humans have enterohepatic circulation of vitamin B12.536 As noted by Herbert, this can allow an initially B12 replete adult go 20 to 30 years without vitamin B12 intake 537:

“The enterohepatic circulation of vitamin B-12 is very important in vitamin B-12 economy and homeostasis (27). Nonvegetarians normally eat 2-6 mcg of vitamin B-12/d and excrete from their liver into the intestine via their bile 5-10 mcg of vitamin B-12/d. If they have no gastric, pancreatic, or small bowel dysfunction interfering with reabsorption, their bodies reabsorb ~3-5 mcg of bile vitamin B-12/d. Because of this, an efficient enterohepatic circulation keeps the adult vegan, who eats very little vitamin B-12, from developing vitamin B-12 deficiency disease for 20-30 y (27) because even as body stores fall and daily bile vitamin B-12 output falls with body stores to as low as 1 mcg, the percentage of bile vitamin B-12 reabsorbed rises to close to 100%, so that the whole microgram is reabsorbed.”70

Thus, humans have a very conservative B12 metabolism. This suggests that the ancestral diet of humans consisted primarily of plants and supplied only small and probably intermittent doses of B12, because this diet would have favored the survival of individuals who had the genetic equipment necessary for efficient B12 recycling and conservation.

Humans Absorption of Animal-Based B12 Appears Limited

People attempting to scientifically justify their consumption of flesh as “natural” often suggest that humans need to eat meat to get vitamin B12, since it seems to occur in greater quantity in animal flesh than in plant foods.

However, some evidence suggests that humans do not reliably absorb animal-based B12. According to data from the Framingham Offspring Study, 39 percent of people aged 26 to 83 years, primarily flesh- eaters, have “low normal” B12 levels.538 (Vegans form less than one percent of the general population.539)

536 Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline. National Academies Press, 1998. 309.

537 Herbert V. Staging vitamin B-12 (cobalamin) status in vegetarians. Am J Clin Nutr 1994 May;59(5 Suppl): 1213S-1222S.

538 McBride J. B12 Deficiency May Be More Widespread Than Thought. USDA Agricultural Research Service News and Events, August 2, 2000.

539 Vegetarian Times. Vegetarianism in America. http://www.vegetariantimes.com/article/vegetarianism-in-america/

186 – HUMAN NUTRITIONAL ADAPTATIONS

In this study, people who consumed B12-containing supplements, B12-fortified cereals, or dairy products – which are commonly consumed with fortified cereals – had a low risk of B12 deficiency. People who ate the most flesh did not have a low risk. In fact, the research found no relationship between flesh intake and plasma B12 levels.

"Oddly, the researchers found no association between plasma B12 levels and meat, poultry, and fish intake, even though these foods supply the bulk of B12 in the diet. ‘It’s not because people aren’t eating enough meat,’ Tucker said. ‘The vitamin isn’t getting absorbed.’"540

Since the B12 in animal flesh occurs in a protein-bound form, perhaps humans do not produce enough of stomach acid or some other factor, perhaps as yet undiscovered, to release the vitamin from its protein binder. Hence, this research suggests that people who eat flesh in amounts presumed to supply adequate B12 may not reliably avoid B12 deficiency unless they regularly consume B12 supplements.

Since this situation could not occur in an animal biologically adapted through evolution to obtaining vitamin B12 from flesh, this research supports the hypothesis that natural selection formed human metabolism to rely on the original, non-flesh source of B12: microbes.

Non-animal B12 Sources

As already noted, only microbes produce vitamin B-12.541 Many microbes have the ability to produce B-12, among them the following genera: Aerobacter, Agrobacterium, Alcaligenes, Azotobacter, Bacillus, Clostridium, Corynebacterium, Flavobacterium, Micromonospora, Mycobacterium, Norcardia, Propionibacterium, Protaminobacter, Proteus, Pseudomonas, Rhizobium, Salmonella, Serratia, Streptomyces, Streptococcus and Xanthomonas.

Bacillus megaterium is a common soil bacteria, not pathogenic to humans, and a producer of vitamin B12.542 Lactobacillus reuturi, a member of the gastrointestinal ecosystems of humans, poultry, swine, and other animals, and present in sourdough culture, produces vitamin B-12.543 Lactobacilli feed on various carbohydrates, such as inulin and fructo-oligosaccharides, present in fruits and vegetables, including bananas, onions, chicory root, garlic, jicama, Jerusalem artichoke, and leeks.

Albert et al. reported that bacteria inhabiting the upper small intestine of people eating plant-based diets produced B12 and made it available for absorption:

540 McBride J. op. cit...

541 Martens JH, Barg H, Warren MJ, Jahn D. Microbial production of vitamin B12. Appl Microbiol Biotechnol (2002) 58:275– 285.

542 Raux E, Lanois A, Warren MJ, Rambach A, Thermes C. Cobalamin (vitamin B12) biosynthesis: Identification and characterization of a Bacillus megaterium cobl operon. Biochem J (1998); 335: 159-166.

543 Taranto MP, Vera JL, Hugenholtz J, et al.. Lactobacillus reuteri CRL1098 Produces Cobalamin. J Bacteriol 2003 September; 185(18):5643-5647.

VITAMINS A & B-12 – 187

“In man, physiological amounts of vitamin B12 (cyanocobalamin) are absorbed by the intrinsic factor mediated mechanism exclusively in the ileum. Human faeces contain appreciable quantities of vitamin B12 or vitamin B12-like material presumably produced by bacteria in the colon, but this is unavailable to the non-coprophagic individual. However, the human small intestine also often harbours a considerable microflora and this is even more extensive in apparently healthy southern Indian subjects. We now show that at least two groups of organisms in the small bowel, Pseudomonas and Klebsiella sp., may synthesize significant amounts of the vitamin.”544

In 1995 Suzuki reported that the marine algae, nori, prevented all signs of B12 deficiency symptoms in 6 vegan children he studied:

“A nutritional analysis was conducted on the dietary intake of a group of 6 vegan children aged 7 to 14 who had been living on a vegan diet including brown rice for from 4 to 10 years, and on that of an age-matched control group. In addition, their serum vitamin B12 levels and other data (red blood cell count, hematocrit, hemoglobin, etc.) were determined in the laboratory. In vegans' diets, 2-4 g of nori (dried laver), which contained B12, were consumed daily. Not a single case of symptoms due to B12 deficiency was found. There were no statistically significant differences between the two groups with respect to any of the examination data, including B12 levels (p < 0.05). Therefore, consumption of nori may keep vegans from suffering B12 deficiency.”545

In 2005 Croft et al. reported that algae acquire vitamin B12 through a symbiotic relationship with bacteria.546

In 2009 Koyyalamudi et al. reported that the common white button mushroom provides vitamin B12 of value equivalent to that found in beef, beef liver, salmon, egg, and milk (not analogues). It appeared that the mushrooms absorbed the B12 from bacteria inhabiting their growth medium:

“High concentrations of vitamin B12 were also detected in the flush mushrooms including cups and flats. HPLC and mass spectrometry showed vitamin B12 retention time and mass spectra identical to those of the standard vitamin B12 and those of food products including beef, beef liver, salmon, egg, and milk but not of the pseudovitamin B12, an inactive corrinoid in humans. The results suggest that the consumer may benefit from the consumption of mushroom to increase intake of this vitamin in the diet.”547

544 Albert MJ, Mathan VI, Baker SJ. Vitamin B12 synthesis by human small intestinal bacteria. Nature. 1980 Feb 21;283(5749):781-2.

545 Suzuki H. Serum vitamin B12 levels in young vegans who eat brown rice. J Nutr Sci Vitaminol (Tokyo). 1995 Dec;41(6): 587-94. Abstract.

546 Croft MT, Lawrence AD, Raux-Deery E, et al.. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature (3 November 2005); 438: 90-93. Abstract. doi:10.1038/nature04056.

547 Koyyalmudi SR, Jeong S, Cho KY, Pang G. Vitamin B12 is the Active Corrinoid Produced in Cultivated White Button Mushrooms (Agaricus bisporus). J Agric Food Chem 2009; 57(14): 6327-6333. Abstract.

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As noted above, some common soil bacteria (Bacillus megaterium) produce vitamin B12. This raises the possibility that some human ancestors may have obtained some of their vitamin B12 from wild mushrooms that had absorbed the vitamin from their growth medium, the soil.

In 1994, Mozafar reported that spinach leaves and barley seeds grown on soil fertilized with organic matter or isolated B12 take up vitamin B12 into their tissues from the soil. The spinach leaves and barley kernels were thoroughly washed with distilled water before being tested for B12 content, so this was not a case of finding B12 on soiled plants. Testing confirmed that these plants contained active B12, not inactive analogues.548

In summary, we have evidence that non-pathogenic soil microbes, human small intestinal bacteria, lactobacilli from fermented foods, some sea algae, common mushrooms, and plants grown on soil fertilized with animal manure can all can provide biologically active B12. Any of these could have served as ongoing sources of B12 for prehistoric human ancestors.

I think we can safely assume that our prehistoric ancestors had more contact with soil than we do, sitting on it, sleeping on it, digging in it, and drawing water from springs in contact with the soil. Humans like other primates are apt to touch their own lips from time to time, providing a vector by which soil microbes or B12 could enter the human gut.

Humans living in modern industrialized nations typically ingest multiple courses of oral antibiotics over a lifetime, reducing or eliminating the population of B12-producing bacteria residing in the small intestine. All prehistoric humans would have received extensive breast feeding and probably kissed often, which transmits flora from one generation to another, and this transmission would not have been interrupted by antibiotic treatments.

Fermentation of plant foods, particularly fruits, occurs spontaneously in nature, providing another route by which our ancestors may have ingested B12-producing lactobacilli. Our ancestors almost certainly consumed any edible wild mushrooms and all of the plants they ate grew in soils teaming with bacteria, providing another B12 source.

All of this information suggests that modern hygiene, indoor lifestyles, antibiotics, and use of isolated chemical rather than biomass fertilizers in farming have reduced the amount of B12 available to humans in modern urban environments from non-animal sources. Thus, the fact that animal products appear to be the only reliable source of B12 among modern foods does not support the idea that animal foods have always been the only reliable sources of B12, nor does it support the idea that humans are biologically adapted to consumption of animal tissues to acquire B12.

548 Mozofar A. Enrichment of some B-vitamins in plants with application of organic fertilizers. Plant and Soil 1994; 167: 305-311.

VITAMINS A & B-12 – 189

Is a B12 Supplement ‘Artificial’?

Artificial synthesis of B12 requires about 70 synthesis steps, making it impractical as a method for commercial production of B12. “Therefore, today vitamin B12 is exclusively produced by biosynthetic fermentation processes, using selected and genetically optimized micro-organisms.”549

In other words, we cultivate, feed and breed living microbes so that they will produce the nutrient we want, just as we cultivate plants for nutrients. If the former is ‘artificial,’ so is the latter.

The information I gave above indicates that modern antibiotics and hygiene have reduced or eliminated intestinal flora that would otherwise produce B12 for us, modern sanitation and agricultural practices have reduced the B12 content of drinking water and plant foods, and humans do not reliably extract B12 from animal products. Hence, probably all individuals in modern nations need to ingest vitamin B12 from cultivated microbes, either via supplements or fortified foods, to prevent B12 deficiency.

Summary

Human requirements for and metabolism of carotenoids, retinol, and cobalamin (vitamin B12) differ markedly from those of animals biologically adapted to eating flesh. Our high requirement for carotenoids for uses other than conversion to retinol combined with a tightly regulated system for conversion of carotenoids to retinol probably evolved in a population having a very high intake of carotenoids from plant foods. Our low tolerance for retinol ingestion provides evidence that our ancestors never had a sustained high intake of this potentially toxic nutrient found concentrated in animal tissues. The high prevalence among humans of a distaste for liver and eyeballs, the major potential dietary sources of retinol, also provides evidence that our ancestors never depended upon liver or eyeballs for vitamin A sufficiency.

Our highly conservative cobalamin metabolism suggests that our ancestors ate a diet that had a low or irregular availability of cobalamin, expected for a plant-based diet. Evidence that we poorly absorb meat-based B12 suggests that our ancestors did not depend on animal flesh for this nutrient. Evidence suggests that humans living on plant-based diets can obtain sufficient B12 from small intestinal flora, fungi, water, or plant foods grown on microbe-rich soils. However, in modern circumstances these do not serve as reliable sources of this vitamin, so, to avoid deficiency, civilized humans can obtain B12 from farmed microbes and take it in a pill.

The characteristics of human carotenoid, retinol, and cobalamin metabolism discussed in this chapter support the hypothesis that human evolution was powered by a plant-based diet, perhaps one including carotenoid-rich starchy fruits from the Curcurbitaceae family, not an animal-based diet.

549 Martens J-H, Barg H, Warren Mj, Jahn D. Microbial production of vitamin B12. Appl Microbiol Biotechnol (2002) 58: 275-285.

190 – HUMAN NUTRITIONAL ADAPTATIONS 16: Carbohydrate & Lipid Metabolism

As I discussed in detail in Chapter 2:

1. If a species inhabits an environment or has a dietary habit that provides a potentially harmful superabundance of a particular nutrient, natural selection will favor the reproduction of individuals who have mechanisms for quickly and safely disposing of any excess that they absorb. Hence, if a species has the aforesaid mechanisms for managing a particular nutrient, we can conclude that its natural or ancestral diet or environment contained a large excess of that nutrient. 2. If a species inhabits an environment or has a dietary habit that provides only a small amount of a particular essential or potentially beneficial nutrient, natural selection will favor the reproduction of individuals who have mechanisms for conserving and minimizing the utilization of that nutrient. Hence, if a species has the aforesaid mechanisms for managing a particular nutrient, we can conclude that its natural or ancestral diet or environment contained only small amounts of that nutrient relative to needs.

Carbohydrate and Fat Oxidation

Human metabolism handles dietary carbohydrates and fats in markedly different ways. Ad libitum consumption of food typically provides the body with more glucose or fat than the body can immediately use, so natural selection favored those individuals who have the ability to store these nutrients for later utilization. Humans store dietary glucose and fats as glycogen and adipose fat, respectively.

Because of the size and hydrophilic nature of glycogen, humans can store only a limited amount of dietary glucose as glycogen–about 400-500 grams, 120 g of this in the liver, most of the rest in the muscles. In humans, ingestion of dietary carbohydrate sufficient to store some as glycogen stimulates carbohydrate oxidation and through this mechanism the body very closely matches carbohydrate oxidation to intake and regulates carbohydrate stores.550

Acheson et al. showed that this mechanism can accommodate ingestion of up to 500 g of carbohydrate daily (the equivalent of 20 bananas or potatoes, or 11 cups of cooked brown rice) without triggering the conversion of carbohydrate into fat (de novo lipogenesis).551 They found that subjects could store 800-900 g of total dietary carbohydrate. Thus, under normal feeding conditions, instead of converting dietary glucose to fat, the system shunts glucose to glycogen stores, and this results in the nearly exclusive use of glucose as a fuel, some of this going simply to increased body heat (thermogenesis), in time reducing the temporary accumulation of glycogen. As explained by Flatt:

550 Flatt JP. Use and storage of carbohydrate and fat. Am J Clin Nutr 1995 April;61(4):952S-959S.

551 Acheson KJ, Schutz Y, Bessard T, et al.. Glycogen storage capacity and de novo lipogenesis during massive carbohydrate overfeeding in man. Am J Clin Nutr 1988;48:240-7.

191

“To induce substantial rates of carbohydrate conversion into fat, the body’s total glycogen stores must be considerably raised, from their usual 4-6 g/kg body wt to >8-10 g/kg body wt. This requires deliberate and sustained overconsumption of large amounts of carbohydrate for ≥2-3 d (13).”552

Flatt comments further:

“Two important conclusions can be deduced from these observations: 1) under usual conditions of unrestricted access to food, glycogen stores are spontaneously maintained far below their maximal capacity, and 2) the common belief that carbohydrates are readily turned into fat can be dismissed as well as the frequently made argument that the high metabolic cost of lipogenesis is a cause for greater energy dissipation on high-carbohydrate diets.”553

Since the human body has this system for regulating the stores of carbohydrate, directed at rapidly oxidizing whatever is ingested and stored after a meal, we can surmise that human metabolism probably evolved on a plant-based diet, since only a plant-based diet will frequently supply enough carbohydrate to require the system for rapid oxidation of excess glucoses as well as the glycogen storage capacity found in humans.

In contrast to carbohydrate storage, humans can store a virtually unlimited amount of dietary fat. A 70 kg male having a lean condition of 10% body fat carries 7000 g of fat, about 20 times the weight of his glycogen stores, and a 55 kg woman having a normal 20% body fat carries 11,000 g of fat, about 31 times the weight of her glycogen stores.

Due to the way the body handles absorption and transport of dietary fat, in Flatt’s words, “Dietary fatty acids are thus targeted for deposition in adipose tissue.”554 In contrast to carbohydrate, ingestion of fat stimulates fat storage not only without any increase in fat oxidation, but accompanied by a suppression of fat oxidation:

“That fat ingestion has so little effect on postprandial substrate oxidation is imputable to the relatively slow rate of fat absorption from the gut and to the fact that dietary fat is converted into chylomicrons targeted for deposition in adipocytes, allowing only a small fraction to reach other cells in the form of free fatty acids (10). Thus, although carbohydrate intake has a powerful effect in promoting carbohydrate oxidation, ingestion of fat promotes fat oxidation only marginally, so that even the consumption of high-fat meals leads to inhibition of fat oxidation during the following hours.”555[Italic added.]

552 Flatt, op. cit., 953S.

553 Ibid.

554 Ibid.

555 Ibid., 955S.

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Whereas carbohydrate ingestion stimulates an immediate increase in carbohydrate oxidation to regulate glycogen stores, fat oxidation only materially increases in response to either 1) a gap between total energy expenditure and the amount of energy ingested as carbohydrate and protein (i.e. energy deficit)556, or 2) a chronic expansion of fat stores, i.e. becoming over-fat.557

Since the body handles dietary fat very conservatively, shunting it directly to storage without immediately increasing fat oxidation, we can surmise that human metabolism evolved in an environment supplying limited amounts of dietary fat, because this environment would favor the survival of individuals who could rapidly store the limited amounts available. Thus, natural selection favored individuals who immediately packaged fat into chylomicrons for transportation directly to fat storage. Probably due to a paucity of dietary fat in the ancestral environment, the human species never had to deal with excesses of this nutrient that would have provided a selective advantage to individuals who could effectively limit fat storage.

This system whereby the body disposes of excess dietary carbohydrate by directing it in part to thermogenesis instead of immediately converting it to fat could only enhance survival in a circumstance wherein humans had access to plentiful carbohydrate but little dietary fat. If in the ancestral diet carbohydrate had been scarce but fat abundant, as proposed by “paleo diet” and low carbohydrate diet advocates, this would have favored survival of systems that were profligate expenders of fat and conservative expenders of glucose. We have characteristics of fat and carbohydrate metabolism exactly the opposite of what one would expect for an animal naturally adapted to a low carbohydrate, high fat, animal-based diet.

Hence, human biochemistry provides evidence that human ancestors pursued a diet that provided a superabundance of carbohydrates – i.e. edible plant foods – and a relative paucity of fat. Further, research suggests that humans handle the unsaturated fats characteristic of plants differently from saturated fats characteristic of animal flesh.

Metabolism of Saturated and Unsaturated Fats

Contrary to popular belief and misinformation, the relative proportion of saturated and unsaturated fats in animal tissues is primarily determined by species genetics, not by diet. Wild and grass fed animals may in some cases have a lower total fat content than the same species fed grain concentrates, but they do not have a markedly different saturated fatty acid profile.

For example, according to Cordain et al., 44% and 45% of the tissue fats from pasture-fed and grain-fed Brangus cross steers, respectively, consist of saturates, virtually identical.558 Moreover, saturated fats

556 Ibid., 954S.

557 Ibid., 956S.

558 Cordain L, Watkins BA, Florant GL, et al.. Fatty acid analysis of wild ruminant tissues: evolutionary implications for reducing diet-related chronic disease. EJCN 2002 March;56(3):181-91.

CARBOHYDRATE & LIPID METABOLISM – 193

form a similar or even greater portion of the tissue fats in various wild animals (Table 16.1). Animals in general, and mammals in particular, have a greater proportion of their fats as saturates than plants. Prehistoric hominins subsisting on animal-based diets would have had a high proportion of their dietary fat composed of saturated fats.

Table 16.1: Comparison of muscle tissue lipid compositions (wt%) in wild ruminants, grass-fed cattle, grain-fed cattle, wild salmon, grain-fed chicken and pigs, and humans.

Species SFA MUFA PUFA

Giraffe 36 16 41

Eland 48 20 34

Hartebeest 48 18 32

Topi 56 15 38

Cape buffalo 39 28 32

White-tailed deer 49 35 16

Pronghorn antelope 43 30 27

Mule deer 45 35 27

Elk 41 33 26

Brangus cross, grass-fed 44 40 10

Brangus cross, grain-fed 45 45 7

Lamb 44 41 8

Salmon, coho, wild 22 37 35

Pigs 37 47 11

Cow milk fat 63 29 3

Chickens 28 44 19

Humans 43 47 10

Sources: Cordain et al., EJCN 2002 March;56(3):181-91; Human fat: Bettelheim et al.. Introduction to General, Organic, and Biochemistry, sixth edition (Brooks/Cole, 2001), 474; Lamb, salmon, pig, cow milk, chicken: USDA, www.cronometer.com

About 55% of the total saturated fat intake of Americans eating animal flesh, eggs, and milk consists of palmitic acid (PA), with beef, cheese, and serving as the primary sources.559 A 2005 study found that

559 Hu FB, Stampfer MJ, Manson JE, et al.. Dietary saturated fats and their food sources in relation to the risk of coronary heart disease in women. Am J Clin Nutr 1999;70:1001-8.

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humans consuming a diet providing 40% of energy as fat with 17% as PA and 16% as oleic acid (OA, the principle fat in olives and olives) showed depressed fat oxidation and resting energy expenditure compared to a diet containing the same amount of total fat, but only 2% of it as PA and 40% as OA.560 Similarly Piers et al. reported that when people were fed a breakfast providing 43% of energy from fat from olive oil they had a significantly higher post-meal thermogenic effect and rate of fat oxidation than when they obtained the same amount of fat from cream.561 Soares et al. found the same effect in abdominally obese postmenopausal women.562

Three other human studies found that a consumption of a diet with a high ratio of saturated to polyunsaturated fat suppressed fat oxidation in the thermogenic response to food consumption.563, 564 565

As noted by Kien et al., the suppression of fat metabolism by saturated fats may also promote insulin resistance, which reduces glucose oxidation.566 In a review, Funaki states that excess storage of fats in adipose tissue causes adipose tissue insulin resistance, “saturated fatty acids secreted into the bloodstream from white adipose tissue impair insulin signaling in non-adipose tissues,” and “Lipotoxicity by SFAs [saturated fatty acids] is one of the underlying pathophysiological mechanisms of obesity and type 2 diabetes.”567

However, diets high in unsaturated fats also appear to induce insulin resistance.568 Parish and Petersen reported that “Five hours of maintaining high levels of plasma fatty acid concentrations resulted in a 50% reduction in insulin-stimulated rates of muscle glycogen synthesis and whole-body glucose oxidation compared with the control study (in the absence of any exogenous fatty acids).”569 It appears likely that diets containing similar amounts of fats produce similar degrees of insulin resistance/

560 Kien CL, Bunn JY, Ugrasbul F. Increasing dietary palmitic acid decreases fat oxidation and daily energy expenditure. Am J Clin Nutr 2005 Aug;82(2):320-26.

561 Piers LS, Walker KZ, Stoney RM, et al.. The influence of the type of dietary fat on postprandial fat oxidation rates: monounsaturated (olive oil) vs. saturated fat (cream). Int J Obesity 2000;26:814-21.

562 Soares M, Cummings SJ, Mamo JCL, et al.. The acute effects of olive oil v. cream on postprandial thermogenesis and substrate oxidation in postmenopausal women. Brit J Nutr 2004;91:245-252.

563 Jones PJ, Schoeller DA. Polyunsaturated:saturated ratio of diet fat influences energy substrate utilization in the human. Metabolism 1988 Feb;37(2):145-51. Abstract.

564 Jones PJ, Ridgen JE, Phang PT, Birmingham CL. Influence of dietary fat polyunsaturated to saturated ratio on energy substrate utilization in obesity. Metabolism 1992 Apr;41(4):396-401. Abstract.

565 van Marken Lichtenvelt WD, Mensink RP, Westerterp KR. The effect of fat composition of the diet on energy metabolism. Z Emahrungswiss 1997 Dec;36(4):303-5. Abstract.

566 Kien et al.. Increasing dietary palmitic acid decreases fat oxidation and daily energy expenditure. Am J Clin Nutr 2005 Aug;82(2):320-26.

567 Funaki M. Saturated fatty acids and insulin resistance. The J Med Invest 2009;56:88-92.

568 Galbo T, Perry RJ, Jurczak MJ, et al.. Saturated and unsaturated fat induce hepatic insulin resistance independently of TLR-4 signaling and ceramide synthesis in vivo. PNAS USA 2013 Jul 30;110(31):12780-5.

569 Parish R, Petersen K. Mitochondrial dysfunction and type 2 diabetes. Current Diabetes Reports 2005 Jun;5(3):

CARBOHYDRATE & LIPID METABOLISM – 195

sensitivity when fat forms a large portion (≥27%) of the diet, with diets higher in saturated fats perhaps having a marginally greater negative effect.570 Type of fatty acid apparently has only a minor effect compared to total amount of fat. This implies that we must reduce total fat intake, not just manipulate types of fats, in order to improve insulin sensitivity. In support of this, an arm of the LIPGENE study, diets high in either saturated or monounsaturated fats had similar effects on insulin sensitivity, whereas a plant-based (low-fat, high-complex carbohydrate) diet containing adequate omega-3 fatty acids improved insulin sensitivity.571

Any food rich in total and saturated fats also supplies large amounts of unsaturated fats; in fact, unsaturated fats generally make up more than 50% of the fats in animal flesh (Table 16.1). About 57% of human animal fat consists of unsaturated fats that fat cells would release for oxidation in case of food shortage. In the case of starvation, the cells would have to oxidize a fat fuel mix consisting of 43% saturated, 47% monounsaturated, and 10% polyunsaturated fats. Therefore, it seems that cellular lipid metabolism evolved in a context wherein any increased exposure to saturated fats, whether from food or adipose tissue during starvation, would always involve a simultaneously increased exposure to unsaturated fats. This makes it unlikely that mitochondria could have highly distinct responses to individual types or sub-fractions of types of dietarily non-essential fats. This would explain why altering ratios of types of fats has little effect on insulin sensitivity.

Together the data in this and the previous section suggest that natural selection favored humans who would reduce their fat and glucose oxidation and total metabolic rate in response to elevated cellular exposure to fats, perhaps particularly if rich in saturated fats.

This same response (insulin resistance with reduced fat and glucose oxidation and metabolic rate) occurs in humans and rodents subjected to energy deprivation through food restriction.572, 573, 574, 575

Why do humans (and some other mammals, such as rodents) have similar metabolic responses to food deprivation and diets rich in fats?

570 Galgani JE. Saturated fat and insulin resistance. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition, and Natural Resources 2009 Dec 9;4(67):1-5.

571 Tierney AC, McMonagle J, Shaw DI, et al.. Effects of dietary fat modification on insulin sensitivity and on other risk factors of the metabolic syndrome–LIPGENE: a European randomized dietary intervention study. Int J Obes (Lond) 2011 Jun;35(6):800-9.

572 Dulloo AG, Girardier L. Adaptive changes in energy expenditure during refeeding following low-calories intake: evidence for a specific metabolic component favoring fat storage. Am J Clin Nutr 1990;52:415-20.

573 Crescenzo R, Lionetti L, Mollica MP, et al.. Altered Skeletal Muscle Subsarcolemmal Mitochondrial Compartment During Catch-Up Fat After Caloric Restriction. Diabetes 2006;55:2286-93.

574 Summermatter S, Mainieri D, Russell AP, et al.. Thrifty metabolism that favors fat storage after caloric restriction: a role for skeletal muscle phosphatidylinositol-3-kinase activity and AMP-activated protein kinase. FASEB J 2008;22:774-85.

575 Deutz RC, Denardot D, Martin DE, Cody MM. Relationship between energy deficits and body composition in elite female gymnasts and runners. Med Sci Sports Exerc 2000;32(3):659-68.

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I suggest that an elevated mitochondrial exposure to a fuel mix predominated by fatty acids primarily occurred among human ancestors when they were metabolizing their own (animal) fat stores (57% unsaturated and 43% saturated fats, Table 16.1) as a result of food shortages. Natural selection would have favored those individuals who would respond to this signal (elevated delivery of fats to the mitochondria) with insulin resistance, a reduced rate of fat and glucose oxidation, and increased fat storage, because these individuals would use nutrient stores at a slower rate during energy restriction and more likely survive prolonged food shortages.

If this is the case, perhaps diets high in fats – particularly diets rich in animal fats having a saturated:unsaturated ratio similar to human body fat – send a false signal of energy deprivation to the cells, leading to down-regulation of fat and glucose oxidation and up-regulation of fat storage mechanisms. This would contribute to explaining why people following diets rich in animal flesh, eggs, and milk tend to carry more body fat and have a higher risk of type 2 diabetes than those who consume low-fat plant-based diets, as mentioned in Chapter 8 and discussed in greater detail below.

Obesity and Meat-Rich Diets

The finding that saturated fats impair fat and glucose oxidation predicts that meat-rich diets will promote fat gain in humans.

In 1997, Kahn et al. reported that among 79,236 caucasians, ten year increases in body mass index and waist weight gain were positively associated with kcalorie-adjusted meat consumption and negatively associated with kcalorie-adjusted vegetable consumption.576 Kahn et al. state that their results “suggest that weight change may be linked to the proportion of energy derived from fat or to other unidentified components of meat.”

In 2010 Vergnaud et al. reported that red meat, poultry, and processed meat all were positively associated with weight gain.577 The data from this study indicated that every increase in meat intake of 250 g/day (e.g. one steak at ~450 kcal) would lead to a 2 kg higher weight gain after 5 years.

In 2011, Halkjaer et al. reported that a higher intake of total protein and animal protein was associated with subsequent weight gain over a mean period of 6.5 years. The association was driven by red meat, processed meat, and poultry. They found no association between plant protein and increases in body weight.578

576 Kahn HS, Tatham LM, Rodriguez C, et al.. Stable behaviors associated with adults’ 10-year change in body mass index and likelihood of gain at the waist. Am J Pub Health 1997 May;87(5):747-54. Quote from page 752.

577 Vergnaud AC, Norat T, Romaguera D, et al.. Meat consumption and prospective weight change in participants of the EPIC-PANACEA study. Am J Clin Nutr 2010 Aug;92(2):398-407.

578 Halkjaer J, Olsen A, Overvad K, et al.. Intake of total, animal and plant protein and subsequent changes in weight or waist circumference in European men and women: the Diogenes project. Int J Obes (Lond) 2011 Aug;35(8):1104-13. Abstract.

CARBOHYDRATE & LIPID METABOLISM – 197

In 2011, Bujnowski et al. reported that among the 1,730 U.S. men who participated in the Chicago Western Electric Study between 1958-1966, those who ate the most animal flesh had a doubled risk of being overweight and a 4.6 times greater risk for obesity compared to those with the lowest intake. Also, those who had the highest intake of plant protein had a 42% reduced risk of obesity compared to those with the lowest intake.579 This finding is remarkable considering that men in the lowest and highest quartiles of animal consumption obtained, respectively, 75 g and 100 g of animal protein daily and cholesterol intakes ranged from 660 mg/d to 812 mg/d. In other words, all of these men were consuming large amounts of animal food.

Mozaffarian et al. reported in 2011 that in the Nurses Health and Health Professionals Follow-up studies involving more than 120,000 women and men, a daily serving of red meat was associated with 0.95 pound weight gain and processed meats with a 0.93 pound gain. In contrast, vegetables, whole grains, fruits, and nuts were associated with weight reductions of 0.22, 0.37, 0.49, and 0.57 pounds, respectively.580

In 2012, Shay et al. reported that among 1794 American participants in the INTERMAP study, higher intakes of fruit, pasta, rice, carbohydrates, fiber, potassium, and magnesium were all associated with lower body mass in both sexes, while higher intakes of meat and several of its components–sodium, cholesterol, saturated fats, and heme iron–were all associated with higher body mass. Among men, higher body mass was associated with higher intakes of fish, beef, pork, veal, and game meats, and lower intakes of whole grains, pasta, rice, nuts, snacks, and sweets. Among women, higher body mass was associated with higher intakes of poultry, beef, pork, veal, and game meats, and lower intakes of whole grains, fish (borderline), and snacks and sweets. Overall, the pattern was of higher body mass associated with more animal-based diets, and lower body mass associated with more plant-based diets.581

Obesity Among Mongols and Inuit

The Mongols and Inuit (Eskimos) have lived for thousands of years in relative isolation on low- carbohydrate, grass-fed and wild animal-based diets. Among them, natural selection has had an extended opportunity to favor any metabolic adaptations humans might have to high fat animal-based diets. Yet the following studies suggests that Mongols and Inuit have an increased risk of obesity, hypertension, and hyperlipidemia when eating animal-based diets and can reduce their risk by reducing animal intake and eating more plant-based diets.

579 Bujnowski D, Xun P, Daviglus ML, et al.. Longitudinal association between animal and vegetable proteins intake and obesity among adult males in the United States: the Chicago Western Electric Study. J Am Diet Assoc 2011 Aug;111(8): 1150-55.

580 Mozaffarian D, Hao T, Rimm EB, et al.. Changes in Diet and Lifestyle and Long-Term Weight Gain in Women and Men. N Engl J Med 2011 June 23;364:2392-2404.

581 Shay CM, Van Horn L, Stamler J, et al.. Food and nutrient intakes and their associations with lower BMI in middle-aged US adults: the International Study of Macro-/Micronutrients and Blood Pressure (INTERMAP). Am J Clin Nutr 2012 Sept; 96(3):483-91.

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In 2009, Wang et al. reported that among 3732 adults greater than 30 years old of Bortala prefecture of the Xinjiang autonomous region, China, including Mongolians, Kazahkans, Uygurs, and Hans, 36% were overweight and 27% obese. The Mongolians had the greatest risk of overweight and obesity. Mongolian men had the highest rate of obesity of the several ethnic groups. An animal-based diet was a risk factor for overweight and obesity in all ethnic groups.582

Dugee et al. reported that Mongols following traditional and “transitional” animal-based dietary patterns had an increased risk of general and abdominal obesity, while those eating more plant-based diets had the lowest risk.583 Dugee et al. also reported high rates of overweight, obesity, and abdominal obesity among Mongolians eating animal-based diets.584

Li et al. also reported that 68% of Mongolians have a body mass index falling into the overweight category. In addition, 56% of Mongolians had hypertension, and 63% had abnormal blood lipids. Li et al. also found high rates of overweight (70% and 66%, respectively), hypertension (40% and 54%, respectively), and dyslipidemia (72% and 67%, respectively) among the Uygur and Kazakh ethnic groups in China. Most of the Mongolians and Kazahks live as herders, and all three ethnic groups have diets high in animal flesh or milk. In comparison, Chinese Han ethnics eat more grain, fresh vegetables, beans, bean products, and less animal products and had lower prevalence of overweight (53%), hypertension (33%), and dyslipidemia (49%).585

In 2012 Zienczuk et al. reported that among Canadian Inuit living in the high arctic and still consuming a predominantly meat-based diet, 60% of men and 66% of women had an at-risk BMI. In this population, obesity affected 42% of men and 27% of women, and overweight affected 33% of men and 25% of women. Zienczuk et al. found that among these Inuit, a significant trend for decreasing prevalence of an at-risk BMI was observed across increasing quartiles of carbohydrate intake, but not for increasing quartiles of high-fat traditional foods intake. Among these Inuit, at-risk BMI was most prevalent among those who ate the diets lowest in carbohydrate.586 Prior to this report, Hopping et al. had reported in 2010 that 72% of 218 Inuit adults were classified as either overweight or obese, despite having high levels of physical activity.587 It seems that Inuit become as over-fat as any other ethnic group would on a high-fat animal-based diet.

582 Wang K, Ao Y, Zhao L, et al.. Analysis on obesity and its risk factors among inhabitants of Bortala prefecture of Xinjiang autonomous region. Chinese J Pub Health 2006-09. Abstract.

583 Dugee O, Khor GL, Lye M-S, et al.. Association of major dietary patterns with obesity risk among Mongolian men and women. Asia Pac J Clin Nutr 2009;18(3):433-440.

584 Dugee O, Khor GL, Lye MS, et al.. Obesity among Mongolian Adults form Urban and Rural Areas. Mal J Nutr 2009;15(2):185-194.

585 Li N, Wang H, Yan Z, et al.. Ethnic disparities in the clustering of risk factors for cardiovascular disease among the Kazakh, Uygur, Mongolian and Han populations of Xinjiang: a cross-sectional study. BMC Public Health 2012;12:499.

586 Zienczuk N, Young TK, Cao ZR, Egeland GM. Dietary correlates of an at-risk BMI among Inuit adults in the Canadian high arctic: cross-sectional international polar year Inuit health survey, 2007-2008. Nutrition Journal 2012;11:73.

587 Hopping BN, Erber E, Mead E, et al.. High levels of physical activity and obesity co-exist amongst Inuit adults in Arctic Canada. J Hum Nutr Diet 2010;23(Suppl 1):110-14.

CARBOHYDRATE & LIPID METABOLISM – 199

Cholesterol

According to the Institute of Medicine, Food and Nutrition Board:

“Cholesterol plays an important role in steroid hormone and bile acid biosynthesis and serves as an integral component of cell membranes. Given the capability of all tissues to synthesize sufficient amounts of cholesterol for their metabolic and structural needs, there is no evidence for a biological requirement for dietary cholesterol. Therefore, neither an Adequate Intake nor a Recommended Dietary Allowance is set for cholesterol.”588 [Italic added]

Since modern humans do not require dietary cholesterol, we can conclude that ancestral humans also had no requirement for dietary cholesterol.

Since all mammals produce cholesterol in their cells and in their livers, the consumption of dietary cholesterol presents the possibility of excessive accumulation of cholesterol in body tissues. Consequently, in carnivores, natural selection would favor the reproduction of individuals capable of limiting endogenous production and increasing excretion of cholesterol.

Although containing virtually no cholesterol, plant foods contain fiber and phytosterols which increase cholesterol excretion or block the reabsorption of cholesterol from bile acids. An animal adapted to a plant-based diet containing little or no animal flesh would therefore probably require a higher endogenous production of cholesterol and more efficient bile acid reabsorption than an animal adapted to a carnivorous diet. In this animal, natural selection will favor high endogenous production of cholesterol and mechanisms for cholesterol conservation in the face of the cholesterol-free and cholesterol-reducing diet.

If such an animal stops eating the whole plant foods to which it is adapted, its own cholesterol production, coupled with strong cholesterol reabsorption, may lead to an excessive cholesterol accumulation. If this animal consumes animal flesh, this also will tend to cause the animal to accumulate cholesterol.

Thus, we expect that animals adapted to carnivorous diets will have mechanisms for preventing cholesterol accumulation, and animals adapted to plant-based diets will have mechanisms for producing and conserving cholesterol. The former type of animal will be resistant to diseases involving excessive cholesterol accumulation, such as hyperlipidemia and atherosclerosis, and the latter type will be prone to such diseases.

588 Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients). The National Academies Press, 2005. 542.

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Hyperlipidemia

Hyperlipidemia consists of having blood lipid levels above physiologically required levels. We can determine physiologically required levels of total lipoproteins and lipoprotein fractions (total cholesterol, LDL, HDL, etc.) by testing those levels in wild animals, foraging humans, newborn humans, and human populations having very low cholesterol levels coupled with a high resistance to cardiovascular disease. Doing so we find that wild animals, non-human primates, human foragers (hunter-gatherers), and human newborns all have serum total cholesterol levels ranging from 70 to 150 mg/dL and LDL levels ranging from 30 to 70 mg/dL.589

Several populations with high immunity to cardiovascular diseases also have average serum cholesterols below 150 mg/dl, including rural Chinese (127 mg/dl)590, Tarahumaras (125 mg/dl)591, and Caucasian men eating macrobiotic diets (147 mg/dl).592

Parasite infections contribute to the low cholesterol levels found in contemporary hunter-gatherer and pastoral tribes consuming large amounts of animal flesh.593 Prehistoric hominins had obtained tapeworms from meat-eating by two million years ago.594 Tapeworms require cholesterol and fats for development of their larval cysts, but have lost the ability to produce these lipids, so they obtain them from their hosts.595 Other parasites also deplete hosts of cholesterol.596, 597, 598, 599

589 O’Keefe JH, Cordain L, Harris WH, Moe RM, Vogel R. Optimal Low-Density Lipoprotein Is 50 to 70 mg/dl. J Am Coll Cardiol 2004;43: 2142–6.

590 Campbell TC, Parpia B, Chen J. Diet, lifestyle, and the etiology of coronary artery disease: the Cornell China study. Am J Cardiol. 1998 Nov 26;82(10B):18T-21T.

591 McMurry MP, Conner WE, Cerqueira MT. Dietary cholesterol and the plasma lipids and lipoproteins in the Tarahumara Indians: a people habituated to a low cholesterol diet after weaning. Am J Clin Nutr l982;35:741-744.

592 Knuiman JT, West CE. The concentration of cholesterol in serum and in various serum lipoproteins in macrobiotic, vegetarian and non-vegetarian men and boys. Atherosclerosis. 1982 May;43(1):71-82.

593 Vasunilashorn S, Crimmins EM, Kim JK, et al.. Blood Lipids, Infection, and Inflammatory Markers in the Tsimane of Bolivia. Am J Hum Biol 2010 Nov-Dec;22(6):731-40.

594 Hoberg EP, Alkire NL, Queiroz AD, Jones A. Out of Africa: origins of the Taenia tapeworms in humans. Proc R Soc Lond B 2001 April 22;268(1469):781-87.

595 Tsai IJ, Zarowiecki M, Holroyd N, et al.. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 2013 April 4;496:57-63.

596 Sianto L, Chame M, Silva CS, et al.. Animal helminths in human archaeological remains: a review of zoonoses in the past. Rev Inst Med Trop Sao Paulo. 2009 May-Jun;51(3):119-30. PMID: 19551285.

597 Bansal D, Bhatti HS, Sehgal R. Altered lipid parameters in patients infected with Entamoeba histolytica, Entamoeba dispar and Giardia lamblia. Br J Biomed Sci. 2005;62(2):63-5. PMID:15997878

598 Stanley RG, Jackson CL, Griffiths K, Doenhoff MJ. Effects of Schistosoma mansoni worms and eggs on circulating cholesterol and liver lipids in mice. Atherosclerosis 2009 Nov;207(1):131-8. PMID: 19464685.

599 Bansai D, Singh Bhatti H, Sehgal R. Role of cholesterol in parasitic infections. Lipids in Health and Disease 2005;4:10.

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In the absence of infections or diseases that affect cholesterol metabolism and levels, human cholesterol levels rise in a dose-response fashion to dietary cholesterol. A cholesterol-free, high fat (40% energy) diet produced average serum cholesterol of 164 mg/dl; adding 126 mg cholesterol produced an average serum cholesterol of 174 mg/dl; 212 mg cholesterol daily raised serum cholesterol to an average of 181 mg/dl; and 317 mg cholesterol daily raised the average to 198 mg/dl.600

In contrast, Pertsemlidis et al. reported that cholesterol-fed dogs do not accumulate cholesterol in the body pools.601 Apparently, in dogs cholesterol-consumption completely suppresses endogenous cholesterol synthesis and enhances bile acid excretion to prevent cholesterol accumulation. This shows that in the canine family, natural selection has favored the reproduction of individuals who have mechanisms for preventing an overdose of cholesterol in the face of a constantly high dietary intake.

Animal proteins also raise serum cholesterol levels in comparison to plant proteins. Carefully conducted studies have shown then given diets with matched amounts and types of fats, cholesterol, and total protein, but different ratios of plant and animal protein, human and animal subjects display higher serum cholesterol levels when eating diets with a higher ratio of dairy or meat protein.602

Elevated serum cholesterol promotes the development of atherosclerosis in animals including humans even in the absence of other risk factors.603 According to the National Heart, Lung, and Blood Institute:

“The induction of hypercholesterolemia is a prerequisite for atherogenesis, and sometimes myocardial ischemia, in various experimental animals. In addition, certain species have hereditary forms of hypercholesterolemia and develop atherosclerosis spontaneously; a classical example is the WHHL rabbit, which carries the same molecular defect as human familial hypercholesterolemia. In contrast, low LDL-cholesterol levels are well tolerated. LDL cholesterol as low as 25–60 mg/dL is physiologically sufficient. Animal species that do not develop atherosclerosis generally have LDL-cholesterol levels below 80 mg/dL. The LDL- cholesterol concentration in the newborn infant is approximately 30 mg/dL, indicating that such low levels are safe. Moreover, persons who have extremely low levels of LDL throughout life due to familial hypobetalipoproteinemia have documented longevity.”604

600 Mattson FH, Erickson BA, Kligman AM. Effect of dietary cholesterol on serum cholesterol in man. Am J Clin Nutr1972; 25(6):589-594.

601 Pertsemlidis D, Kirchman EH, Ahrens EH. Regulation of Cholesterol Metabolism in the Dog. J Clin Invest 1973 Sept; 52(9):2353-2367. PMCID: PMC333040.

602 Sirtori CR, Lovati MR, Manzoni C, et al.. Soy and Cholesterol Reduction: Clinical Experience. J Nutr 1995 March 1;125(3):598S-605S.

603 Samson S, Mundkur L, Kakkar V. Immune Response to Lipoproteins in Atherosclerosis. Cholesterol. 2012; 2012: 571846.

604 National Institutes of Health. Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III), NIH Publication No. 02-5215 September 2002.

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In short, in humans not suffering from cholesterol-depleting parasitic infections, eating cholesterol (animal flesh, eggs, or milk) raises serum total and LDL cholesterol, and this promotes atherosclerosis. In contrast, intact animals physiologically adapted to consumption of flesh can consume cholesterol in their daily diet without elevation of serum lipids or increased risk of atherosclerosis.

Spontaneous Atherosclerosis

Scientists have induced atherosclerosis in many other species biologically adapted to primarily plant- based diets, including other primates, rodents (mice, rabbits, rats, hamsters, guinea pigs), swine, and some birds. However, according to Dr. Mohammed Moghadasian, DVM, MSc, PhD, they have found it quite difficult to induce atherosclerosis in animals biologically adapted to eating animal flesh.605 In a historical review of atherosclerosis research in animal models he wrote:

“Spontaneous atherosclerosis is rare in dogs; even high cholesterol diet does not result in the development of advanced atherosclerotic lesions in dogs.”606

“Cats have not been frequently used in atherosclerosis research, simply because they are resistant to atherosclerosis.”607

In contrast to the flesh-eating animals, humans readily develop atherosclerosis when consuming diets regularly containing animal flesh. Atherosclerosis begins in early childhood, and elevated non-HDL cholesterol constitutes one of the greatest risk factors for advancement of the disease throughout life.608

Proponents of flesh-based diets have suggested that humans living on “traditional” diets consisting largely of animal flesh had no coronary atherosclerosis so long as they had no contact with wheat or refined carbohydrates. Evidence casts much doubt on this suggestion.

Autopsies of the frozen bodies of pre-contact Inuit (Eskimo) individuals dating to as early as 400 CE and as late as 1520 CE have found both coronary and aortic atherosclerosis.609 Of further interest, two of these mummies, females aged 25-30 y and 42-45 y, “showed severe osteoporosis.”610

605 Moghadasian MH. Experimental atherosclerosis: A historical overview. Life Sciences 70 (2002) 855–865.

606 Ibid.

607 Ibid.

608 McMahan CA, Gidding SS, Malcom GT, et al.. Pathobiological Determinants of Atherosclerosis in Youth Risk Scores Are Associated with Early and Advanced Atherosclerosis. Pediatrics 2006 Oct 1;118(4):1447-1455.

609 Zimmerman MR. The Paleopathology of the Cardiovascular System. Texas Heart Institute Journal 1993;20:252-7.

610 Ibid.

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The idea that Inuit have historically enjoyed a high immunity to cardiovascular disease has never had firm evidential support. In fact, physicians have reported high rates of both atherosclerosis and heart disease at young ages in Inuits since the early 19th century:

“Bertelsen in his classic 1940 description of the disease and mortality pattern among the Inuit of Greenland stated that ‘arteriosclerosis and degeneration of the myocardium are quite common conditions among the Inuit, in particular considering the low mean age of the population.’[1]. Bertelsen, who is considered the father of epidemiology in Greenland, based his opinion both on many years of clinical practice in Greenland and on the reports of medical officers since 1838.”611

“The current scientific evidence from clinical, X-ray and ultrasound studies seem to allow the cautious conclusion that atherosclerosis has been present among the Inuit at levels by and large similar to those of white populations of North American and Europe, at least in the Eastern Arctic...Our updated analyses of mortality indicate that the mortality from IHD [ischemic heart disease] was similar among the Inuit and the southern comparison populations or slightly lower.”612

Contemporary Inuits have suffered high rates of cardiovascular disease “despite the substantial proportion of the populations maintaining traditional lifestyles and high intakes of omega-3 fatty acids” and, among these people, high levels of serum cholesterol strongly correlate with both heart disease and stroke risk.613

CT scans of mummies of five Unangan natives from the Aleutian Islands, dating to 1850-1900 CE, found that three (60%) had definite atherosclerosis.614 Of those, two were females aged 25-29 y and 47-51 y, and the third a male aged 40-44 y. The other two individuals died before the age of 25; one of those was a child aged 4-5 y. These people consumed diets consisting primarily of marine mammals, shellfish, sea urchins, eggs, and fish.

Ancient native Americans also had atherosclerosis. CT scans of two of four (50%) of mummies of ancestral Puebloans dated to 1500 BCE-500 CE found probable atherosclerosis; one case was a male aged 18-23 y with probable aortic atherosclerosis, and the other a female aged 46-51 with definite disease of the carotids, coronaries, aorta, and iliac/femoral arteries.615 During the dated period of Pueblo

611 Bjerregaard P, Young TK, Hegele RA. Low incidence of cardiovascular disease among the Inuit––what is the evidence? Atherosclerosis 2003;166:351-7.

612 Ibid.

613 Howard BV, Comuzzie A, Devereaux RB, et al.. Cardiovascular Disease Prevalence and its Relation to Risk Factors in Alaska Eskimos. Nutr Metab Cardiovasc Dis 2010 June;20(5):350-358.

614 Thompson RC, Allam AH, Lombardi GP, et al.. Atherosclerosis across 4000 years of human history: the Horus study of four ancient populations. Lancet 2013 Apr 6;381(9873):1211-22.

615 Ibid.

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culture, the people were making a transition from hunting and gathering to early agriculture. They hunted with spears and consumed rabbits, mice, big horn sheep, mule deer, and fish. One of these mummies was found in a cave with a buckskin sack.

The authors of the HORUS study that included the Unangan and Puebloan mummies discussed above claimed that the presence of atherosclerosis in these as well as ancient Egyptian and Peruvian mummies “suggests that the disease is an inherent component of human aging and not characteristic of any specific diet or lifestyle.”616 Yet they also state that none of the mummified members of these four cultures ate a plant-based diet; all ate animal products.617 All animal flesh provides dietary cholesterol. Since none of these groups ate diets free of cholesterol, these authors have no basis for their suggestion that diet plays no role in development of atherosclerosis.

In fact, the HORUS data shows the lowest incidence of probable or definite atherosclerosis in the ancient Peruvian farmers (25%), followed by the Egyptian royalty (38%), Puebloans in transition from hunting and gathering to farming (40%), and Unangan hunter-gatherers (60%). Further, the mean ages for the four groups were 37, 37, 28, and 29 years, respectively; and, the oldest Unangan was 47-51, whereas the Peruvian and Egyptian mummies included individuals older than 55. Thus, the Puebloan and Unangan mummies were of younger age, but a greater proportion had lesions. As stated by the authors, the Peruvians were farmer-foragers who lived in mud huts and ate corn, potatoes, sweet potatoes, tarwi, manioc, peanuts, beans, and bananas; but the mummified Egyptians included royalty, scribes, and priests, individuals of higher social status and greater wealth who probably had significant intakes of domesticated grass-fed animal products.618 Hence, in this study, it appears that the incidence of atherosclerosis probably increased step-wise with the intake of animal flesh across these four ancient populations.

In 1925, Kuczynski reported that the Kirghiz nomads who lived almost exclusively on grass-fed animal products suffered cardiac symptoms and arteriosclerosis “in an intense degree and often at an early age.”619, 620

616 Ibid., 11.

617 Ibid., 10.

618 Ibid., 10.

619 Bernstein FL, Burton C, Healey D. Soviet Medicine: Culture, Practice, Science. Northern Illinois University Press, 2010. 75.

620 Bjornsson J. Arteriosclerosis: A Chemical And Statistical Study. Copenhagen, 1942. 32.

CARBOHYDRATE & LIPID METABOLISM – 205

Simian Diet Effect On Human Blood Lipids

Jenkins et al. performed an experiment to evaluate the effect of a “simian diet” on serum lipid risk factors for cardiovascular disease.621 The diet contained no animal products and consisted entirely of plant foods that humans can consume uncooked:

• Unlimited green leaves, emphasizing cabbage, bok choy, chard, spinach, brussels sprouts, and leeks (goal: 600 g) • Unlimited flowers (broccoli and cauliflower) • Unlimited fresh vegetables that subjects could consume raw, such as carrots, celery, radishes, and mushrooms • Large amounts of botanical fruits: • Unlimited savory fruits (tomatoes, okra, sweet peppers, zucchini, cucumbers, and eggplant) • Unlimited fresh legumes, including green beans, bean sprouts, and garden peas, with a goal of 500 g of peas • Sweet yellow corn, aiming for 500 g per day • Fresh sweet fruits, as much as needed to maintain body weight • Raw almonds, cashews, peanuts, and avocados in limited amounts (nuts, 60 to 129 g per day), or as needed to maintain body weight

Subjects could boil or steam any food if desired. When on this diet, subjects consumed an average of 2300 kcal, 72 g protein (12% energy), 65 g fat (25% energy), 9 g saturated fat (4% energy), and 64 g fiber. After just two weeks on this regimen, although body weight had not significantly changed, the subjects had markedly reduced serum lipoproteins and lipids, as follows:

• Total cholesterol, down 25% • LDL cholesterol, down 33% • Triglycerides, down 20% • Apo B, down 30% • Lp(a), down 24%

At the start of the primate diet phase, subjects had an average total cholesterol level of 4.7 mmol/L (182 mg/dL) and LDL of 2.76 mmol/L (107 mg/dL); after two weeks on the primate diet they had levels of 3.7 mmol/L (143 mg/dL) and 1.95 mmol/L (75 mg/dL), respectively, putting them in the normal range for wild animals.

This evidence suggests that humans have a cholesterol metabolism adapted to a diet free of animal flesh, eggs, and milk, and consisting primarily of vegetables and botanical fleshy and dry fruits, including culinary sweet and savory fruits, legumes, nuts, and seeds.

621 Jenkins DJA, Popovich DG, Kendall CWC, et al.. Effect of a Diet High in Vegetables, Fruit, and Nuts on Serum Lipids. Metabolism 1997 May;46(5):530-37. http://www.vegsource.com/nuts/jenkins.pdf

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Summary

If humans had significant biological adaptation to consumption of animal flesh, we would probably oxidize fats at least as readily as we oxidize glucose, and if our ancestral diet had been high in fats, we would have mechanisms for regulating body fat stores. The facts that we oxidize glucose more readily than we store it, we store dietary fats more readily than we oxidize them, and we lack mechanisms for regulating body fat storage, altogether imply that human metabolism evolved in response to a diet containing plentiful carbohydrate but little fat, a profile that characterizes a plant-based diet.

If humans had significant biological adaptation to consumption of animal flesh, we would probably oxidize saturated fats at least as readily as we oxidize unsaturated fats. The data presented in this chapter indicates that we oxidize unsaturated fats somewhat more readily than we oxidize saturated fat. This supports the hypothesis that human lipid metabolism is primarily adapted to a plant-based rather than animal-based diet.

The human metabolic response to consumption of diets high in saturated animal fats resembles the metabolic response to food energy restriction. During food restriction, cells metabolize our own stored saturated animal fats and proteins. This suggests the hypothesis that elevated cellular metabolism of saturated fats or other components of animal flesh serves as a signal to down-regulate nutrient oxidation in order to prolong survival during food restriction. If so, frequent consumption of animal foods sends a false signal of starvation to muscle cells, resulting in insulin resistance, reduced fat and glucose oxidation, and increased fat storage. A substantial body of data indicates that consumption of animal tissues promotes fat gain and diabetes, consistent with this hypothesis.

When humans consume animal flesh, eggs, or milk, they ingest cholesterol, saturated fat, and animal protein, and, as a general rule, absent pathologies that reduce cholesterol, these all work together to raise the serum lipids to biologically abnormal levels and promote atherosclerosis. Animals naturally adapted to consumption of flesh, such as cats and dogs, do not develop elevated serum lipids nor atherosclerosis when consuming cholesterol or flesh-based diets, and spontaneous atherosclerosis occurs only in herbivores fed cholesterol or other animal-derived nutrients. Humans rapidly achieve serum biologically normal lipid levels when consuming a plant-based, largely frugivorous diet similar to that consumed by wild great apes.

All of this data supports the conclusion that humans have a lipid metabolism naturally adapted to a plant-based diet and not requiring nor tolerant of any significant, habitual intake of animal flesh. Probably human cholesterol metabolism evolved on a diet providing little or no cholesterol, which occurs only in animal flesh, eggs, and milk.

CARBOHYDRATE & LIPID METABOLISM – 207

17: Brain Size & Metabolism

Some people believe that in human evolution a presumed need to hunt animals imposed cognitive demands that favored of reproduction of individuals with greater intelligence and larger, more complex brains, and that consumption of flesh, particularly of brains, marrow, or sea animals, provides specific nutrients absent or limited in plants but required by a species developing a larger, more complex brain over evolutionary time spans (millions of years). Supporters of this hypothesis suggest that no activity other than hunting imposes similar or greater cognitive demands, and make statements like “meat made us human.”622

This raises three questions: First, do carnivorous animals have larger, more complex brains than any other kind of animal? Second, does the claim that only animal flesh could supply human ancestors with sufficient amounts of any of the nutrients identified as essential for brain evolution withstand critical scrutiny? Third, do any activities other than hunting impose similar or greater cognitive demands on a primate species?

Encephalization Quotient

If among terrestrial animals, hunting or eating flesh provides the most potent stimulus or nutritional support for brain growth, we would expect flesh-eating animals to have the largest brains and all relatively large-brained species to have diets based on flesh. However, when we compare the relative encephalization of various species, the flesh-eating animals do not dominate, and not all large-brained species have flesh-based diets.

The encephalization quotient (EQ) compares the brain size (relative to body mass) of any species to the value for a non-existent “average mammal” of comparable body mass. If a species has an EQ of 2.0, this means it has a relative brain size twice that expected for a “average” mammal of its body mass; and a species with an EQ of 0.5 has a relative brain size half that expected for an “average” animal of its body mass. Table 17.1 shows the EQ values for a number of species.

Chimpanzees, capuchin monkeys, and elephants have among the largest EQs, yet they live on primarily plant-based diets. The folifrugivorous chimp’s EQ is more than double that of the carnivorous canines. The only carnivores with remarkably large EQs are marine species; no known terrestrial carnivore has a remarkably large EQ. Among terrestrial animals, frugivores have the largest EQs.

622 Bunn HT. Meat Made Us Human. In Evolution of the Human Diet: The Known, the Unknown, and the Unknowable, edited by Peter S. Ungar. Oxford University Press, 2007.

209

Table 17.1: Encephalization quotient, brain mass, cortical neuron count, and diet for selected species. Species EQ Brain Mass (g) Cortical Neuron Count Diet (primary food) (millions) Human 7.4–7.8 1200-1450 11-14,000 Frugivore Dolphin (bottlenose) 5.3 1350.0 5800.0 Carnivore White-fronted 4.8 57-80 600-700 Frugivore capuchin Capuchin monkeys 2.4-4.8 26-80 600-700 Frugivore Chimpanzee 2.2–2.5 330-440 6200.0 Frugivore Squirrel monkey 2.3 23.0 430.0 Frugivore Rhesus Monkey 2.1 88-106 Frugivore Gibbon 1.9-2.7 88-105 Frugivore (66%) Gorilla 1.5-1.8 430-570 4300.0 Folivore or frugivore Whale 1.8 2600-9000 10,500 Varies Fox 1.6 53.0 Carnivore Elephant 1.3 4200.0 11,000 Herbivore Dog 1.2 64.0 160.0 Carnivore Squirrel 1.1 7.0 Frugivore Cat 1.0 25.0 300.0 Carnivore Horse 0.9 510.0 1200.0 Herbivore Sheep 0.8 140.0 Herbivore Lion 0.6 260.0 Carnivore Mouse 0.50 0.3 4.0 Herbivore Rat 0.40 2.0 15.0 Herbivore Rabbit 0.40 11.0 Herbivore Source: Roth G, Dicke U. Evolution of brain and intelligence in primates. In: Evolution of the Primate Brain: From Neuron to Behavior. Ed. by Michel A Hofman and Dean Falk. Elsevier, 2012. 424.

Is Seafood Superior Brain Food?

The EQ is based on an expected brain mass for an animal of the size found in any species. However, when discussing nutritional influences on brain size, people refer to the need for a certain dietary amount of certain nutrients imagined to be essential for building the brain, usually omega-3 fats or certain minerals. They seem to suggest that large intakes of these nutrients favors evolution of an unusually large brain.

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According to Sea World, an adult dolphin has a body mass in the range of 150 to 450 kg623 and consumes about 4 to 5 percent of its body mass in food each day.624 Taking the median body mass of 300 kg, this amounts to 12 to 15 kg seafood daily. Despite this massive intake of seafood, the dolphin has a brain mass of 1350 g, about the same as a human, in a body 6 times the mass of the human. Comparing brain mass to body mass, a 70 kg human has up to 20 g brain mass per kg body mass, and a 50 kg chimpanzee has up to 8 g brain mass per kg body mass, whereas a 300 kg dolphin has only about 5 g of brain mass per kg body mass.

To wit, other mammals also consume loads of seafood, yet do not have extraordinary brains in terms of mass or EQ. Although whales consume enormous amounts of seafood, they have an EQ smaller than either chimps or capuchins. Polar bears (males, 350-770 kg) primarily prey upon ringed seals, whose flesh has a high concentration of marine fats and minerals, yet they only have 500 g brains.625 California sea lions (males, average 300 kg) eat anchovies, sardines, and mackerel, all fatty fish rich in omega-3 fats, yet have only 363 g brains.626

In comparison, the elephant develops a brain 8 to 10 times as large as a polar bear or sea lion mammals, without eating any seafood or land animal foods, obtaining all the nutrients it requires for brain development from a variety of terrestrial plant foods. Chimpanzees develop more brain mass per kg body mass than a dolphin, without ever consuming marine animals. Billions of humans develop brains of the same mass as found in a dolphin, without consuming anywhere near the amount of sea animals.

When examined in this fashion, it does not appear that a diet of marine animals provides any extraordinary support or stimulus for development of brain mass. We simply lack evidence that development of a large brain requires ingestion of seafood or any of the nutrients it seemingly uniquely provides.

Cerebral Neuron Count

Although carnivorous dolphins have a larger EQ than chimpanzees, the frugivorous chimpanzees, who weigh 30 to 70 kg, have about the same number of cerebral neurons as carnivorous bottlenose dolphins weighing 150 to 450 kilograms. Compared to the dolphin, the chimp has at least twice as many cerebral cortex neurons per kilo of body mass.

The number of neurons per gram of brain mass gives some idea of the complexity of the brain as well as the amount of brain activity in terms of number of communicating neurons. Possibly, the greater the number of neurons per unit of brain mass, the greater the capacity for information processing. Dolphins

623 Sea World. Bottlenose Dolphin Physical Characteristics. http://www.seaworld.org/animal-info/info-books/bottlenose/ physical-characteristics.htm

624 Sea World. Bottlenose Dolphin Diet and Eating Habits. http://www.seaworld.org/infobooks/bottlenose/dietdol.html

625 Chudler EH. Brain Facts and Figures. http://faculty.washington.edu/chudler/facts.html

626 Ibid.

BRAIN SIZE & METABOLISM – 211

have about 4 million neurons per gram of brain mass, while chimps have about 16 million neurons per gram of brain mass, exceeding even humans, who have about 9 million neurons per gram of brain mass.

Taken at face value, the chimpanzee’s frugivorous, virtually 100 percent vegetarian diet,627 seems to support both more cerebral neurons per unit body mass, and more cerebral neurons per unit of brain mass, than either the seafood-based diet of the dolphins. This seems to rule out the idea that animal flesh in general, or seafood in particular, provides the best nutrition for unusual brain complexity.

The Favored Frugivores

If animal flesh provided the best fuel to support evolutionary expansion of a primate brain, one might expect to find a trend toward larger brains among the most insectivorous primates, since insects have a nutritional composition substantially similar to that of wild game or beef.628 However, among primates, the more insectivorous species do not have the larger EQs, and brain size appears related to the degree to which the species depends on carbohydrate-rich botanical fruits as food.629

The spider monkey and the howler monkey both diverged from a common ancestor, as did humans and chimps. These two monkey species inhabit the Barro Colorado forest and have similar body size (about 7 kg) and simple stomach structure. They both eat almost exclusively plant-based diets consisting of fruits and leaves.

The spider monkey has a small colon and long small intestine, similar to humans, whereas the howler has a large colon and short small intestine, similar to chimpanzees. Both howlers and chimps rely extensively on hindgut fermentation of fiber, while spider monkeys and humans rely primarily on enzymatic digestion in the small intestine. The spider monkeys’ diet consists on average of about 72 percent fruits and nuts, 22 percent leaves, and 6 percent flowers, while the howlers’ diet consists of about 42 percent fruit, 48 percent leaves, and 10 percent flowers.

The spider monkey has a brain weight almost twice that of howlers.630 A recent meta-analysis of studies of primate cognition came to the conclusion that the spider monkey performs better in tests of domain- general cognitive abilities than any other New World monkey, ranking just below chimpanzees and above gorillas in ability.631 This suggests a positive correlation between degree of frugivory, brain size,

627 See Appendix B.

628 van Huis A, Van Itterbeeck J, Klunder H, et al.. Edible insects: future prospects for food and feed security. FAO Forestry Paper 171. Food and Agriculture Organization of the United Nations, Rome, 2013. Chapter 6: Nutritional value of insects for human consumption. 67-76.

629 Milton K. Diet and Primate Evolution. Scientific American 1993 August: 86-93.

630 Ibid.

631 Deaner RO, van Schaik CP, Johnson V. Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology 2006; 4: 149-196.

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and cognitive capacities, and that among primates the pursuit of a diet based on carbohydrate-rich botanical fruits drives brain evolution.

Table 17.2: Selected primate guts, locomotion, brain/body ratios, and diets.

Species Small Coloni Locomotion Brain:body Natural Diet (% Fruit:Leaves: Intestinei (g) Other Plant Matter)

Howler Monkey1 54 29 Quadruped, 0.007 42:48:10 by feeding time1 arboreal

Chimpanzee2 23 52 Quadruped, 0.007 48:25:27 by feeding time3 arboreal

Spider Monkey1 62 18 Quadruped, 0.015 72-83:7-22:6-10 by feeding time1 arboreal

Human2 67 18 Biped, 0.024 Probably >72% botanical fruits or terrestrial similar sugar-rich foods (e.g. tubers)

i. Proportion as percentage of total gut. 1. Milton K. Food choice and digestive strategies of two sympatric primate species. The American Naturalist, April 1981; 117 (4): 496-505. 2. Milton K. Primate diets and gut morphology: Implications for Hominid Evolution. In Harris M (ed.), Food And Evolution: Toward a Theory of Human Food Habits, Temple University Press, 1989. 93-116. 3. The Chimpanzee Species Survival Plan. Caring For Chimpanzees. http://www.lpzoosites.org/chimp-ssp/ chimpanzees.htm

As shown in Table 17.2, the howler monkey and chimpanzee have similar brain/body mass ratios and dietary habits/proportions, and they both have a larger proportion of the gut devoted to the colon compared to spider monkeys and humans. Spider monkeys and humans have similar gut proportions, while the spider monkeys have a brain:body mass ratio twice that of howlers or chimps, and humans have a brain:body mass ratio more than three times that of chimps.

Both spider monkeys and howler monkeys are relatively small bodied (6-8 kg) compared to chimps and humans (40-70 kg). A howler monkey requires about 700 kcal daily, or about 100 kcal/kg, whereas a chimpanzee requires more like 3000 kcal daily, or about 50 kcal/kg. Small-bodied species expend more energy per kg body mass than larger species, so they must eat easily digested, energy dense foods; however, they don’t need to focus on abundant foods because their total energy requirements are relatively low. In contrast, large-bodied species have smaller energy requirements per unit weight, but higher total energy requirements, resulting in a need for abundant but not necessarily very easily digested foods. Consequently, large-bodied primates generally eat diets consisting of some mix of abundant leaves and easily-digested fruits. The largest primates, gorillas, focus on leaves and stems. Since the chimpanzee has a much larger body than the howler monkey, the former must devote more of its foraging to ingesting abundant leaves, and consequently must have a greater proportion of the gut devoted to the colon for hindgut fermentation.

BRAIN SIZE & METABOLISM – 213

As large-bodied primates, humans have a relatively low energy requirement per unit weight (kcal/kg) compared to spider monkeys. However, humans have a gut like the spider monkey, devoted primarily to processing carbohydrate- and energy-rich fruits rather than to fermentation of fiber. A part of the capacity of the human body to support a relatively larger brain:body ratio than either the spider monkey or the chimpanzee comes from the combination of an energy-efficient large body with a small-intestine- dominated gut and a diet based on relatively energy-rich fruits and similar plants.

Further, as discussed in Chapter 4, in their empirical refutation of the Expensive Tissue Hypothesis, Navarrete et al. indicate that the efficiency of human bipedal locomotion dramatically reduces the energy demands of movement thus allowing the system to invest in other energy-intensive organs, such as the brain.

“One likely trade-off could be found between brain size and the costs of locomotion. The efficient form of bipedal locomotion that arose with the transition from australopithecines to early Homo27 could have led to major reductions in energy expenditure in two ways. On one hand, its low costs in comparison with the climbing and quadrupedal locomotion of nonhuman apes28 should have lowered daily energy expenditure on locomotion7, and on the other hand, bipedalism may reduce the effect of increased weight due to adipose depots on the energy costs of locomotion (Supplementary Information 3.7).” 632

Sockol et al. report that “human walking is approximately 75% less costly than both quadrupedal and bipedal walking in chimpanzees.”633 Thus, bipedal locomotion also helps humans sustain a larger brain:body mass ratio than spider monkeys with only a minor increase in the proportion of the gut devoted to nutrient absorption (small intestine) and without further reduction of the colon. Further, as shown in Chapter 10, colonic fermentation of fiber can contribute sufficient energy to significantly offset human brain requirements.

This data suggests that the humans may have guts and brains adapted to a diet having a somewhat higher proportion of carbohydrate-rich botanical fruits (or similar foods) than the spider monkey, namely somewhat greater than 72 percent sweet fruits, starchy tubers, legumes, nuts (e.g. chestnuts), and seeds (grains). I provide an example of a diet providing 94 percent of its energy from botanical fruits in Table 17.6.

The Capuchin Catch

Some advocates of meat-based diets have noted that capuchin monkeys have the largest brain-to-body size ratio of any primate other than humans and also spend a lot of their time hunting for insects and very small game. However, capuchins range in body mass from 1.3 to 4.0 kg, about half the mass of a spider monkey and less than one-tenth the mass of a chimpanzee or human. As noted above, as a

632 Navarrete A, van Shaik CP, Isler K. Energetics and the evolution of human brain size. Nature 2011 Dec 1; 480: 91.

633 Sockol MD, Raichlen DA, Pontzer H. Chimpanzee locomotor energetics and the origin of human bipedalism. Proc Natl Acad Sci U S A. 2007 July 24; 104(30): 12265–12269.

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general rule, only very small-bodied primates specialize in faunivory because of the difficulty a large- bodied primate has in meeting total energy requirements using animal matter.634 Moreover, capuchins eat a largely frugivorous diet supplemented with insects.

Also, many small-bodied animals have large brain:body mass ratios. For example, the primarily herbivorous mice and squirrels also have a brain:body mass ratio similar to humans, and small birds actually have a larger brain:body mass ratio than humans or capuchins.635 In short, since the capuchin has a small body, we therefore expect it to have a large brain:body mass ratio, and can’t attribute its relatively large brain:body mass ratio exclusively to consumption of animal matter.

Flesh Does Not Provide Ready Brain Fuel

The human brain requires glucose for fuel, and uses 25 percent of total body glucose utilization. Animal flesh provides almost no glucose, and consists primarily of protein and fat. Only about 50 percent of amino acids composing animal proteins convert readily to glucose, the rest getting metabolized as ketoacids. Thus, animal flesh does not provide the most readily available brain fuel.

Among terrestrial species, those specializing in eating flesh (protein and fat) have relatively small brains (Table 17.1) compared to highly or extremely frugivorous species. It seems clear that among terrestrial species, only those that have specialized in eating carbohydrate-rich botanical fruits have exceptionally large brains.

As noted in Chapter 3, some scientists have suggested that the ability to taste and enjoy the sweet flavor provided by sugars played a significant role in guiding primates toward frugivory and ingestion of the sugar required to support brain metabolism.636

Neural Fatty Acids

Some people have advanced the hypothesis that human ancestors had to consume flesh (brains, marrow, fish, or eggs) to get enough omega-3 fatty acids to build the new neural cell membranes required for brain expansion.

I find it somewhat surprising that this hypothesis gets much traction since we have abundant evidence that modern humans can produce children with structurally and functionally healthy brains with little or no animal flesh intake. For example, natives of Papua New Guinea consume a diet consisting of more

634 Fleagle JG. Primate Adaptation and Evolution. Academic Press, 1998. 286.

635 Kinser PA. Thinking about Brain Size. http://serendip.brynmawr.edu/bb/kinser/Int3.html

636 Nofre C, Tinti JM, and D. Glaser D. Evolution of the Sweetness Receptor in Primates. II. Gustatory Responses of Non- human Primates to Nine Compounds Known to be Sweet in Man. Chem. Senses 1996;21:747-762.

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than 90 percent sweet potatoes, with a meat intake described as “negligible” and only 6 total grams of daily dietary fat,637 yet they produce children with healthy brains.

This supports the conclusion that humans do not now and probably never have required the intake of animal brain tissue, marrow, eggs, or fish to support development of the infant brain or maintenance of the adult brain.

From an evolutionary perspective, if humans required consumption of animal flesh to support full brain development, this would make the star biological achievement of our species quite fragile. Had the hunters failed to bring home the bison with adequate regularity, numerous children would have grown up half-witted. In fact, we have biochemical evidence that human ancestors never depended upon dietary flesh as a source of structural fatty acids for neurons.

Proponents of the hypothesis that humans must eat flesh in order to build or maintain brain tissue focus their attention on the role of docosahexaenoic acid (DHA), an omega-3 fatty acid, in brain structure. This fatty acid does not occur in land plants and proponents of the meat hypothesis argue that humans do not convert the omega-3 fatty acid found in plants, alpha-linoleic acid (αLNA ) with an efficiency sufficient to support human brain health.

The evidence that humans have weak ability to convert αLNA to DHA comes entirely from studies of men who probably have preformed DHA in their diets. Studies have shown that dietary DHA suppresses conversion of αLNA to DHA, and absence of dietary DHA stimulates it, particularly in women.638 Apparently natural selection favored the survival of humans, particularly women, who would convert αLNA to DHA when the diet did not contain the latter. This would have only occurred if the ancestral diet usually lacked DHA, giving the reproductive advantage to those who could produce DHA from αLNA.

Evidently the body regulates DHA production by negative feedback. The fact that natural selection favored reproduction of humans having a system for tight regulation of DHA production suggests that accumulation of excess DHA has negative effects on reproduction. Both EPA (eicosapentaenoic acid) and DHA suppress cell-mediated immune responses of both innate and adaptive immunity,639 and below I will discuss evidence that dietary DHA may impair embryo development. Intake of preformed DHA circumvents this evolved regulatory process, and may lead to toxic levels of DHA causing immune suppression and defects of embryos.

637 Sinnett P, Whyte M. Papua New Guinea. In: Western Diseases: Their emergence and prevention. Ed. by H. Hubert Carey Trowell and Dennis Parsons Burkitt. Harvard University Press, 1981. 174.

638 Burdge GC, Calder PC. Dietary α-linolenic acid and health-related outcomes: a metabolic perspective. Nutrition Research Reviews (2006); 19: 26–52.

639 Shaikh SR, Edidin M. Polyunsaturated fatty acids, membrane organization, T cells, and antigen presentation. Am J Clin Nutr 2006 Dec; 84(6): 1277-1289.

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Further, studies of αLNA (a.k.a. αΑLNA) metabolism in men have little relevance to the question of whether a diet lacking DHA can support brain development in humans, since a developing child depends on mother for neural nutrients during gestation and lactation. Studies of women have found that they perform the conversion much more efficiently than men:

“Two reports have specifically studied αΑLNA conversion in women of reproductive age. Burdge and Wootton (2002) showed that conversion of αΑLNA to EPA and DHA in women aged about 28 years was substantially greater (2·5-fold and >200-fold, respectively) than in a comparable study of men of similar age (Burdge et al. 2002) (Table 5). This finding is strongly supported by kinetic analysis, which showed that the rate-constant coefficient for the conversion of DPA to DHA was approximately 4-fold greater in women compared with men (Pawlosky et al. 2003a) (Table 5).”640

Research has strongly supported the conclusion that estrogen stimulates the conversion of αLNA to DHA, and testosterone suppresses it.641 These sex differences in metabolism of αLNA probably resulted from natural selection to ensure that any human fetus has an adequate supply of DHA when the diet supplies only αLNA, i.e. in the absence of animal flesh.

“In this context, the capacity to increase maternal DHA synthesis by the action of oestrogen may be of particular importance in ensuring a supply of DHA to the fetus. Speculatively, this ability may have evolved to protect the developing fetal brain from a deficit in DHA accumulation, a risk which would be substantially greater if supply of DHA from the maternal diet was the sole source of DHA for supply to the fetus.”642

Thus, female physiology ensures that most of the DHA supplied to a fetus comes from stores in her adipose tissue, so that the infant does not depend primarily on either dietary DHA or immediate but slow conversion of dietary αLNA. A woman stores DHA in her adipose continuously from puberty until menopause, and especially during the third trimester of pregnancy, when she will store ten times more DHA in her adipose than the fetus incorporates into its brain:

“Furthermore, accumulation of DHA into adipose tissue during the third trimester is about 10- fold greater (380 mg/week) than into the fetal brain (35 mg/week) (Clandinin et al. 1981). This suggests that one of the reasons why man (Poissonnet et al. 1984), unlike other primates (Adolph and Heggeness, 1971; Lewis et al. 1983), has evolved the capacity to accumulate adipose stores in late gestation may be to provide a nutritional buffer during the transition from placental to oral supply (Kuzawa, 1998; Correia et al. 2004), thus preventing a deficit in DHA. This store is likely to depend upon supply of preformed DHA from the mother.”643

640 Burdge and Calder. op. cit. Nutrition Research Reviews (2006); 19: 26–52.

641 Ibid.

642 Ibid.

643 Ibid.

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Further, most of the DHA in the milk of women who eat animal products comes from maternal fat stores, not diet:

“Studies using isotope-labeled fatty acids show that 60–80% of LCPUFAs in human breast milk come from maternal fat stores, rather than from the mother's current dietary intake (Del Prado et al., 2000; Demmelmair et al., 1998; Fidler et al., 2000; Hachey et al., 1987), presumably because of the rapid rate of infant brain development relative to limited dietary supplies of LCPUFAs.”644

The fact that modern women have the ability to slowly convert αLNA to DHA and store it up over a long period of time in preparation for a pregnancy suggests strongly that the bulk of human ancestors had limited or no dietary supplies of DHA, making such equipment necessary to support infant brain development.

Women naturally store DHA in the adipose tissue on their buttocks and thighs, and women with a low waist-to-hip ratio (WHR), i.e. hips larger diameter than waist, tend to have higher blood levels of DHA .

“Gluteofemoral fat is richer than abdominal and visceral fat in essential LCPUFAs, and a lower WHR is associated with higher DHA levels in the blood.”645

It thus seems that the universally admired hour-glass figure may serve as a signal that the woman possessing it has the ability to properly nourish the growth of a human child both in utero and through lactation.

In addition, infants can synthesize DHA from αLNA provided that the diet does not contain large amounts of linoleic acid or DHA:

“Studies using stable isotope tracers have detected the conversion to DHA of precursors supplied in formula to preterm infants with a gestational age of 27-35 weeks at the time of the study...The synthesis of DHA occurs within the placenta, fetal liver, and fetal brain...and its rate increases with fetal age...The absolute rate of synthesis by fetuses and newborns has not been calculated and appears to vary substantially...It is known to be inhibited by excessive quantities of linoleic acid...That rate may also be sensitive to the intake of preformed DHA: synthesis was elevated in infant baboons fed a formula lacking in DHA...and in rats with a fat-free diet.646

During development, the infant’s brain does not depend on dietary DHA because buffering mechanisms (borrowing DHA from non-neural tissues, primarily adipose), de novo synthesis, and long term

644 Lassek WD, Gaulin SJC. Waist-hip ratio and cognitive ability: is gluteofemoral fat a privileged store of neurodevelopmental resources? Evolution and Human Behavior (2008) 29: 26–34.

645 Ibid.

646 Langdon JH. Has an aquatic diet been necessary for hominin brain evolution and functional development? Brit J Nutr 2006;96:7-17.

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accumulations give the infant’s brain a continuously adequate supply of DHA under most circumstances.647 In the event of a temporary shortage of dietary omega-3 fats leading to low levels of DHA in neural tissues, the body builds the brain with alternative fats (docosapentaenoic acid or arachidonic acid), and, once supplied with αLNA, catch-up synthesis and accumulation of DHA in neurons “appears to be normal and is probably due in part to the increasing ability of the infant to synthesize DHA from other n-3 fatty acids.”648

Experiments in animal models probably provide information sufficient to explain the low rate at which human males convert αLNA to DHA.

“Furthermore, experiments in animal models suggest that recycling of DHA in cell membranes of the brain and the retina is highly efficient (Wiegand et al. 1991; Chang et al.. 1999). In rats, 97% of DHA in the brain is derived from the recycling of DHA from membrane sources (Chang et al. 1999). If this is also found in human adults, this suggests that the actual daily requirements for DHA to replenish neural membranes may be very small, and so could be provided by relatively low dietary intakes.“ 649, 650

Furthermore, a study of vegan men found that they have stable (not declining) tissue levels of DHA despite ingesting no preformed dietary DHA, presumably due to continuous, sufficient endogenous synthesis from αLNA.651 We have no evidence that people eating plant-based diets suffer from any neurological impairments due to DHA deficiency. Millions of individuals around the world, including adherents of several religious doctrines that emphasize abstention from animal consumption (Jainism, Buddhism, Taoism), which form a significant proportion of modern populations, produce children with normal brains.

“In the case of these vegetarians, many have maintained such a restricted diet for generations. Neurological impairment under generational deficiency of DHA should result if dietary DHA is essential for neural function. Given that these populations experience normal brain growth and development in the absence of dietary DHA, it seems reasonable to question the nature of our dietary requirement for n-3 fatty acids. If preformed DHA is essential...the expected outcome of a vegetarian lifestyle is the failure of neural growth and development. On the other hand, there is no evidence to suggest that the capacity for DHA synthesis in vegetarians is limited...A logical

647 Ibid.

648 Ibid.

649 Burdge and Calder, op cit.

650 Langdon JH, op. cit.

651 Roselll MS, Lloyd-Wright Z, Appleby PN, et al.. Long-chain n-3 polyunsaturated fatty acids in plasma in British meat- eating, vegetarian, and vegan men. Am J Clin Nutr 2005 Aug; 82(2):327-334.

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explanation involves the sufficiency of LNA from the dietary intake of plants to provide sufficient DHA for the neural development of these populations.”652

Currently, the bulk of evidence indicates that adult humans do not have a dietary DHA requirement, and that ongoing slow conversion of αLNA to DHA coupled with traditional breast-feeding of infants meets all requirements at all stages of life, including pregnancy and lactation.653 Humans have a dietary requirement for only one omega-3 fatty acid, αLNA, amply provided by plants.654 The claim that human brain evolution required dietary DHA because biosynthesis of DHA from αLNA does not meet requirements for brain growth and maturation lacks evidential support, whereas we have much evidence suggesting that consumption of αLNA, widely available within a number of terrestrial ecosystems, provides adequate nutrition for normal brain development and maintenance in modern humans and presumably our ancestors.655

As already mentioned, the highlands people of Papua New Guinea exhibit complete neurological development eating a diet supplying only 6 grams of fat daily, almost all of that from sweet potatoes and a “negligible” intake of animal products. Twenty medium sweet potatoes supply 2052 kcal, with a mere 1.4 percent of that provided by fats, including a mere 0.09 g of αLNA.656 Apparently humans can achieve full neurological development on a diet providing less than one gram of αLNA daily, without regularly ingesting preformed DHA.

These facts indicate that natural selection did not favor the survival of humans dependent upon dietary DHA to support brain development of offspring or brain maintenance of adults. On the contrary, it appears that natural selection favored the reproduction of women who would, due to the influence of estrogen, continuously convert αLNA into DHA and store this lipid in their hip and thigh fat over the course of years, so that they would always have a sure supply of DHA for any children that they mothered. As for men, they don’t convert αLNA to DHA very efficiently probably because they don’t have a very high requirement for endogenously produced DHA for maintenance of their neural tissues due to highly efficient (97%) recycling of DHA.

“Overall, the capacity of modern man to convert αLNA to longer-chain PUFA, in particular DHA, appears to be consistent with our evolutionary past and the [putative] fatty acid content of our ancestral diet. This is reflected in differences in the efficiency of conversion of αLNA to DHA between men and women. In women, capacity to up regulate may be important for protecting the development of the fetal brain against deficit in DHA accumulation during

652 Carlson BA and Kingston JD. Docosahexaenoic Acid, the Aquatic Diet, and Hominin Encephalization: Difficulties in Establishing Evolutionary Links. Am J Hum Biol 2007;19:132-141.

653 Food and Nutrition Board, Dietary Reference Intakes for Energy, etc. National Academies Press, 2005. 434-5

654 Ibid., 423.

655 Carlson BA and Kingston JD, op. cit.

656 USDA data. www.cronometer.com

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pregnancy. The contrastingly low level of DHA synthesis in men may reflect the activity of recycling mechanisms that may limit the demands of neural tissue for DHA.”657

Dietary DHA Potentially Harmful to Embryos

As mentioned above, the body tightly regulates DHA production to prevent an accumulation of excess. Apparently, this serves a purpose. Of concern, a diet high in preformed DHA may have adverse effects on a developing embryo. The long chain omega-3 polyunsaturated fatty acids have a high propensity to react with oxygen to generate reactive oxygen species (ROS) which could poison and damage an embryo. In a murine study, Wakefield et al. found that mares supplemented with DHA (and EPA) produced embryos with significant developmental impairments when compared to unsupplemented mares. The mares enriched with DHA and EPA produced more poor-quality zygotes, and their zygotes had significantly reduced ability to properly cleave to form a two-celled embryo. The supplemented mares also had more than 4 times as many embryos arrested at some stage of development. The authors concluded “the exposure of oocytes to a high n-3 PUFA environment during in vivo fertilization adversely affected zygote morphology and delayed embryo development.”658

Plants Provide The Only Required Omega-3 Fat

In short, human metabolism of DHA supports the conclusion that human evolution proceeded on a diet wherein small amounts of plant-sourced αLNA probably provided the stable source of omega-3 fatty acids required for brain growth. As noted by primatologist Katherine Milton:

“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, Brussels sprouts, parsley). But most Americans do not consume large quantities of these plant foods either fresh or cooked; cooking of these foods also tends to destroy ALA. The diet of human ancestors (like the diets of extant monkeys and apes) was likely rich in both linoleic acid and ALA from fresh plant tissues and for this reason the fatty acid composition of such plant foods is likely to be most compatible with human biology.”659

A plant-based diet supplies the glucose (from botanical fruits) and the essential fatty acids (from green leaves, legumes, nuts, and seeds) nutritionally required to support growth and development of the neural system providing the physiological basis for cognitive abilities.

657 Burdge and Calder, op cit.

658 Wakefield SL, Lane M, Shulz SJ, et al.. Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am J Physiol Endocrinol Metab 2008; 294:E425-E434.

659 Milton K. Nutritional Characteristics of Wild Primate Foods. Nutrition 1999; 15:488-498.

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Brain-Specific Minerals

Some authors have argued that the human requirement for specific “brain-selective” minerals –namely iron, copper, zinc, selenium, and particularly iodine –suggests that early humans inhabited coastlines and depended upon sea animals as sources of those minerals.660 Verhaegen et al. argue thus:

“Of all the major food groups, shellfish requires the least amount (900 grams) to meet the minimum requirement for all five minerals, and is also the food group for which these requirements are most evenly distributed. Eggs (2500 grams) and fish (3500 grams), both more abundant at the waterside than in terrestrial environments, are next, while 5000 grams of meat, five times more than shellfish, would be needed to meet the minimum requirement for all five minerals (Table 5).”661

In support of their claim, they provide their Table 5, which I reproduce here (Table 17.3):

Table 17.3: Reproduction of Verhaegen et al.’s Table 5, entitled “Daily amount of major food groups (in kilograms), arranged from low to high, minimally required for five brain-selective minerals: Iodine, iron, copper, zinc, and selenium (I, Fe, Cu, Zn, and Se) after Cunnane (2005).”

I Fe Cu Zn Se

shellfish 0.7 0.8 0.9 0.5 0.3

eggs 0.2 0.6 2.5 0.9 0.9

fish 0.2 3.5 3.1 2.7 0.7

pulses 3.7 0.4 0.3 0.5 3.0

cereals 3.2 3.1 4.8 1.9 2.2

meat 1.5 0.8 1.7 0.9 5.0

nuts 1.5 0.8 0.9 0.5 5.5

vegetables 4.2 2.1 2.7 8.7 6.7

fruit 6.0 3.7 4.8 9.3 6.0

milk 6.7 24.0 12.5 47.0 5.5

The figure in italic is the most limiting factor in each food group.

From: Verhaegen M, Munro S, Vaeechoutte M, et al.. The Original Econiche of the Genus Homo: Open Plain or Waterside? In: Ecology Research Progress, ed by Sebastian I Munoz. Chapter 6. Nova Science Publishers, Inc, 2007.

660 Verhaegen M, Munro S, Vaeechoutte M, et al.. The Original Econiche of the Genus Homo: Open Plain or Waterside? In: Ecology Research Progress, ed by Sebastian I Munoz. Chapter 6. Nova Science Publishers, Inc, 2007.

661 Ibid.

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Verhaegen et al. failed to provide any description of the method by which either they or Cunnane produced this table. I find it questionable, for several reasons.

First, the results presented in this table depend tremendously on what foods you choose to analyze for each group, but they failed to provide that information. As a glaring example to me, they claim that one would have to consume 5.5 kg of nuts to satisfy one’s selenium requirement. I would guess that they did not include brazil nuts in their analysis. Since one brazil nut, a mere 5 grams, provides 96 mcg of selenium, 1.3 times the human daily requirement, if they had included this nut in their analysis, they would not have come to the conclusion that one needs to eat 5.5 kg of nuts to meet the selenium requirement. For example, the mean selenium content of almonds, walnuts, brazil nuts, cashews, and pecans in equal portions equals 390 mcg/100 g, and using this mythical mean selenium concentration found in no actual nut, one need only consume about 18 g of nuts to meet the selenium requirement, not 5.5 kg.

Secondly, Verhaegen et al. failed to identify which vegetables served as the basis for the calculations for that food group. Primates (including humans) feed very selectively on vegetables. Milton has commented upon this:

“....primates typically have larger brains than do other mammals of their size. I believe the difference arose because primates feed very selectively, favoring the highest-quality plant parts––for instance, even primates that eat leaves tend to choose very immature leaves or only the low-fiber tips of those leaves.”662

The large-brained and highly frugivorous primates emphasize consumption of tender green leaves over other types of vegetables. For example, as already mentioned (Table 17.2), about 25 and up to 22 percent of diet of chimpanzees and the large-brained spider monkey, respectively, consists of green leaves. Green leaves have extraordinarily high mineral contents compared to other vegetables. In their table, Verhaegen et al. (and Cunnane) claim that one must consume 8.7 kg of “vegetables” to acquire the daily requirement for zinc. In contrast, just 3 kg of raw mesclun mix or kale provides the daily requirement for zinc (USDA data).

Table 17.4 depicts the actual mineral intakes of wild howler monkeys (body mass, 7 kg), derived primarily from wild leaves and fruits, in comparison to the modern RDA for adult humans. A howler acquires minerals in these quantities from wild foods providing about 700 kcalories daily.

As shown, a howler consumes 39 mg iron and 3 mg copper in the course of obtaining its daily 700 kcal. Howlers have a diet consisting of about 42 percent fruits and 58 percent leaves and other plant foods (Table 17.2); assuming this distributes their energy intake, they get 294 kcal from fruits and 406 kcal from vegetables.

662 Milton K. Diet and Primate Evolution. Scientific American 1993 August: 86-93. 90.

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Table 17.4: Estimated mineral intakes of wild monkeys compared to the human RDA.

Mineral Total daily intake–7 kg adult RDA, 70 kg adult male (mg) monkey (mg)

Calcium 4571 800

Phosphorus 728 800

Potassium 6419 2000

Sodium 182 500

Chloride 1778 750

Magnesium 1323 350

Iron 39 10

Manganese 18 5

Copper 3 3

Source: Milton K. Nutritional Characteristics of Wild Primate Foods. Nutrition 1995;15(6): 488-98. 493.

Among cultivated leafy vegetables, the most tender (spinach and lettuce) provide about 0.2 kcal/g, and tougher varieties like kale and collards supply about 0.5 kcal/g. The tenderest of wild leaves resemble the toughest of cultivated leaves. Wild fruits may have an average energy density similar to cultivars, i.e. about 1.0 kcal/g (Table 17.5).

Assuming that their fruits provide a conservative average of 0.8 kcal/g and their vegetables a very conservative average of 0.4 kcal/g (a little less than kale), howler monkeys consume 0.4 kg of fruits and 1.0 kg of vegetables to obtain these nutrients. Thus, their food has average iron and copper concentrations of 28 mg/kg and 2.1 mg/kg, respectively.

A modern human eating these wild foods would require less than 1 kg of this food to obtain her required iron (18 mg) and 1.5 kg to obtain her required copper (3 mg). Brand-Miller and Holt report that edible leaves and plants available to Australian Aborigines supply 5 mg and 15 mg iron/100 g, respectively (they supply no data on copper); so just 350 g of those leaves, or 120 g of the mix of plant foods, would supply the daily requirement of iron.663 Yet Cunnane (Table 17.3) implies that a protohuman would require 2 to 4 kg and 3 to 5 kg of fruits and vegetables to get the human requirements for, respectively, iron and copper.

663 Brand-Miller and Holt, Australian Aboriginal plant foods, Nutr Res Rev 1998;11:5-23. Tables 2 and 3.

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Table 17.5: Energy density of wild African and cultivated fruits

Wild Fruit Kcal/g Cultivars Kcal/g

Wild plum 0.8 Apple 0.6

Morula fruit 0.3 Apricots 0.5

Wild apricot 1.4 Banana 0.9

Monkey orange 1.0 Orange 0.5

Amatungulu 0.8 Grape 0.7

Baobab1 3.4 Dates, medjool 2.8

Sour plum 1.3 Mango 0.7

Kei-apple 0.2 Pineapple 0.5

Red gherkin 0.6 Durian 1.5

Average 1.0 Average 1.0

1. Wild baobab has a very low moisture content (7.0%) Sources: Wild fruits: Wehmeyer AS. The nutrient composition of some edible wild fruits found in the Transvaal. South African Med J 1966 Dec 17: 1102-04. Table 1. Energy density calculated from macronutrient data. Cultivated fruits: USDA

From this I conclude that Cunnane did not use the known nutrient contents of wild fruits and vegetables to calculate his table. If one wishes to make claims about the food requirements of wild protohuman primates, one should use data on the nutrient contents of wild foods they may have consumed, if it is available. Use of data from cultivated foods that are known to differ markedly from wild foods can give very misleading results.

A protohuman of 50 kg would require at least double the energy intake of a howler (i.e. 1400 kcal) which would require consumption of twice the amount of fruits and vegetables (i.e. at least 3.0 kg) and with them, she would ingest at least twice the amounts of minerals consumed by the howler. My calculations indicate that the howler diet of fruits and vegetables may have an iron concentration that Cunnane (Table 17.3) claims occurs only in eggs and shellfish. Regarding copper, Cunnane’s table shows legumes having the highest concentration. I see no reason to believe that any protohuman would have to eat anything other than wild vegetables and botanical fruits (including legumes) to obtain adequate iron or copper.

Thirdly, although Verhaegen et al. and Cunnane argue that a seaside habitat would best support human encephalization, their table conspicuously lacks any information about edible sea vegetation, such as kelp (Laminaria sp.), alaria (Alaria sp.), nori/laver (Porphyra sp.), or dulse (Palmaria sp.), all plant foods

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very rich in minerals, particularly iodine. According to Verhaegen et al.’s chart, 0.7 kg (700 g) of shellfish supplies the daily requirement for iodine. According to Maine Coast Sea Vegetables, a mere 14 g of dried laver (Porphyra umbilicalis) provides 196 mcg of iodine, and one need consume only about one gram of alaria, dulse, or kelp to meet the daily iodine requirement.664 Since humans world wide consume sea vegetation to this day, Verhaegen et al. need to include these foods in their seaside scenario.

If one wishes to provide evidence that any protohuman primate would require any type of sea food (vegetable or animal) to acquire adequate iodide, one must also provide evidence that the land plants consumed by extant primates or ancient hominins could not provide adequate iodide.

Non-human primates require approximately 0.35 mg iodine per kg of food (dry weight), which does not differ much from the 0.3 mg/kg food (dry weight) required by humans.665 Apparently, extant wild chimpanzees, gorillas, and orangutans, all closely related to humans, obtain adequate iodine from their terrestrial plant-based diets without resorting to consumption of any type of sea food. This implies that their habitats supply adequate iodine, cycling from soil into animals and back to the soil (via urine, feces, and decaying carcasses). Also, ocean winds carry iodine-bearing moisture inland,666 allowing iodine to enter the terrestrial food chain in the form of plants that grow on soils located near but not at the shore. Migrating herbivores may transport some of this iodine further inland and deposit it in soils via urine, feces, and carcasses.

Consequently, we lack evidence that protohumans inhabiting African woodlands similar to modern primate habitats had a dietary requirement for marine foods as a source iodine.

This underscores a general point: Since modern humans do not live in the ancestral habitat, and consume artificially cultivated foods grown in soils and locations very different from those of the ancestral habitat, and may find excuses (flavor, cost, convenience) to avoid eating the foods that we require to meet our nutrient requirements (e.g. dark green vegetables), the foods we consume may lack the nutritional value of the foods consumed by our ancestors. Consequently, in modern circumstances, we may need to take specific steps, such as careful diet planning or specific nutrient fortification or supplementation, to obtain adequate intakes of specific minerals.

However, the fact that we may need to take deliberate steps to meet our needs for specific nutrients – such as eating sea vegetables or iodine-fortified salt, or taking an iodine supplement – does not imply that our protohuman ancestors (eating very different foods) had the same need to (deliberately) find specific sources of this same nutrient. Nor does our need to carefully plan or supplement any specific type of diet consisting primarily of cultivars (e.g. plant-based) imply that our ancestors, who ate more nutrient-dense wild foods, required some other type of diet (e.g. marine animal flesh based).

664 Maine Coast Sea Vegetables. Nutritional Charts. http://www.seaveg.com/shop/index.php? main_page=pageandid=15andchapter=5

665 Committee on Animal Nutrition, National Research Council of the National Academies. Nutrient Requirements of Nonhuman Primates, Second Revised Edition. National Academies Press, 2003. 192-193.

666 Ibid. 104.

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Fourthly, Verhaegen et al. present this data as if suggesting that protohumans strove to meet all their mineral requirements from the smallest possible quantity of one type of food. Do Verhaegen et al. want us to believe that protohumans consciously sought out the foods which would provide them with their mineral requirements with the least food volume, regardless of how much of the food they would have to consume to meet energy requirements? Actually, all organisms eat primarily to satisfy hunger and energy requirements, not to minimize food volume. In fact, most organisms seek to maximize food volume and will eat as much as possible whenever possible.

An organism usually does not need to find the most concentrated source of any nutrient(s) it requires, it needs to meet its various nutrient needs as a result of satisfying its energy requirements with whatever variety of foods it finds attractive. For this reason, any analysis of the micronutrient delivery of foods should report the results relative to energy (kcalorie) content, not weight, because our interest is whether or not the individual will satisfy his micronutrient needs while satisfying his total energy needs. For example, using again the five nuts mentioned above, on average, they supply 0.62 mcg selenium per kcalorie. A lactating woman requiring 70 mcg selenium per day would need to eat only 113 kcalories of the mythical “average nut” to meet her selenium requirement.

Primates do not need to rely on any one food group for any of these minerals. Many foods contain small amounts of each mineral, and in the course of eating whole foods to meet energy requirements and satisfy hunger, one can meet mineral requirements without focussing on consuming only the richest sources of those minerals.

In fact, an attempt to eat only the richest sources of the “brain-selective” minerals can lead to serious, even life-threatening nutritional imbalances. Via Table 17.3, Verhaegen et al. claim that 0.9 kg of unspecified shellfish will meet all the “brain-specific” mineral needs. They don’t mention that 900 g of clams (mixed species) provides 603 mg of cholesterol and 230 g of animal protein, levels harmful to human health.

As already discussed (Chapter 16), humans do not require nor tolerate dietary cholesterol intake without adverse cardiovascular effects, and the 603 mg provided by 900 g of clams would raise serum cholesterol levels (absent any interfering factor such as parasite infection), which may promote infertility (Chapter 11), and certainly promotes cardiovascular disease (Chapter 16).

As already discussed, humans have a metabolism adapted to a daily protein intake of about 50 g. Sixty- nine percent of the energy (kcalories) provided by clams consists of protein, and 900 g of clam meat provides 230 g of animal protein, about 4 to 5 times the human daily requirement. Metabolism of the excess protein would increase blood ammonia to levels that tax the human liver’s ammonia detoxification ability and probably lead to somewhat toxic blood levels of amino acids and ammonium,667 which as I have already discussed, have deleterious effects on fetal health and

667 Rudman D, DiFulco TJ, Galambos JT, et al.. Maximal Rates of Excretion and Synthesis of Urea in Normal and Cirrhotic Subjects. J Clin Invest 1973 September; 52(9):2241-2249. PMC333026

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development (Chapter 11). Meanwhile the clam diet provides a mere 1332 kcal, about half the requirements of a physically active 25 year old woman (particularly if pregnant) and less than half of the amount required by a physically active male.

This shows that an individual hyper-focused on eating the food group supplying the highest concentration of specific minerals would poison him/her self with excesses of other nutrients before ingesting adequate total energy.

Table 17.6 outlines a diet which supplies more than 100 percent of the presently recommended levels of the so-called brain-selective minerals without inclusion of any shellfish or other animal tissues, or even the very unusually selenium-rich brazil nut. This demonstrates that a plant-based diet with sufficient variety can supply adequate amounts of these micronutrients.

Table 17.6: So-called brain-selective minerals supplied by a 3061 kcal plant-based diet composed primarily of botanical fruits.

Food Measure Cu (mg) I (mcg) Fe (mg) Se (mcg) Zn (mg)

Oranges 4 (2-7/8” dia) 0.2 – 0.7 0.0 0.4

Bananas 6 med (7-8”) 0.6 – 1.8 7.1 1.1

Tomatoes 4 (2-3/5” dia) 0.3 – 1.3 0.0 0.8

Avocados 1 fruit 0.2 – 0.8 0.5 0.9

Lettuce, romaine Half head 0.2 – 3.0 1.3 0.7

Pumpkin seeds 2 ounces 0.8 – 5.0 5.3 4.4

Peas, green, raw 2 cup 0.5 – 4.3 5.2 3.6

Kale, raw 4 cups 4.0 – 3.9 2.4 1.5

Spaghetti, whole 8 ounces, before 1.0 – 8.3 166.4 5.4 wheat, dry cooking

Laver, dried 15 g 0.3 186.0 1.8 0.0 1.0

Total 8.1 186 30.9 188.2 19.8

RDI or EAI 2.0 150.0 18.0 70.0 15.0

% RDI or EAI 400.0 124.0 388.0 342.0 181.0

Sources: Cronometer.com/USDA data, except for laver data from Maine Coast Sea Vegetables.

Whatever human ancestors ate, they acquired all of the minerals they required (or we wouldn’t be here). Clearly, a diet of modern plant foods can supply more than adequate amounts of all of the minerals required for brain development and health, and wild plants have much higher mineral contents and do

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meet the requirements of extant hominoid apes. This supports the conclusion that our ancestors also could have obtained all the minerals they required from an adequate variety of plant foods.

In summary, I see no reason to believe that hominins had to habitually consume any foods other than fruits, vegetables, legumes, nuts, and seeds to obtain sufficient nutrition to support purported gradual evolutionary increases in brain size and complexity occurring over millennia. In short:

“The hypothesis of an evolutionary dependency of the human brain on aquatic or marine resources or on any other single food source is unnecessary and unsupported.”668

Factors Correlating With Primate Encephalization

According to Lefebvre,669 26 large-scale comparative studies provide robust evidence for the following five lifestyle correlates of increased brain or neocortex size relative to body size, lower brain size, and/or evolutionary time:

• Strong reliance on vision • Group living • A large home range • “High quality” diet • Arboreal and forest dwelling

As discussed in Chapter 3, humans rely heavily on vision; we also live in complex social groups, so these probably played important roles in human encephalization.

Regarding home range, Amato et al. studied the foraging behavior of howler and spider monkeys, and found that the heavily folivorous howler monkey spends much less time moving than the frugivorous spider monkey, largely due to the fact that leaves are far more abundant than fruits.670 They also found that in foraging the spider monkey (5-9 kg) traveled a similar distance to the much smaller squirrel monkey (0.5-1 kg), which eats fruits and insects.

In short, a large bodied, highly frugivorous primate must have a large home range in order to obtain sufficient food resources. As a consequence, extreme frugivory strongly favors locomotive efficiency. As mentioned earlier in this chapter and discussed in Chapter 4 (Locomotion), human bipedalism uses about 75 percent less energy than quadrupedalism, and emerged among forest-dwelling, frugivorous

668 Langdon JH. Has an aquatic diet been necessary for hominin brain evolution and functional development? Brit J Nutr 2006;96:7-17.

669 Lefebvre L. Primate encephalization. In: Progress in Brain Research, Vol. 195: Evolution of the Primate Brain: From Neuron to Behavior. Ed. by Michel A Hofman and Dean Falk. Amsterdam, Elsevier, 2012. 393-412.

670 Amato KR, Onen DD, Emel SL, May CH. Comparison of Foraging Behavior Between Howler Monkeys, Spider Monkeys, and Squirrel Monkeys. Dartmouth Undergraduate Journal of Science 2006 Fall: 28-31.

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hominins. This suggests that pursuit of a extremely frugivorous diet requiring a very large home range may have favored bipedalism in the human lineage.

Of interest, according to Fleagle671, spider monkeys can walk bipedal along tree branches, and Thorpe et al.672 have argued that human bipedalism evolved from hand-assisted bipedalism of a common ancestor of humans and the moderately to heavily frugivorous orangutan.

As for “high quality” diet, I have provided evidence that a plant-based diet can provide all the energy (Chapter 1), fatty acids, and minerals required to support human encephalization. So, do we have any reason or evidence to support the hypothesis that a plant-based diet could have played important roles in the unusual degree of human encephalization?

Plant-based Intelligence

It seems that many people assume that plant-eating animals have no particular need for cognitive power. However, frugivorous primates have relatively large brains (particularly compared to carnivores), and, as already discussed in Chapter 5 above, due to the large amount of brain tissue devoted to sensory and motor functions of the human hand, we can safely conclude that natural selection would favor increases in brain size and complexity in any animal that specializes in eating foods that place demands on manual sensitivity and dexterity in collection and processing, such as: very ripe fruits, particularly berries; small tender seeds, particularly those found in pods, such as fresh peas and beans; fruits that requiring peeling or seeding; and energy-rich oil seeds borne by fruits, such as sunflower seeds and pumpkin seeds.

Further, successful pursuit of a plant-based, highly frugivorous lifestyle in a wild ecosystem involves gathering and processing a large amount of information on flowering plants that produce botanical fruits or vegetables, such as:

• Cataloguing in memory all of the available edible plants in the home range. • Linking flowers with fruits to provide foreknowledge of ripe fruits. • Knowledge of place and time the flowering and fruiting will take place. • Knowledge of how to get to the exact place within a large range where one can find ripe fruit at any point in time. • Knowledge of specific details that distinguish between ripe and unripe fruits and vegetables. • Knowledge of specific details that distinguish between safely edible fruits and vegetables, and poisonous look-alikes. • Knowledge of which parts of a fruit, vegetable, or plant are safely edible, and which are not, and of the most efficient ways to process (peel, pit, etc.) any given fruit or vegetable to eliminate useless or dangerous portions.

671 Fleagle JG. Primate Adaptation and Evolution. Academic Press, 1998.

672 Thorpe SKS, Holder RL, Crompton RH. Origin of Human Bipedalism as an Adaptation for Locomotion on Flexible Branches. Science 2007 June 1;316(5829):1328-1331.

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Discussing the differences between the sympatric, genetically related spider (6 to 8 kg body, 100 g brain) and howler monkeys (6 to 8 kg body, 50 g brain), Milton notes:

“Considering that the most striking difference between howler and spider monkeys is their diets, I proposed that the bigger brain of spider monkeys may have been favored because it facilitated the development of mental skills that enhanced success in maintaining a diet centered on ripe fruit.

“A large brain would certainly have helped spider monkeys to learn and, most important, to remember, where certain patchily distributed fruit-bearing trees were located and when the fruit would be ready to eat. Also, spider monkeys comb the forest for fruit by dividing into small, changeable groups. Expanded mental capacity would have helped them to recognize members of their particular social unit and to learn the meaning of the different food-related calls through which troop members convey over large distances news of palatable items. Howler monkeys, in contrast, would not need such an extensive memory, nor would they need so complex a recognition and communication system. They forage for food as a cohesive social unit, following well-known arboreal pathways over a much smaller home range.”673

Spider monkeys engage in co-operative foraging and sharing of food; for example, if a single member of a small foraging group finds a tree filled with fruit, s/he will call the group members to the feast.674 Spider monkeys also co-operate in defense against predators. This monkey provides evidence that a frugivorous lifestyle can foster three of the characteristics commonly claimed to have evolved in humans as a result of hunting, i.e. communication, co-operative action, and food sharing.

Further, the spider monkey is sexually monomorphic, with males weighing only about 25% more than females (10 and 8 kg respectively), similar to the 24% difference between human males and females (68 and 55 kg respectively), using female weights as the base. This raises the possibility that a frugivorous habit favors this characteristic.

Chimps utilize somewhere in the neighborhood of 200 different plants for food and medicine:

“Wrangham (1977) estimated that adult males eat 60 different food items each month, and that their diet diversity was stable from month to month. One hundred forty plant foods were reported for chimpanzees at Gombe by Wrangham (1977) and another sixty-one identified from the observation files there. The number of plant species used by chimpanzees at Gombe is similar to the 141 plant foods recorded by Hladik (1973) at Ippasa, Gabon, and the 205 recorded by Nishida (1974) at Mahale, Tanzania. The list of plant foods used by chimpanzees will probably

673 Milton K. Diet and Primate Evolution. Scientific American 1993 August: 86-93.

674 The Primata. Black Spider Monkey (Ateles paniscus). http://www.theprimata.com/ateles_paniscus.html

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continue to grow with further observations, and as new foods are added to the diet (Teleki, 1981).”675

According to primatologist Tetsuro Matsuzawa, chimps have a “botanist’s memory” for plants: For each of the 200 plants they use, chimps remember the time of year they grow, their locations, and their specific uses.676, 677, 678

Chimpanzees also may have knowledge of how to treat their own illnesses with specific medicinal plants, or food plants in specific stages of development. For example, Krief et al. report observing a 17- year-old chimpanzee who had a parasite infection consume only unripe figs while the rest of the party consumed only ripe figs.679 The latex of unripe figs contains ficin,680 which digests living intestinal parasites without harming chimps or humans.681

Krief et al. also report observing a 6-year-old female, diagnosed by veterinary examination with parasitic infection, consume the bark of Albizia granibraceata, which no other member of the troupe consumed. Laboratory evaluation of this bark demonstrated it has anti-parasitic properties.682

Citing other such observations, Krief et al. state that “the evidence that sick chimpanzees eat peculiar food items, which are not eaten by the healthy individuals of the group, raises the issue of specific medication,” and “Further investigations would be necessary to infer in such specific plant choices a different way of learning including individual or social learning.” 683

With cognitive catalogue of at least 200 edible food species, including their locations and time of availability; knowledge of how to use common foods in unusual ways for medicinal effect (e.g. latex of unripe figs); and a memorized pharmacopeia of an unknown number of strictly medicinal plant parts (e.g. Albizia bark), chimps have the rudiments of botanical and medical sciences.

675 Fulk R, Loomis M, Garland C. Nutrition of captive chimpanzees. In: The care and management of chimpanzees in captive environments. Chimpanzee Species Survival Plan – Husbandry Manual. Fulk R and Garland C, Eds. American Association of Zoos and Aquariums, 1992. Retrieved September 26, 2013 from http://www.nagonline.net/HUSBANDRY/Diets%20pdf/ Chimpanzee%20Nutrition.pdf

676 Grandin T, Johnson C. Animals Make Us Human: Creating the Best Life for Animals. Houghton Mifflin Harcourt, 2009. 241

677 Balcombe J. Second Nature: The Inner Lives of Animals. Palgrave Macmillan, 2010. 33.

678 Spinney L. What only a chimp knows. New Scientist 2006;190(2555):48-49.

679 Krief S, Hladik CM, Haxaire C. Ethnomedicinal and bioactive properties of plants ingested by wild chimpanzees in Uganda. J Ethnopharmacology 2005; 101: 1-15.

680 Purdue Horticulture. Fig – Ficus carica. http://www.hort.purdue.edu/newcrop/morton/fig.html#Other%20Uses

681 Krief S, Hladik CM, Haxaire C, op. cit.

682 Ibid.

683 Ibid.

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It seems noteworthy here that orangutans have outperformed chimps and gorillas in tests of general cognition,684 and utilize at least twice as many types of food as the chimps:

“Over 400 food types have been documented as part of the orangutans’ diet, and although it consists mainly of fruit, in times of scarcity orangutans will shift their eating habits to lower quality food, such as bark, leaves and termites, rather than travel to a different area.”685

Primatologist Carel Van Schaik found that orangutans can perform tasks beyond chimpanzee’s abilities, “such as using leaves to make rain hats and leakproof roofs over their sleeping nests” and also “in some food-rich areas...had developed a complex culture in which adults would teach youngsters how to make tools and find food.”686

Orangutans “very rarely” eat small vertebrates (birds, lizards, rodents, slow loris);687 in 20 years of observation, only 5 individual orangutans have been observed to eat vertebrate animal flesh, on a total of only 9 occasions.688 To the point, orangutans eat less meat than chimpanzees, and perform better than chimpanzees on tests of cognitive abilities. This casts doubt on the claim that hunting and meat-eating promotes cognitive improvements in hominoid primates.

The wild orangutan menu includes fruits enjoyed by humans: figs, rambutan, jackfruit, and durian. The spider monkey and orangutan intelligence tests suggest that, among primates, extreme frugivory or dependence on less fibrous plant foods involving utilization of a large number of different plant species found dispersed in a large home range may favor greater encephalization than utilization of animal flesh.

Ellen reports that human tropical rainforest populations also display extensive botanical knowledge:

“A recent attempt to collate data on the total inventories of plant categories for different subsistence populations (Brown 1985: 44) shows strikingly how rainforest populations have repeatedly been found to yield much longer lists than populations living in other environments, lists which may consist of between 800 and 2000 items at the upper end.”689

684 Deaner RO, van Schaik CP, Johnson V. Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology 2006; 4: 149-196.

685 Orangutan Foundation. Orangutan Diet. http://www.orangutan.org.uk/about-orangutans/diet

686 Leake J, Dobson R. Chimps knocked off top of the IQ tree. The Sunday Times 2007 April 15.

687 San Diego Zoo. Orangutan, Pongo pygmaeus, Pongo abelii. July 2003. http://library.sandiegozoo.org/factsheets/ orangutan/orangutan.htm#diet

688 Hardus ME, Lameira AR, Zulfa A, et al.. Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii). Int J Primatol 2012;33:287-304.

689 Ellen R. Anthropological approaches to understanding the ethnobotanical knowledge of rainforest populations. In: 'Tropical rainforest research: current issues', eds. D. S. Edwards, W.E. Booth and S.C. Choy. Kluwer: Dordrecht 1996. 457-465.

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Let me re-emphasize that Lefebvre690 (discussed above) found that arboreal or forest-dwelling lifestyle correlates with increased encephalization in primates, and, as just noted, human rainforest populations appear to cognitively catalogue much larger amounts of botanical information than people dwelling in non-forest environments. Africa has more than 1000 species of edible wild fruits, which to this day still play a key role in rural human nutrition, particularly for children.691 As discussed in Chapter 1, African grasslands provide more than 100 plant species having edible USOs. This suggests that an African hominin that utilized both woodland and grassland plant resources for both food and medicine – such as early human ancestors – would require considerable cognitive power to manage those resources.

In addition, natural selection would certainly favor any primarily frugivorous primate who had the cognitive capacity to notice the relationship between seed and fruit, and between environmental conditions and plant productivity, and figure out ways to encourage the growth and productivity of the wild plants that provided the most nutritious fruits and vegetables, such as sheltering from pests or increasing water supply. Such a primate would obtain more food to fuel reproduction, and also have an excellent chance of eventually inventing agriculture.

Meat-eating Mentality

The evidence reviewed in this book indicates that humans lack any of the specific psychical or physical adaptations to eating flesh found in nonhuman carnivores. Humans eat flesh in spite of their natural (pre-socialization) aversion to blood and guts and lack of physical equipment for hunting. Few people enjoy harming or killing other sentient creatures, leading those who eat flesh to reduce their discomfort with carnivory via attempts to magically transmute, deny, disguise, or rationalize the act:

• Magical thinking: Butchering animals with “religious” ritual to assuage our shame and natural revulsion to the practice. • Fantasy consecration: Imagining that hunting and meat-eating constitute “sacred” acts that enable humans to establish some special connection to the earth, creatures, community, and some (imaginary) divine entity.692 • Concealment: Hiding butchery from common view. • Disguise: o Draining the blood from butchered animals and cutting them into pieces that prevent recognition that the food came from a living animal. o Using various plant-based sauces and condiments to add flavor to the otherwise flavorless flesh. • Euphemistic distraction: We eat “meat” rather than muscle, “beef” rather than cow, “pork” rather pig, and so on.

690 Lefebvre, op. cit.

691 National Research Council. Lost Crops of Africa:Vol. III: Fruits. National Academies Press, 2008. 185.

692 For example: Eaton RL. The Sacred Hunt: Hunting As a Sacred Path. Sacred Press, 1999.

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• “Scientific” rationalization: Meat made us human; maintenance of human ‘superiority’ requires a meat-based diet.

Bratanova et al. found that when people believe that someone uses a non-human animal for food, they judge that animal to have less sensitivity to pain in comparison to when they believe that no-one uses the same animal as food, despite receiving the same evidence in either case.693 We have no evidence to support the notion that prey animals have lesser pain sensation than predators, but we nevertheless fantasize that any animal we choose to eat feels less pain than any animal we don’t choose to eat.

Practices of this kind amount to elaborate self-deception and characterize mental distress, not mental health or extraordinary intelligence. They suggest that we go into trances of denial and delusional thinking both to support killing and flesh-eating, and to recover from the trauma that our nervous system endures when we indulge these actions. This hardly seems like a leg up on the evolutionary ladder.

If engaging in meat-eating does promote delusion and other mental pathologies, it may serve as the basis for or accompaniment to other pathological behavior exhibited by humans.

Animal Cruelty and Social Violence

Prehistoric humans killed animals with primitive weapons (stones, clubs, dull wooden spears) and any method they would have used would have resulted in the animal dying a relatively slow, tortured death as blood oozed copiously from wounds while the creature had full consciousness and cried and writhed in pain. In other words, their killings had all the essential marks of cruelty.

Randour states that “Animal cruelty is a precursor to disruptive and delinquent behavior; it also co- occurs with the commission of family violence and other criminal behavior.”694 A U.S. Department of Justice document by Ascione reports that research has found animal cruelty, including torturing and killing animals, strongly linked to violent and antisocial behavior.695

If as the data cited by Randour and Ascione suggests, hunting, killing, and eating of animals fosters violent and antisocial behavior in modern humans, it may also have done so in human ancestors. Perhaps it set the stage for hunting and eating human children and adolescents, as apparently done by some stone age Europeans.696 Such behavior would probably have retarded the development of human intelligence and civilization.

693 Bratanova B, Loughnan S, Bastian B. The effect of categorization as food on the perceived moral standing of animals. Appetite 2011;57: 193-196.

694 Randour ML. Including Animal Cruelty as a Factor in Assessing Risk and Designing Interventions. The National Conference of the Hamilton Fish Institute on School and Community Violence. 2004.

695 Ascione FR. Animal Abuse and Youth Violence. U.S. Department of Justice, Office of Justice Programs, Office of Juvenile Justice and Delinquency Prevention. September 2001.

696 Owen J. Human Meat Just Another Meal for Early Europeans? National Geographic News 2010 Aug 31.

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Animal-Based Diets and Brain Damage

According to paleontological research, in the past 20,000 years, human brain size has significantly declined in both agricultural and recent hunter-gatherer populations, apparently despite meat consumption:

“....the average volume of the human male brain has decreased from 1,500 cubic centimeters to 1,350 cc, losing a chunk the size of a tennis ball. The female brain has shrunk by about the same proportion... If our brain keeps dwindling at that rate over the next 20,000 years, it will start to approach the size of that found in Homo erectus, a relative that lived half a million years ago and had a brain volume of only 1,100 cc.”697

Of interest, some evidence suggests that animal-based diets may induce chronic brain inflammation and damage, resulting in impaired cognition, depression and hostility, while plant-based diets may have the opposite effects.

Animal flesh inevitably provides its consumer with dietary arachidonic acid (AA) because this fat is used in muscle cell membranes. The AA content of flesh from grass-fed animals (g/100 g edible) does not appear to differ significantly from that of animals fed corn-based concentrate.698

Humans do not require dietary arachidonic acid, but produce it from dietary linoleic acid (LA), most richly supplied by plants. Large increases in dietary LA apparently do not increase tissue levels of AA:

“Increasing LA by as much as 551% from baseline and reducing LA by as much as 90% from baseline failed to yield compelling evidence supporting the concept that any conversion of dietary LA to downstream metabolites results in tissue enrichment of AA, a notion commonly assumed.”699

This indicates that human metabolism regulates production of AA, only producing it as needed. Direct consumption of AA in the form of animal flesh bypasses the regulation, resulting in elevations of tissue AA.700

697 McAuluffe K. If Modern Humans Are So Smart, Why Are Our Brains Shrinking? Discover Magazine 2010 September. Published online January 20, 2011. Retrieved September 25, 2013 from http://discovermagazine.com/2010/sep/25-modern- humans-smart-why-brain-shrinking#.UkOhERlbv4g

698 Kraft J, Kramer JKG, Schoene F, Chambers JR, et al.. Extensive Analysis of Long-Chain Polyunsaturated Fatty Acids, CLA, trans-18:1 Isomers, and Plasmalogenic Lipids in Different Retail Beef types. J Agric Food Chem 2008;56:4775-4782.

699 Rett BS, Whelan J. Increasing dietary linoleic acid does not increase tissue arachidonic acid content in adults consuming Western-type diets: a systematic review. Nutr Metab (Lond) 2011;8:36.

700 Thies F, Nebe-von-Caron G, Powell JR, et al.. Dietary supplementation with gamma-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older adults. J Nutr 2001 July 1;131(7):1918-1927.

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High levels of AA in the brain promote neuroinflammation and brain damage, and chronic neuroinflammation is associated with slow progressive neurodegenerative diseases such as Alzheimer’s, Parkinson’s, Down syndrome, Huntington disease, and multiple sclerosis.701 These represent the end stage of chronic or severe neuroinflammation; the research discussed below suggests that antisocial changes in mood, including increased hostility and aggression, may represent the early stages.

D’Anci et al. found that people on low carbohydrate, flesh-based diets experience impairment of memory tasks, visuospatial memory, and reaction time.702 Brinkworth et al. assigned overweight subjects to either a 61% fat, 4% carbohydrate animal-based diet, or a 46% carbohydrate, 30% fat, more plant-based diet, and followed them for one year; at week 52, the subjects eating the animal-based diet scored higher on scales for anger-hostility, confusion-bewilderment, and depression-dejection.703 Holloway et al. reported that people assigned to eat a 75% fat, low-carbohydrate animal-based diet for 5 days showed impaired attention, cognitive processing speed, and mood when given standardized tests.704

In a study sponsored by low-carbohydrate diet advocate Robert Atkins, MD, McClernon et al. reported that subjects who followed a low-carbohydrate ketogenic animal-based diet had better mood than those following a low-fat, more plant-based diet.705 However, Brinkworth et al. note that this study did not assess mood using validated scales; instead, “they used a symptom checklist developed by practitioners specifically for evaluating and treating individuals using an LC diet for weight loss that may have biased the result toward a positive effect of an LC diet as opposed to an LF diet.”706

A considerable body of evidence suggests that flavonoids richly provided by plant foods (but poorly provided by animal foods) contribute to brain health. According to Spencer, flavonoids appear to have an influence on brain function and structure:

“Evidence suggests that dietary phytochemicals, in particular flavonoids, may exert beneficial effects in the CNS by protecting neurons against stress induced injury, by suppressing the activation of microglia and astrocytes, which mediate neuroinflammation, and by promoting synaptic plasticity, memory, and cognitive functioning. Evidence also supports the localization of

701 Farooqui AA, Horrocks LA, Farooqui T. Modulation of inflammation in brain: a matter of fat. J Neurochemistry 2007:101:577-599.

702 D’Anci KE, Watts KL, Kanarek RB, Taylor HA. Low-carbohydrate weight-loss diets. Effects on cognition and mood. Appetite 2009;52:96-103.

703 Brinkworth GD, Buckley JD, Noakes M, et al.. Long-term Effects of a Very Low-Carbohydrate Diet and a Low-Fat diet on Mood and Cognitive Function. JAMA Internal Medicine (Formerly Archives of Internal Medicine) 2009 Nov 9:169(20): 1873-1880.

704 Holloway CJ, Cochlin LE, Emmanuel Y, et al.. A high-fat diet impairs cardiac high-energy phosphate metabolism and cognitive function in healthy human subjects. Am J Clin Nutr, 2011 Apr;93(4):748-55.

705 McClernon FJ, Yancy WS, Eberstein JA, Atkins RC, Westman EC. The effects of a low-carbohydrate ketogenic diet and a low-fat diet on mood, hunger, and other self-reported symptoms. Obesity (sliver Spring) 2007 Jan;15(1):182-7.

706 Brinkworth et al., op. cit.

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flavonoids within the brain, thus these phytochemicals may be regarded as a potential neuroprotective, neuromodulatory or anti-neuroinflammatory agents.”707

Dietary intervention studies in multiple mammals, including humans, have found that flavonoids improve memory and learning, protect against neuronal death, and may prevent dementia and Alzheimer’s disease.708

In contrast to the trend toward impaired cognition and hostile mood in the above studies of people eating animal-based diets, several studies have found improved cognition and reduced hostility in people eating plant-based diets.

Kjeldsen-Kragh et al. reported that patients who adopted a vegetarian diet for treatment of rheumatoid arthritis showed an unexpected decrease in psychological distress in comparison to patients who continued to consume animal flesh.709 Schweiger et al. reported that healthy young women assigned to a vegetarian weight loss diet had significantly better global mood than those assigned to a mixed diet group; they found a significant correlation between relative carbohydrate intake and global mood.710

Weidner et al. studied the effect of 5 years of dietary cholesterol reduction on negative emotions including depression and aggressive hostility.711 They reported that people who followed a low-fat, high complex carbohydrate diet (more plants, less animal flesh) at the end of the study had significantly greater improvements in depression and a reduction of aggressive hostility, concomitant with a reduction in blood cholesterol levels, compared to those who ate a high-fat “American diet.”

Beezhold et al. compared the mood states of vegetarian and omnivorous Seventh Day Adventist adults.712 They found that omnivorous SDAs reported significantly higher levels of anger-hostility, tension-anxiety, depression-dejection, and confusion than vegetarians. Further analysis revealed that individuals with low intakes of EPA, DHA, and AA, fatty acids found only in animal flesh, reported having the better moods.

707 Spencer JPE. Flavonoids: modulators of brain function? British Journal of Nutrition 2008;99(E-Suppl 1): ES60-ES77. doi: 017/S0007114508965776.

708 Spencer JPE. Food for thought: the role of dietary flavonoids in enhancing human memory, learning, and neuro-cognitive performance. Proceedings of the Nutrition Society 2008; 67:238-252. doi:10.1017/S0029665108007088

709 Kjeldsen-Kragh J, Haugen M, Forre O, et al.. Vegetarian diet for patients with rheumatoid arthritis: can the clinical effects be explained by the psychological characteristics of the patients? Br J Rheumatol 1994 Jun:33(6):569-75. Abstract.

710 Schweiger U, Laessie R, Kittl S, et al.. Macronutrient intake, plasma large neutral amino acids and mood during weight- reducing diets. J Neural Transm 1986;67(1-2):77-86. Abstract.

711 Weidner G, Conner SL, Hollis JF, Conner WE. Improvements in Hostility and Depression in Relation to Dietary Change and Cholesterol Lowering: The Family Heart Study. Ann Intern Med 1992:117(10):820-823.

712 Beezhold BL, Johnston CS, Daigle DR. Vegetarian diets are associated with healthy mood states: a cross-sectional study in Seventh Day Adventist adults. Nutrition Journal 2010;9:26.

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Following up on this research, Beezhold and Johnston randomly assigned 39 omnivores to consume either an omnivorous diet, a diet restricting flesh to fish only, or a lactovegetarian diet free of meat, fish, and poultry.713 They reported that the individuals assigned to the vegetarian group experienced a significant improvement in mood scores on standardized tests. In their words:

“These data suggest that consuming a diet high in meat, fish, and poultry may negatively impact mental state. Beyond differences in the ratio of long-chain fatty acids, vegetarian diets are typically rich in antioxidants, potentially conveying mood protection for the VEG group via reduction of oxidative stress.”714

This data suggests that consumption of animal flesh of any type (wild, grass-fed, or concentrate-fed) may cause acute and chronic brain damage that adversely affects mood and behavior to variable degrees depending on individual constitution, quantity of flesh consumed, and total dietary context (some authors suggest that increased intake of DHA may reduce the harmful effects of dietary AA715 although Beezhold et al. did not find EPA or DHA intake protective against antisocial moods716).

This data also suggests that the human brain may require substantial daily intake of fruit and vegetable flavonoids to develop and maintain healthy structure and function, and provides additional evidence suggesting that the human brain evolved in dependence on a plant-based diet. It raises the possibility that various defects in brain structure, memory, learning, and cognition may result from chronic dietary fruit and vegetable flavonoid deficiency or slow poisoning by AA, EPA, and DHA. It further raises the possibility that humans deprived of adequate dietary fruits and vegetables or eating animal-based diets may develop pathological changes in neurological structure and function that may lead to pathological patterns of perception, cognition, communication, and behavior.

Apparently the great Chinese philosopher, Kong Qiu (Confucius) believed that killing animals and meat- eating has a negative effect on on human mental and social health, reflected in the following words attributed to him:

“The honorable and upright man keeps well away from both the slaughterhouse and the kitchen. And he allows no knives on his table."

Confucius believed that butchery makes us less humane, therefore less human. The data cited above revealing the potentially negative effect of dietary arachidonic acid on brain health suggests that Western science may eventually catch up with him.

713 Beezhold BL, Johnston CS. Restriction of meat, fish, and poultry in omnivores improves mood: A pilot randomized controlled trial. Nutrition Journal 2012;11:9.

714 Ibid.

715 Ibid.

716 Beezhold BL an Johnston CS, op. cit..

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Does Meat-Eating Make People Warlike?

If cruelty to animals increases the propensity to violence, and an animal-based diet impairs cognition and increases anger and hostility, as suggested by the data discussed above, one might wonder if populations who eat animal-based diets have a greater inclination to war in comparison to populations who eat more plant-based diets.

In A Study of War, esteemed political scientist Quincy Wright ranked the relative warlikeness of historical civilizations based on four criteria: (i) habituation in cruelty arising from bloody religious rites, sports, and spectacles, (ii) aggressiveness manifested by frequency of active invasions in imperial or interstate wars, (iii) military morale indicated by discipline of armies and reserves, and (iv) political despotism manifested by completeness of territorial and functional centralization of authority with absence of constitutional and customary limitations.

Wright noticed that civilizations dependent on grazing (and therefore consuming arachidonic acid via meat) tended to be more warlike, and that civilizations that depended more on irrigated agriculture (and therefore eating more plants) tended to be more peaceful. He identified Chinese civilization as one of the most peaceful of historical civilizations, whereas Western civilization ranked as a moderately warlike civilization (Table 17.7).717 Among the peaceful cultures, the Indic, Hindu, Sinic, and Chinese all had ethics (Vedic, Jain, Buddhist, Confucian, Taoist) that discouraged eating animals and encouraged predominantly plant-based diets.

Table 17.7: Civilizations and Warlikeness

Warlike Moderately warlike Peaceful

Babylonian Hittite Byzantine Classic Arabic Egyptian Tartar Scandinavian Minoan Japanese Western Mesopotamian Andean Russian Nestorian Syriac Yucatec Irish Iranian Germanic Indian Mexican Hindu Sinic Chinese Mayan

Source: Wright Q. A Study of War. University of Chicago Press, 1983. 45-46.

This raises these questions:

717 Wright Q. A Study of War. University of Chicago Press, Nov 15, 1983. 45-46

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1. Does an animal-based diet, by providing dietary arachidonic acid, alter human brain chemistry to favor moods of depression, hostility, and aggression, and in turn lead people to lean towards the war path? 2. Does a plant-based diet establish a brain chemistry that favors moods of humor, friendliness, and co- operation, and in turn lead people to lean towards the peace path, rather than the war path? 3. Has meat-eating retarded human evolutionary development and survival by creating a brain condition (neuroinflammation due to overload of arachidonic acid and lack of phytonutrients) that causes people to behave more aggressively in general, and to ignore or deny the destructive impact of their actions on other humans, animals, and the ecosystem on which they depend?

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18: Meat-Adaptive Genes?

Finch and Stanford have proposed that modern humans have “meat-adaptive genes”:

“During the last several million years, our human ancestors evolved two major changes in life history that would appear to be mutually antagonistic: a shift from vegetarian to meat-rich diets and an increase in adult life expectancy...The major increase in meat eating in human ancestors would be expected to elevate blood cholesterol, which is a risk factor in both Alzheimer’s disease and vascular disease. Other hazards of meat-rich diets include diet-induced hypercholesterolemia and infections. Thus, the increases in meat eating would be predicted to shorten life expectancy by promoting chronic diseases. We propose that meat-adaptive genes were evolved to delay dysfunctions and diseases of brain and heart caused by this increasingly meat-rich diet.”718

While Finch and Stanford offer this as a hypothesis, Leonard et al.719 state that Finch and Stanford720 “have recently shown that the evolution of key ‘meat-adaptive’ genes in hominid evolution were critical to promoting enhanced lipid metabolism necessary for subsisting on diets with greater levels of animal material.” It seems both comical and sad that in a scientific context Leonard et al. interpret a paper proposing a hypothesis as ‘showing’ that humans have ‘meat-adaptive’ genes, apparently without subjecting that hypothesis to critical analysis, as I will do in this chapter.

Further, Finch and Stanford suggest that these ‘meat-adaptive genes’ only delay the onset of diseases promoted by meat consumption; not that these genes make humans capable of living on meat-rich diets without those diseases, or give humans anatomical equipment that improves hunting ability. If a gene merely delays the onset of a disease caused by meat-eating by 5 or 10 years, how ‘meat-adaptive’ is it?

This brings us back to the concept of kluge. Even if these genes confer some increased but limited protection against diseases induced by meat-eating, we still would not have humans that, as a whole, have adapted to meat-eating. Instead, these genes would amount to naturally-selected kluges: they constitute patch-work that may reduce the impact of a problem, but not eliminate it.

Finch and Stanford’s list of possible ‘meat-adaptive genes’ includes apoE3, Lp(a), CMAH, HLA, Prp, CFTR, and Hb. They suggest that a unique human allele of apolipoprotein E, apoE3, serves as the best supported example of meat-adaptive gene because of alleged effects on lipid metabolism. In contrast to Finch and Stanford, others have adduced evidence indicating that the human CMAH mutation renders humans specifically poorly adapted to consumption of mammalian meat. Consequently, for the sake of brevity, I will focus on apoE3 and CMAH in this critical analysis of their hypothesis.

718 Finch CE and Stanford CB. Meat-Adaptive Genes and the Evolution of Slower Aging in Humans. The Quarterly Review of Biology 2004 Mar;79(1): 3-50.4.

719 Leonard WR, Snodgrass JJ, Robertson ML. Evolutionary Perspectives on Fat Ingestion and Metabolism in Humans. In: Montmayeur JP, le Coutre J (eds.). Fat Detection: Taste, Texture, and Post Ingestive Effects. CRC Press, 2010. Chapter 1.

720 Finch and Stanford, op. cit..

243

ApoE3: Meat-Adaptive, or Agriculture-Adaptive?

Humans have three primary apoE alleles: apoE2, apoE3, and apoE4. In all modern human populations, the apoE3 allele predominates, followed by apoE4, while apoE2 is least common. In non-human primates, the apoE allele most resembles the human apoE4. Finch and Stanford based their hypothesis that apoE3 provides a specific adaptation to meat-eating on the claim that apoE3 provides protection against while apoE4 lends susceptibility to vascular and Alzheimer’s diseases in modern civilized human and captive primate populations.

Finch and Stanford argued that “the evolution of the human apoE3 and other candidates for meat- adaptive genes enabled the shift from an herbivorous ape diet to the more omnivorous diet of hominids, while also enabling a major increase in life span.”721 The apoE3 mutation appears to have first increased in frequency approximately 200,000-300,000 years ago722, while hominins appear to have started eating animal flesh at least 2.6 million years ago.723 The date of origin of apoE3 remains uncertain, but if it existed before 300,000 years ago, meat-eating by australopithecus species, H. habilis, and H. erectus apparently did not favor its reproduction for more than two million years. In short, the apoE3 allele started increasing in frequency 2.3 million years too late to facilitate the shift from an herbivorous ape diet to the more omnivorous diet of early hominins.

Finch and Stanford argue that a hunting and meat-eating lifestyle favored longevity-enhancing genes, specifically apoE3, to accommodate “long years of skills training” because “Humans lack the anatomical weapons (specialized teeth and claws) of other hunting mammals, which necessarily extends the time to full independence.” Archaeological evidence suggests that H. erectus may have had sufficient skill in hunting to contribute to the extinction of elephants in some regions before 400,000 years ago.724 Like modern humans, H. erectus lacked the anatomical weapons of other hunting mammals, so he presumably also needed “long years of skills training” in order to become a successful hunter. Apparently, H. erectus obtained the requisite lifespan without the benefit of a high frequency of the apoE3 allele, since, as noted above, this gene first increased in frequency at least 100,000 years too late to help H. erectus avoid dietary lipid-induced vascular and neurological diseases long enough to become a skilled elephant hunter.

The hypothesis that apoE3 serves primarily as a meat-adaptive gene predicts that apoE3 will occur at the highest frequencies in populations with the most meat-rich diets, and at the lowest frequencies in populations with more plant-based diets.

721 Finch and Stanford, op. cit., 29.

722 Fullerton SM, Clark AG, Weiss KM, et al.. Apolipoprotein E Variation at the Sequence Haplotype Level: Implications for the Origin and Maintenance of a Major Human Polymorphism. Am J Hum Genet 200 Oct;67(4):881-900.

723 Pobiner B. Evidence for Meat-Eating by Early Humans. Nature Education Knowledge 2013;5(6):1.

724 Ben-Dor et al., Man the Fat Hunter. PLOS One 2011;6(12): e28689. doi:10.1371/journal.pone.0028689.

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Corbo and Scacchi examined the frequency of apoE alleles across 44 African, European, Asian, Native American, and Oceanic ethnic groups.725 They found that the highest frequencies of the apoE3 allele occur in populations with a long-established agricultural economy, such as those of the Mediterranean basin or East Asia. As they state, this suggests that “It is possible that the metabolic properties of the E3 isoform proved to be particularly advantageous in the transition from food collection to food production.”726

Moreover, the apoE4 allele occurs with greatest frequency in populations with a foraging economy, or a currently or historically scarce, sporadically available, or qualitatively poor food supply. Populations with relatively high frequencies of apoE4 include Pygmies, Khoi San, aborigines of Malaysia and Australia, Papuans, Lapps, and some native Americans, specifically Cayapas and Inuit. Among Pygmies, the apoE4 and apoE3 occur at, respectively, the highest and lowest frequencies so far recorded – 0.41 and 0.54.727

According to Cohen,”the transition from small mobile hunting and gathering groups to larger sedentary populations relying on storage and agriculture is likely to have been accompanied by a reduction in the proportion of animal products in the diet.”728 If so, this data casts doubt on the hypothesis that meat- eating selects for apoE3, since it occurs with greatest frequency in populations with a lower meat intake (agriculturalists) compared to those with higher meat intake. For example, it occurs with a frequency of 0.88 and 0.90 among plant-based Greeks and Sardinians, respectively, but 0.64 among reindeer-based Lapps. Among native Americans, it occurs with a frequency of 0.77 among the carnivorous Inuit, but 0.92 among the agricultural Mayans.

Since apoE3 occurs with greater frequency in populations with agricultural diets than those with hunting diets, it seems that more plant-based diets favor apoE3, and meat-rich diets may favor apoE4. This data certainly fails to support the Finch and Stanford hypothesis that meat-rich diets more strongly favor apoE3 than plant-based diets. On the contrary, this data suggests that starch-based diets favor apoE3!

Corbo and Scacchi suggest one possible survival advantage to apoE4 in a foragers’ environment:

“Since APOE*4 is associated with higher absorption at intestinal level, and higher plasma cholesterol levels, individuals carrying it would be favoured because this allele could help in rebalancing cholesterol levels which would otherwise be too low.”729

725 Corbo RM, Scacchi R. Apolipoprotein E (APOE) allele distribution in the world. Is APOE*4 a ‘thrifty’ allele? Ann Hum Genet (1999);63:301-310. 307.

726 Ibid., 306.

727 Ibid., 303.

728 Cohen MN. Health and the Rise of Civilization. Yale University Press, 1989. 61.

729 Corbo and Scacchi, op. cit., 307

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This suggests that natural selection may favor apoE4 when the environment limits or places a drain on cholesterol levels, and apoE3 when the environment places less drain on cholesterol levels. Among foragers, many features of diet may reduce cholesterol levels, including high fiber intakes, low total energy intake, sporadic episodes of nutritional stress (famine), and, as discussed in detail in Chapter 16, parasite infections primarily acquired by consuming animal flesh.

Finch and Stanford note some evidence suggesting that apoE4 “is a resistance factor for lipophilic parasites.”730 Notably, the increase in frequency of apoE3 and concomitant decrease in apoE4 frequency seems to have occurred well after evidence for widespread habitual control of fire, 300,000 to 400,000 years ago,731 and approximately coincident with two other events that occurred about 200,000 years ago: duplication of the salivary amylase gene in humans,732 and the first evidence of emergence of H. sapiens.733 Cooking foods probably reduces selection for parasite-adaptive apoE4. Coupled with the evidence that apoE3 occurs with greater frequency in agricultural populations than in hunting-based populations, this suggests that either starch-based diets or cooking of meat reduces natural selection of apoE4 and favor the reproduction of apoE3.

Finch and Stanford argue that meat-rich diets favor apoE3 because it would delay the vascular and Alzheimer’s diseases that such diets promote. Based on some evidence that captive chimpanzees or other primates (all of whom have an apoE genotype similar to apoE4 and lacking apoE3) have a high susceptibility to early onset of vascular diseases when fed meat-rich diets, Finch and Stanford suggest that current age-related diseases would have affected reproductive fitness in presumably apoE4- genotype prehistoric humans by striking at very early ages.

In contrast to Finch and Stanford, Corbo and Scacchi point out that, in accord with Darwinian theory, “the association with the two diseases could have no effect on the allele frequency because both occur in the post-reproductive age.”734 Moreover, Corbo and Scacchi point out that apoE4 appears not to increase the risk of coronary artery disease (CAD) or Alzheimer’s disease (AD) in non-Westernized populations.

“Although the data are still rather scarce, some evidence for the change taking place can be brought to light by comparing the APOE*4 behaviour pattern between the Africans and African Americans (APOE*4 frequency = 0.260 (Kamboh, 1995a)). Among Sub-Saharan Africans the

730 Finch and Stanford, op. cit., 25.

731 Roebroeks W, Villa P. On the earliest evidence for habitual use of fire in Europe. PNAS 2011 Mar 14. doi:10.1073/pnas. 1018116108

732 Perry GH, Dominy NJ, Claw KG, et al.. Diet and evolution of human amylase gene copy number variation. Nat Genet. 2007 October; 39(10): 1256–1260.

733 University Of Utah (2005, February 28). The Oldest Homo Sapiens: Fossils Push Human Emergence Back To 195,000 Years Ago. ScienceDaily. Retrieved September 12, 2013, from http://www.sciencedaily.com/releases/ 2005/02/050223122209.htm

734 Corbo and Scacchi, op. cit., 307.

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levels of plasma total and LDL cholesterol (major risk factors for CAD) observed in APOE*4 carriers were similar to those of the APOE*3 homozygotes...., whereas significantly raised total and LDL cholesterol levels were associated with APOE*4 in African Americans... suggesting that their carrying the APOE*4 could represent a risk for developing CAD. The association between APOE*4 and AD was not found in Nigerians or East Africans..., but is present in African Americans, though weaker than in whites...

“The comparison confirms that to carry APOE*4 may become disadvantageous in a Westernized environment...”735

Greenland Inuit belong to a lineage that has inhabited the Arctic and eaten a very meat-rich diet (at least 95% animal flesh) in relative genetic isolation for about 15,000 years. The hypothesis that apoE3 protects against vascular disease induced by meat-rich diets predicts that Greenland Inuit with apoE3 genotype would have less vascular disease than those with apoE4 genotype. Boudreau et al. reported finding no significant association between apoE genotypes and extent of atherosclerotic lesions in the aorta or coronary arteries, nor any strong evidence for an association with serum lipid levels, in 98 post- mortem Greenland Inuit with a mean age of 59 and a genotype frequency of 0.78 for apoE3 and 0.21 for apoE4.736

Similarly, Sandholzer et al. found no significant effect of apo E variation on cholesterol concentration among Khoi San (!Kung, Ju/‘hoansi), who had a mean total cholesterol of 149 mg/dl and an apoE3/E4 distribution of 0.55/0.37.737 According to Cordain et al., these people obtain 33% to 68% of their subsistence from animal flesh.738 The absence of a significant difference in vascular pathology or its major risk factor (serum cholesterol) between different apoE genotypes in hunter-gatherer populations eating meat-rich diets casts doubt on the assertion that natural selection favored apoE3 because it delayed the disease in prehistoric meat-eaters.

As discussed in Chapter 16, both contemporary and prehistoric hunter-gatherers had high incidences of cholesterol- and iron-depleting parasite infections, and this alone would have provided significant

735 Corbo and Scacchi, op. cit., 308.

736 Boudreau DA, Scheer WD, Malcom GT, et al.. Apolipoprotein E and atherosclerosis in Greenland Inuit. Atherosclerosis 1999 Jul;145(1):207-19. Abstract.

737 Sanholzer C, Delport R, Vermaak H, et al.. High frequency of the apoE4 allele in Khoi San from South Africa. Hum Genet 1995 Jan;95(1):46-8. Abstract.

738 Cordain L, Eaton SB, Brand-Miller J, et al.. The paradoxical nature of hunter-gatherer diets: meat-based, yet non- atherogenic. Eur J Clin Nutr 2002;56(S1):542-552. 544, Table 1.

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protection against meat-related vascular and neurological diseases.739, 740, 741 , 742 Prehistoric hominins had obtained tapeworms from raw meat-eating by two million years ago.743 As noted in Chapter 16, tapeworms require cholesterol and fats for development of their larval cysts, but have lost the ability to produce these lipids, so they obtain them from their hosts.744 Since eating raw or undercooked meat and drinking untreated ground water both provide the parasites that protect against the chronic diseases the meat itself would promote, parasite infections very probably explain the low cholesterol levels and incidence of vascular diseases and dementia in many hunter-gatherer populations, rendering unnecessary the hypothesis that prehistoric humans needed apoE3 to avoid these diseases.

Similarly, all of the evidence for early onset of vascular and neurological degenerative diseases in primates comes from studies of sedentary captives kept free of parasites by modern medicine, and fed formula diets (not wild plants) and cooked domesticated animal products higher in total and saturated fat than wild animal flesh. Further, captive apes with heart disease die from diffuse myocardial fibrosis of unknown cause, not the coronary artery atherosclerosis found in humans; “The typical myocardial infarction of humans due to coronary artery thrombosis is rare in these apes, despite their human-like coronary-risk-prone blood lipid profiles.”745 These experiments do not replicate prehistoric conditions (hominins drinking untreated water or handling or eating raw or undercooked wild game flesh, with no medical care and endemic parasites) and don’t produce thrombotic myocardial infarctions in apes so they don’t shed much light on the subject.

Since we lack evidence that apoE4 increased the risk of vascular and neurological diseases in wild hominoids or African or Inuit hunter-gatherers, we have no reason to believe that natural selection would have favored apoE3 on the basis of its ability to delay those diseases. Hence, we lack evidence that prehistoric hominins eating limited amounts of meat suffered early-onset vascular and neurological diseases that would affect reproductive fitness. I have to agree with Corbo and Scacchi that the association of apoE4 with vascular and Alzheimer’s diseases could have no effect on the allele frequency in prehistoric populations because, so far as we know, both diseases primarily impact vitality

739 Sianto L, Chame M, Silva CS, et al.. Animal helminths in human archaeological remains: a review of zoonoses in the past. Rev Inst Med Trop Sao Paulo. 2009 May-Jun;51(3):119-30. PMID: 19551285.

740 Bansal D, Bhatti HS, Sehgal R. Altered lipid parameters in patients infected with Entamoeba histolytica, Entamoeba dispar and Giardia lamblia. Br J Biomed Sci. 2005;62(2):63-5. PMID:15997878

741 Stanley RG, Jackson CL, Griffiths K, Doenhoff MJ. Effects of Schistosoma mansoni worms and eggs on circulating cholesterol and liver lipids in mice. Atherosclerosis 2009 Nov;207(1):131-8. PMID: 19464685.

742 Bansal D, Bhatti HS, Sehgal R. Role of cholesterol in parasitic infections. Lipids in Health and Disease 2005;4:10.

743 Hoberg EP, Alkire NL, Queiroz AD, Jones A. Out of Africa: origins of the Taenia tapeworms in humans. Proc R Soc Lond B 2001 April 22;268(1469):781-87.

744 Tsai IJ, Zarowiecki M, Holroyd N, et al.. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 2013 April 4;496:57-63.

745 Varki N, Anderson D, Herndon JG, et al.. Heart disease is common in humans and chimpanzees, but is caused by different pathological processes. Evol Appl. 2009 Feb;2(1):101-112.

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only in the post-reproductive age and only in modernized populations having meat-rich diets but low parasite loads.

Finch and Stanford suggested that prehistoric humans needed apoE3 to protect against age-related diseases promoted by meat-eating because they had to eat meat to ensure reproductive success:

“We conclude that meat eating was important to human evolution by reducing the risk of marginal neurological impairments from sporadic deficits of micronutrients, as well as providing a highly efficient energy source”746

They suggested that diets lacking meat produce deficiencies of vitamins B12 and D and permanent mild cognitive impairments in children on the basis of studies of people consuming “vegan-type macrobiotic diets” in modern nations, and the statement that “Vitamin B12 is not provided by plant foods.”

Human skin manufactures as much vitamin D as required in response to adequate sun exposure, so prehistoric humans did not depend on diet for vitamin D. As shown in Chapter 15, humans also have physiological equipment for protection against sporadic deficits of vitamin B12, microbes (not animals) produce B12, meat-eating does not reliably prevent B12 deficiency, and our prehistoric ancestors probably would have obtained B12 from water, plants, and possibly intestinal flora. Given that modern children eating “vegan-type macrobiotic diets” are not living in the prehistoric environment nor drinking the B12-rich water or eating the plant foods available to our prehistoric ancestors, and probably have had antibiotic treatments, their experience probably has little or no relevance to this topic.

Moreover, the claim that meat-eating would have provided “a highly efficient energy source” for australopithecus species, early Homo, or H. erectus remains open to question given considerations I discussed in Chapter 1 and 4.

Finch and Stanford also suggest that prehistoric humans would have suffered neurological impairments from “sporadic” lack of essential fatty acids without consuming meat. They imply that not only humans but all mammals have a dietary requirement for arachidonic acid (AA) and docosahexaenoic acid (DHA) because of a lack of required enzymes:

“Mammals lack enzymes to synthesize the ‘essential’ PUFAs (Innis 200; Nakamura et al. 2001). In particular, arachidonic acid (AA) and docosahexaenoic acid (DHA) are made from different precursor fatty acids (AA from linoleic acid, DHA from alpha-linolenic acid) by desaturases and elongases.”747

Mammals do lack the enzymes to produce the essential PUFAs, linoleic and linolenic acid (LA and LNA), which occur abundantly in plants; however, mammals do not lack the enzymes necessary to synthesize AA and DHA from the essential precursors. As discussed in Chapter 17, plants, particularly

746 Finch and Stanford, op. cit., 12.

747 Finch and Stanford, op. cit., 11.

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green leaves, provide plenty of LA and LNA, human mothers eating plant-based diets convert these to AA and DHA and store sufficient quantities of them for use in pregnancy and lactation, humans have physiological systems to buffer variations in essential fatty acid supplies, and we lack evidence that people eating plant-based diets suffer neurological deficits from “sporadic” essential fatty acid deficiencies. In short, we lack an evidence base for the claim that prehistoric humans required dietary animal flesh to avoid “marginal neurological impairments from sporadic deficits of micronutrients.”

In summary of this section, we lack sufficient evidence for the claim that apoE3 is a specifically ‘meat- adaptive’ gene. Evidence from foraging populations does not support the hypothesis that in prehistoric apes or hominins, apoE3 genotype delayed vascular disease or dementia. In contrast, we have reasonable evidence that chronic parasitic infections both favored a higher frequency of apoE4 and stalled the progression of iron- and lipid-related diseases associated with meat-rich diets. Significant evidence suggests that factors other than meat-eating may favor apoE3 over apoE4, including cooking meat to reduce parasite exposure, and cooking starch-rich USOs and practicing agriculture to stabilize the food supply via a starch-based diet.

CMAH and Neu5Gc Sialic Acid

Neu5Gc is a type of sialic acid produced by non-human mammals, including non-human hominoids (chimps, gorillas, orangutans, and bonobos), but not found in plants. Humans lack the ability to produce Neu5Gc due to mutational deactivation of the CMAH gene that occurred in the human lineage about 2.0-3.0 million years ago, just before emergence of our genus.748

Finch and Stanford believed that deactivation of CMAH was ‘meat-adaptive’ by increasing resistance to zoonotic viral and bacterial pathogens that bind to Neu5Gc on host cell surfaces.749 They knew that “traces of Neu5Gc in human tissues may have dietary origins.”750 Apparently they did not know that once human cells, particularly those epithelial cells lining hollow organs and the endothelium of blood vessels, incorporate dietary Neu5Gc (from mammalian flesh or milk) into cell membranes, the immune system treats this diet-derived Neu5Gc as a foreign antigen, and initiates an inflammatory process in the affected tissues.751

“Thus, although underlying mechanisms exist for many vascular diseases, we suggest that endothelial incorporation of Neu5Gc combines with circulating anti-Neu5Gc antibodies to aggravate processes such as atherosclerosis (81). This Neu5Gc accumulation may facilitate

748 Varki A. Uniquely human evolution of sialic acid genetics and biology. PNAS May 11, 2010; 107(2): 8939-8946.

749 Finch and Stanford, op. cit., 26.

750 Ibid.

751 Varki A. Uniquely human evolution of sialic acid genetics and biology. PNAS May 11, 2010; 107(2): 8939-8946.

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production of anti-Neu5Gc antibodies and further aggravate chronic inflammation in atherosclerosis progression.”752

Through a similar mechanism, dietary Neu5Gc probably promotes other meat-related inflammatory diseases, including cancer. Tumor cells have particularly high concentrations of Neu5Gc, and the incorporation of Neu5Gc into tumor cells may protect the tumor cells from immune-system regulation.753

As with the diseases associated with apoE4, the diseases associated with neu5Gc from mammalian meat “would not have affected natural selection in times past, because they are manifest primarily after the age of peak reproductive fitness.”754

In addition, contrary to Finch and Stanford’s suggestion, the accumulation of dietary Neu5Gc in gut cells may actually increase our susceptibility to pathogens delivered by meat-eating:

“Dietary Neu5Gc loads up epithelial and endothelial cells over time. Subsequent exposure to meat or milk products contaminated with SubAB toxin-expressing Escherichia coli would then allow the toxin to bind to gut epithelium, gain access to the blood stream, and target the kidney endothelium, giving a hemolytic-uremic syndrome (92). The process may be facilitated by the fact that (unlike the cows in which this toxin is usually found) humans do not have circulating Neu5Gc-containing glycoproteins to act as natural toxin inhibitors (92). Thus, we speculate that individuals who consume large amounts of red meat and milk may not only increase their risk for this type of food poisoning but also preprepare their tissues for attack by the toxin (93).”755

Thus, deactivation of CMAH resulted in humans having a specific, heritable, immunological intolerance of one of the basic constituents of mammalian meat and milk, and probably a higher risk of bacterial food poisoning from these foods. Finch and Stanford could not have picked a genetic mutation less supportive of their argument for hypothetical ‘meat adaptive’ genes.

Summary

The fact that apoE3 occurs with a greater frequency among agriculturalists than among hunter-gatherers casts considerable doubt on the claim that apoE3 is a specifically ‘meat-adaptive’ gene. Even if apoE3 genotype does provide some measure of protection against age-related diseases, we have evidence indicating that reductions of parasite loads (largely via cooking), consumption of starch instead of meat, and stabilization of the food supply via agriculture have probably all favored apoE3 over apoE4.

752 Ibid.

753 Ibid.

754 Ibid.

755 Ibid.

MEAT-ADAPTIVE GENES – 251

We probably don’t even need the hypothesis that apoE3 was ‘meat-adaptive’ for ancient humans by delaying susceptibility to diseases caused by dietary fats and cholesterol because a) we have no evidence that apoE genotype affected incidence of these diseases in non-Westernized populations consuming meat-rich diets, and b) parasites obtained by drinking untreated water and meat-eating probably delayed these diseases in foragers by depleting them of fats, cholesterol, and iron.

Since inactivation of the CMAH gene gives humans a specific immunological intolerance of a key component of mammalian flesh, and this probably increases our susceptibility to meat-borne infections and meat-related inflammatory diseases, it does not qualify as a “meat-adaptive” genetic trait. Consequently, even if apoE3 granted many humans some small measure of improved metabolism of the fats and cholesterol in red meat, their immunological intolerance of Neu5Gc would still render them susceptible to meat-related diseases of aging.

Since we have abundant evidence that meat-rich diets promote multiple vascular, immune, and metabolic diseases in humans, any ‘meat-adaptive’ genes we might have clearly do not have a significant impact on these diseases in modern circumstances. At most, these genes delay disease and disability caused or promoted by eating animal flesh. In conclusion, in part due to the CMAH mutation, humans are genetically poorly adapted to consumption of mammal’s meat, regardless of whether any other genes have any minor ‘meat-adaptive’ effects.

252 – HUMAN NUTRITIONAL ADAPTATIONS 19: Science or Science Fiction?

In an interesting paper on the stories of human evolution,756 Landau studied the narratives offered by five individuals considered authorities on human evolution: Arthur Keith, Grafton Elliot Smith, Frederick Wood Jones, Henry Farfield Osborn, and William King Gregory. Landau found that all agreed that human evolution occurred in four main episodes: a shift from arboreal to terrestrial habit; development of upright bipedal posture; development of the brain, intelligence, and language; and development of technology, morals, and society. However, each of the five authors proposed a different sequence for the unfolding of these episodes.

More interesting, Landau found that all five stories conformed to the mythic hero’s journey.

All evolution stories start with our hero, a relatively helpless, humble primate, living a safe existence in the trees. He eventually leaves his forest home, but the authors disagree on the reason for this. Some authors attributed the exodus to a change in the hero (e.g. enlarged brain or bipedalism), while others attributed it to a change in the environment (e.g. climate change destroys his home).

Next comes the journey or adventure. For example, bipedalism gives the hero the power to escape the danger (e.g. starvation) or limits (e.g. arboreal existence) imposed by his former home. Again, the authors do not agree on the reason for or many of the details of this journey.

During this journey, the hero enters a new realm (the savannah) where he must survive a series of tests imposed either by the environment (climate, predators, etc.) or by his own character (burgeoning brain, bipedalism). As in the myths, these tests “bring out the human” in the hominin.

In myths, the hero depends upon some magical agent to master his tests; for example, a cloak, a sword, a ring, or special powers acquired by long training with an enlightened master. Similarly, in human evolution stories, the hero depends on special gifts–e.g. tools, weapons– provided by his almost supernatural intelligence.

To develop and prove his humanity, he undergoes more tests, in the evolutionary story provided by both environment (Ice-Ages) and his own character. Finally, as in many myths where the hero succumbs to pride or hubris, the hero of evolution stories undergoes trials imposed by his own greatest assets (cleverness, civilization) as their overdevelopment comes to threaten his own survival.

The science of human evolution involves a large amount of guesswork and creative imagination, due to the paucity of evidence. Most of us would have difficulty producing an accurate account of what happened in our own lives just five or ten years ago, let alone accurately reconstructing the lifestyle of a stranger from a foreign land who lived 300 years ago without leaving any diaries, only a few piles of garbage here and there. If undertaking the latter task, you would almost inevitably fall into dubious speculations.

756 Landau M. Human Evolution as Narrative. American Scientist 1984;72: 262-68.

253

By pointing to the similarities between human evolution narratives and the mythic hero’s journey, Landau highlights the fiction in stories of human evolution, and suggests that the savannah story may serve someone’s need to have heroic ancestors. In the ‘man the hunter’ story of human origins, we find our ancestors using brain and brawn to overcome obstacles, behead behemoths, and survive against all odds, just as we expect of heroes. Moreover, in this story, man dominates nature and beast, brings bison to his distressed damsel, and conquers the planet. It makes the perfect action story with males saving the day.

In contrast, a story of a largely forest-dwelling frugivore who grows bipedal and big-brained primarily because s/he needs to comprehend, collect, catalogue, cultivate, and consume flowers, fruits, and vegetables; foster extended families; manage complex social relationships; and avoid violent confrontations except in co-operative self-defense just wouldn’t have the same thrilling, male-ego- stroking appeal as the usual evolution stories which depict ‘man’ as a sort of action hero.

So far, Darwinians have constructed their stories of human evolution on very sparse and highly biased archaeological evidence. Since stones and bones are much more likely to survive for millions of years than anything made from plant fibers, we really have no idea where the story started, and we have less than two dozen incomplete specimens of H. erectus and H. habilis to represent more than 2 million years of human experience, it seems inevitable that any story of human evolution based on archaeological evidence will include more fiction than fact.

The currently dominant theories of human origins assume that humans have become more neurologically healthy and intelligent by route of hunting and flesh consumption. Yet the fossil record does not give us that information; it simply provides evidence that some ancient humans did eat flesh (including, apparently, the flesh of human children and adolescents757) at some space-time locations. Whether this promoted or retarded development of human health and intelligence remains a question for further examination. As I have argued in this book, the only way to answer this question is to study the effects of meat-eating on modern humans. The evidence I have presented supports the hypothesis that human evolution was powered by a plant-based diet based on cooked and raw botanical fruits and roots.

Moving Beyond Carnism

As I discussed in the Introduction of this book, if you grew up eating animal flesh, and continue to do so, and most of the people around you do the same, your mind will naturally gravitate to the belief that eating animal flesh is normal, natural, and, consequently, necessary. If your mother, father, or other caregivers told you, at an early age, that you must eat animal flesh to be healthy, big, and strong, this cultic conditioning will unconsciously influence your adult mind as you interpret evidence and your experience. If you have an emotional (familial or social sentiments) or commercial interest in continuing the habit of eating animal flesh, your mind will seek out justification for this habit; it will habitually interpret evidence and your personal experience as support for the habit.

757 Owen J. Human Meat Just Another Meal for Early Europeans? National Geographic News 2010 Aug 31.

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While many humans conduct their lives as omnivores and fervently believe that they biologically require at least some dietary animal flesh, these individuals simply do not have an evidence-based understanding of human physiology. At the present time, their belief stands on par with those individuals who believe that the Earth is flat. While in everyday experience, the Earth’s surface certainly does appear to be flat, a limited perspective creates this illusion. Similarly, while the fact that many humans do eat animal flesh today and have eaten flesh for millennia certainly generates the appearance that humans “are” obligate carnivores, this may be an illusion that arises from a limited perspective that may have its origins in childhood conditioning.

As already mentioned, psychologist Melanie Joy has coined the term carnism to refer to the belief that eating some animals (but not all) is normal, natural, and necessary.758 Until you understand the fundamentally fallacious nature of carnism, you will continue to view the world through the carnist lens.

Scientists influenced by carnism will tend to filter all evidence through their preconception of the importance of animal flesh in human nutrition. I suggest that this may account for the central place the “meat made us human” has taken among anthropologists attempting to give a Darwinian account of human origins. To repeat, if your parents and culture raise you with emotionally charged admonitions that you must eat meat to achieve health and adulthood, you will almost certainly believe in adulthood that “meat makes us human” and may attempt to prove or support this ideology in your quest to understand human origins. A Darwinian unaware of his carnistic conditioning may not even imagine, let alone entertain, the possibility that meat-eating played only an accidental, not a unique or essential role in human evolution, let alone the possibility that it constitutes a pathology rather than an evolutionary advancement.

I hope that this book has helped free you from bondage to carnism, so that you can think outside the limits this ideology places upon you.

758 Joy M. Why We Love Dogs, Eat Pigs, and Wear Cows. Conari Press, 2011.

SCIENCE, OR SCIENCE FICTION? – 255

Part III: Appendices & Bibliography

257

Appendix A: Essential Nutrients

At the time of this writing, after more than 100 years of nutrition research, we have no evidence that humans have a dietary requirement for any nutrient uniquely provided by animal sources. We appear to have a physiology adapted to a diet consisting primarily of fruits, vegetables, seeds, and nuts. Eaten in adequate variety and quantity, with the addition of some vitamin B12 produced by microbes (plentiful on wild fruits and vegetables and in wild water sources), and regular sunlight exposure, such a diet supplies all the nutrients presently known to be required for health and fitness.

TABLE A.1: ORIGINAL SOURCES OF ALL NUTRIENTS KNOWN ESSENTIAL IN HUMAN DIETS Nutrient Original Food Source(s) Essential amino acids (9) Plants Linoleic acid Plants Linolenic acid Plants Glucose Plants ß-carotene (provitamin A) Plants Tocopherols (vitamin E) Plants Cholecalciferol (vitamin D3) Sunlight Phylloquinone (vitamin K) Plants Thiamine (B1) Plants and microbes Riboflavin (B2) Plants and microbes Niacin (B3) Plants Pantothenic acid (B5) Plants and microbes Pyridoxine (B6) Plants and microbes Folate Plants and microbes Cobalamin (B12) Microbes Ascorbic acid (vitamin C) Plants Minerals Earth, water, plants

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Appendix B: A Whole Foods Plant-Based Diet

The following table displays the principal foods of a whole foods plant-based diet.

Table B.1: Principal Foods For A Whole Food Plant-Based Diet

Category Subcategory Examples

Botanical fruits, Fleshy fruits apple, banana, berries, cherries, cucumbers, durian, eggplants, carbohydrate-rich, jackfruit, kiwi, mangos, melons, okra, oranges, papaya, peach, fleshy and dry pineapples, pumpkin, sweet peppers (red, green, yellow), tomatoes, winter squash, watermelon, zucchini, and others

Legumes beans (various, fresh and dried), lentils, peas (fresh and dried)

Grains and seeds, amaranth, barley, buckwheat, corn, kamut, millet, quinoa, rice, rye, whole spelt, teff, wheat

Nuts chestnut

Vegetables Flowers broccoli, cauliflower, many others

Stems and leaves arugula, asparagus, bok choy, brussels sprouts, cabbage, celery, chard, collards, kale, lettuce (various), mustard, spinach, tat soi, etc.

Bulbs, roots, and beets, burdock, carrot, onion, radish, rutabaga, sweet potato, turnip, tubers white potato

Marine algae alaria, dulse, hijiki, kelp/kombu, laver/nori, sea palm, wakame, etc.

Fungi Mushrooms button, bella, cremini, protabella, shiitake, oyster

Yeast wild yeasts (naturally occur on fresh fruits), nutritional yeast

Botanical fruits, fat- Fleshy fruits avocado, olive rich, fleshy and dry Legumes peanuts

Seeds flax, hemp, sesame, sunflower, pumpkin

Nuts almonds, brazil nuts, filberts, cashews, pecans, walnuts

Micronutrients Sun exposure vitamin D

Microbial products vitamin B12 supplements

Minerals salt or other mineral supplements as necessary

Processing plant foods to remove fiber or concentrate macronutrients (sugar, starch, fat, or protein) generally produces a potentially harmful food. Consequently, I generally suggest minimizing your consumption of refined plant products to less than 2 percent of your total energy (kcalorie) intake if you are healthy and lean, and to less than 1 percent if you have excess body fat or other health issues. In

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addition, as discussed in the text, humans have no clear biological adaptation to or nutritional requirement for any type of animal flesh, egg, or milk; and a large body of evidence (not thoroughly discussed in this book) indicates that consumption of even small amounts of animal foods promotes many human diseases.759 The following table displays foods that I recommend you minimize or avoid.

Table B2: Items to avoid or minimize (no more than 5 percent of your total energy intake if lean and healthy)

Minimize

Category Subcategory Examples

Refined plant Refined white rice, refined wheat products, corn starch, refined sugar products carbohydrates

Refined fats and oils from coconut, palm, olive, sesame, corn, canola, soy, flax, oils hemp, almonds, etc.

Refined plant texturized vegetable protein (TVP); protein powders from soy, proteins peas, rice, hemp, etc.

Alcohol wine, beer, spirits

Avoid

Animal flesh beef, pork, lamb, bison, game meat, chicken, turkey, duck, lard, tallow, all fish, shellfish

Eggs chicken eggs, duck eggs, fish eggs, etc.

Milk products milk, butter, cheese, yogurt, cream, whey, etc.

In general, I recommend emphasizing consumption of carbohydrate-rich botanical fruits, and to include intake of fat-rich botanical fruits as follows: nuts and seeds, 1 to 2 ounces (30 to 60 g) daily; avocados, one-half to one whole daily. Whole olives supply only 3 g fat per ounce but have a high sodium content so I recommend using them only as a seasoning.

I recommend including some fat-rich plant foods in your daily diet. We need dietary fat to fully absorb pro-vitamin A carotenoids, lutein, lycopene, and other fat-soluble nutrients. Nuts, seeds, and avocados also provide vitamin E, minerals, and cholesterol-reducing phytosterols. As discussed in Chapter 16, research led by David Jenkins has shown that a “simian” diet that excludes oils but provides about 25% of energy from fat-rich whole plant foods, principally almonds, can reduce total cholesterol and LDL to less than 150 and 80 mg/dL, respectively, levels known to allow reversal of atherosclerosis.

You do not need to avoid all fat-rich whole foods to achieve maximum sports performance or a negative fat balance and body fat loss. The American College of Sports Medicine has stated that athletes do not

759 Campbell TC and Campbell TM. The China Study. Benbella Books, 2006. Also see www.nutritionfacts.org, or www.drmcdougall.com/medical_ailments.html .

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benefit from diets providing less than 20% of energy from fat. Fat loss requires a negative energy balance; diets lacking adequate fats may lead some people to overeat low-fat foods in an attempt to satisfy their taste for fat. Inclusion of a small amount of fat-rich whole plant foods as defined above will make your whole foods plant-based diet much more nutritious, enjoyable and sustainable.

In practice, base your diet on low-fat botanical fruits and vegetables, and use high-fat fruits as condiments and dressings for the low-fat fare. For example:

• Breakfast • Very large bowl of mixed fresh fruit (at least 3 to 4 whole fruits) with 3 cups of fresh spinach, a sprinkle of chopped walnuts, whole grain cereal, and a cup of unsweetened soy milk. • Large bowl of rolled oats topped with chopped almonds, several fresh fruits and plant-based milk. • Lunch • Green pea guacamole, sweet peppers, tomatoes, cucumbers, celery, and collard leaves, all rolled up in a whole grain tortilla, with oranges or apples. • Sandwiches made of sprouted grain bread topped with low-fat hummus, tomatoes, lettuce, roasted onion, and a thin spread of avocado, plus fresh fruits. • Supper • Whole wheat pasta topped with low fat, low sodium marinara, along with a large salad of kale, tomato, cucumber, and sweet pepper and a lemon-tofu dressing. • Very large mixed green salad dressed with a blend of orange juice and avocado, vegetable lentil soup, and fresh corn on cob. • Large kale salad with a lemon-tahini dressing, black bean soup, and baked sweet potatoes. • Fresh baked potatoes topped with chili beans (non-carne) and a very large green salad dressed with avocado and garlic.

For more detailed suggestions and guidance for implementation of a plant-based diet, obtain a copy of Make Every Bite Count!, a guidebook written by my wife, Tracy Minton.

Supplements

Contrary to popular belief, animal-based diets tend to lack certain nutrients unless fortified or supplemented. For example:

• In the early 20th century in the US, goitre from iodine deficiency prevailed in the Great Lakes and Pacific Northwest regions, despite widespread consumption of animal flesh, eggs, and dairy products. Since 1924, omnivores have been using salt fortified (supplemented) with iodine to prevent this deficiency.760

760 Food and Nutrition Board, Institute of Medicine. Dietary Reference Intakes: Guiding Principles for Nutrition Labeling and Fortification (2003). National Academies Press, 2003. 224.

A WHOLE FOODS PLANT-BASED DIET – 263

• In the 1930s and 1940s, despite widespread consumption of animal foods, scientists identified specific vitamin and mineral deficiency disease syndromes in the United states, so in 1940 the Food and Nutrition Board of the National Academies of Science recommended the addition of thiamin (B1), niacin (B3), riboflavin (B2), and iron to flour, which continues to this day.761 Notably, deficiencies of these nutrients were prevalent due to reliance on refined grains and inadequate intakes of whole fruits and vegetables, despite the fact that people regularly consumed animal flesh.

• According to the CDC, about 9%–16% of US females aged 12–49 years of age exhibit iron deficiency.762 The incidence of iron-deficiency in vegetarians does not differ significantly from that of nonvegetarians763 so eating meat and fortified grain products does not appear to provide better protection from iron deficiency. It must be remembered that iron deficiency arises from inadequate consumption of iron-rich foods, not specifically from avoidance of animal flesh.

• Due to widespread vitamin D deﬁciency in the general population, milk producers started fortifying dairy products with vitamin D in 1933.764 Nevertheless, in 2010, according to the NHANES, “The overall prevalence rate of vitamin D deﬁciency [in the USA] was 41.6%, with the highest rate seen in blacks (82.1%), followed by Hispanics (69.2%).” 765

• As discussed in Chapter 14, Tufts University and the USDA have reported that about 40 percent of U.S. citizens, the vast majority of whom eat meat daily, may have some degree of vitamin B12 deﬁciency.

A plant-based diet with sufficient daily intake of fruits, green leafy and sea vegetables, and legumes will easily meet all recommended nutrient intakes. However, due to modern hygiene destroying microbes that produce vitamin B12 and insufﬁcient sun exposure, probably all modern people eating plant-based diets will need to supplement one or both of these nutrients at some time.

Some people incorrectly believe that no nonhuman wild species requires or uses dietary supplements. In fact, nonhuman species suffering nutritional shortages will go out of their way to consume unusual items that we can only consider supplements to their regular foods. For example:

761 Ibid.

762 Centers For Disease Control. Iron Deficiency in the United States, 1999-2000. MMWR Weekly, October 11, 2002 / 51(40);897-899.

763 Craig WJ. Iron Status of Vegetarians. Am J Clin Nutr 1994 May;59(5):1233S-1237S.

764 Food and Nutrition Board, Institute of Medicine. Dietary Reference Intakes: Guiding Principles for Nutrition Labeling and Fortification (2003). National Academies Press, 2003. 224.

765 Forrest KY, Stuhldreher WL. Prevalence and correlates of vitamin D deficiency in US adults. Nutr Res 2011 Jan;31(1): 48-54.

264 – APPENDICES & BIBLIOGRAPHY

• Herbivorous deer requiring additional calcium or phosphorus to support antler growth will chew on cast-off antlers, eat soil surrounding decayed bones, lick rocks, and drink brackish water to obtain the minerals, if the plants they normally consume do not provide enough.766

• When deﬁcient in sodium, African buffaloes will lick salt-encrusted plants, rocks, and other sweaty buffaloes.767

• Wherever possible, herbivores seek out bogs, marshes, and rivers for aquatic plants that contain more sodium and other minerals than the land plants on which they primarily feed.768

• A biologist witnessed a herd of cattle crowding around a tree and licking its bark; she found that the tree had one copper nail embedded in the bark where the cattle had focused their attention––and that the cattle had a copper deﬁciency.769

These examples show that natural selection has favored the survival of individuals who can detect when their habitual food lacks sufﬁcient nutrients and ﬁnd alternative sources for those nutrients. If it is important to you, you can now say that using supplements is “natural.” Several of these examples also show that nonhuman animals will use non-organic sources of minerals (e.g. rocks, soil, metals) whenever necessary; unlike some humans, they do not erroneously believe that only minerals embedded in plant or animal tissues can serve as vital nutrient sources. Fortunately, we have cleaner, safer mineral supplements manufactured according to the standards set by the U.S. Pharmacopeia.

Regarding calcium, even though low intakes of total animal protein and adequate vitamin D status may reduce calcium requirements,770 I recommend that people eating plant-based diets aim for calcium intakes of at least 800 mg per day as a minimum, since this seems to represent the minimal short-term human requirement for calcium,771 and the calcium intakes of wild leaf-eating primates far exceed this.772

Elephants consume a strictly plant-based diet. Adult male elephants weigh between 1,800 and 4,500 kg, and females slightly less. They build very large skeletons and have large calcium requirements which vary with sex and stage of life.

766 Engel C. Wild Health: Lessons in Natural Wellness from the Animal Kingdom. Houghton Mifflin Harcourt, 2003. 29.

767 Ibid., 32.

768 Ibid.

769 Ibid., 34.

770 Nordin BEC. Calcium requirement is a sliding scale. Am J Clin Nutr 2000;71(6):1381-83.

771 Hunt CD and Johnson LK. Calcium requirements: new estimations for men and women by cross-sectional statistical analyses of calcium balance data from metabolic studies. Am J Clin Nutr 2007 Oct;86(4):1054-63.

772 Milton K. Nutritional characteristics of wild primate foods. Nutrition 1999;15 (6):488-98.

A WHOLE FOODS PLANT-BASED DIET – 265

“Calcium requirements of 8-9 g/day have been determined for tusk growth in male elephants, and up to 60 g of calcium daily has been estimated as necessary for a lactating cow to meet the growth needs of her calf.”773

Like wild non-human primates, elephants meet their calcium requirements primarily by consuming green leafy vegetation. I recommend that you adopt this practice yourself, focussing particularly on cabbage-family greens. One cup of raw kale, collards, or bok choy provides 75 to 100 mg calcium. I recommend consuming 4 to 8 cups of one of these vegetables every day.

Table B.3 lists the nutrients of frequent concern in human nutrition, food sources, and additional information. Generally, whole foods plant-based diets containing adequate green and yellow-orange vegetables and fresh fruits generously provide all essential nutrients. In fact, such diets tend to have a much greater nutrient density than animal-based diets. However, in response to the widespread misconception that plant-based diets do not provide adequate amounts of certain nutrients, I have provided this chart primarily to show where we can ﬁnd the nutrients of common concern in adequate concentrations to meet human needs.

Table B.3: Nutrients Of Common Concern In Plant-Based Diets.

Nutrient Non-animal Additional Information Recommendations (Requirement/ Modern Sources day)

Omega-3 Green leafy Deficiency increases the risk of Eat at least three cups of raw or Alpha-linolenic vegetables, flax inflammation and blood clotting two cups of cooked dark leafy acid (1.5 g/d) seed, hemp seed, leading to cardiovascular disease greens every day, or use ground walnuts whole flax seed daily (1 tablespoon).

Vitamin B12 (2 None reliable Deficiency increases risk of Supplementation mandatory due to mcg) neurological and cardiovascular unreliability of food sources. Use diseases B12-fortified nutritional yeast and plant milks daily. Take 1000 to 2000 mcg B12 supplement once weekly.

Vitamin D Sun exposure (10 Deficiency increases risk of bone Get sensible summer sun exposure (400-600 IU) a.m. to 2 p.m. diseases and may increase risk of without sunscreen when possible. several times cancer and heart disease. RDI is Have levels checked; supplement if weekly without probably too low; research has deficiency found or if you avoid or sunscreen, at shown that we need about 4000 IU get insufficient sun exposure, least 20% of skin daily to maintain blood levels particularly in winter. exposed, 20 similar to daily sun exposure. minutes) Winter sun does not stimulate D production in skin. Sunscreen may block formation of vitamin D.

773 Fowler ME, Mikota SK. Biology, Medicine, and Surgery of Elephants. John Wiley and Sons, 2006. 60.

266 – APPENDICES & BIBLIOGRAPHY

Table B.3: Nutrients Of Common Concern In Plant-Based Diets.

Nutrient Non-animal Additional Information Recommendations (Requirement/ Modern Sources day)

Vitamin E (15 Whole grains, Deficiency increases risk of Monitor your intake. Consume mg) legumes, nuts, cardiovascular and neurological beans and greens daily. Eat up to 1 seeds, avocados, diseases and cancers. ounce of whole nuts or seeds or green leafy half an avocado daily. Minimize or vegetables avoid extracted oils.

Calcium (800 Cruciferous Chronic deficiency may reduce Eat at least 4 cups raw or 2 cups mg) green leafy bone mass and increase risk of cooked greens daily; have calcium- vegetables (kale, colon cancer. Excess supplemental rich tofu or fortified foods several collards, bok calcium may cause constipation, times weekly. choy); dark green increases the risk of urinary stone leaf lettuces; formation and kidney dysfunction, fortified foods and may also increase the risk of (e.g. soy milk); cardiovascular disease. tofu made with calcium; blackstrap molasses

Iron (women 18 Green leafy Deficiency causes anemia, Consume leafy greens, legumes, or mg, men 10 mg) vegetables, impairing physical and mental whole grains daily. If you have legumes, grains. performance and cold tolerance. symptoms of anemia, get tested for Excess increases risk of heart deficiency. If deficient, increase disease, cancer, diabetes, immune intake of greens and beans, and eat disorders, birth defects, dementia. iron-rich foods with foods rich in vitamin C and organic acids.

Zinc (men 11 Pumpkin seeds, Deficiency causes loss of sense of Eat legumes daily and pumpkin mg, women 9 legumes, grains, taste, impairs immune system, seeds several times weekly. mg) greens slows wound healing; men lose zinc in ejaculation.

Selenium (55 Whole wheat, Deficiency increases the risk of Eat nutritional yeast, whole wheat, mcg) nutritional yeast, heart disease, cancer, and or one whole brazil nut daily. brazil nuts hypothyroidism; one brazil nut or three ounces of whole wheat pasta (dry) or bread supplies full requirement.

Iodine (150 Sea vegetables, Deficiency causes hypothyroid in Consume sea vegetables several mcg; 220 mcg iodized salt adults and cretinism in children times weekly, or use iodized salt pregnancy; 290 daily. mcg lactation)

A WHOLE FOODS PLANT-BASED DIET – 267

Appendix C: Proposed Human Ancestors

Contrary to impressions given by some proponents of animal-based diets, there exist within paleoanthropology important questions about proposed human ancestors and accounts of human evolution, which could markedly change ideas about the role of food in human evolution.

Was The Alleged Last Common Ancestor Chimpanzee-like?

Loren Cordain, Ph.D., author of The Paleo Diet, as well as other advocates of “paleo” and low- carbohydrate diets have suggested that the fact that some chimpanzees eat some meat serves as evidence that humans require an animal-based diet.774 However, we have reasons to doubt the idea that human ancestors resembled living chimpanzees.

According to the Darwinian account, chimpanzees and hominins both descended from the last common ancestor (LCA), a Miocene ape, at least 6 million years ago. Since the Darwinian account proposes that both lineages started with similar genetic material (obtained from the common ancestor) and simultaneously inhabited Africa for 6 million years, it would seem very likely that both were exposed to similar stimulants for and amounts of random genetic mutation as well as natural selection. In other words, unless the chimpanzee lineage has been isolated from evolution by natural selection, living chimpanzees very likely differ significantly from the LCA.

Curiously, the current account of evolution seems often to propose that during the 6 million years since the LCA, random mutations and natural selection of the genetic material of the human lineage resulted in a dramatic evolutionary transformation, while the great ape lineages showed nowhere near as much variation and transformation, despite having a common genetic starting point and evolving through the same time period and climatic changes. Since evolution is allegedly caused by natural selection of beneficial genetic mutations, but beneficial mutations are quite rare (estimated at 1/1000), what explains (i.e. what caused) the apparently greater occurrence of both dramatic and beneficial random genetic mutations in the human lineage in comparison to the other great ape lineages? Changes in diet and lifestyle do not cause the type of genetic mutations involved.

Pickford has noted nine characteristics of extant chimpanzees that differ from those of Miocene apes and humans (Table C.1) which “raise difficulties for the hypothesis that the last common ancestor of African apes and humans looked like a chimpanzee, in that interposing a chimp-like ancestor between Miocene apes and humans would mean that several evolutionary reversals would have to occur.”775 Chimpanzees have incisor/molar proportions that “fall way off the hominoid regression (Pickford, 2004), indicating

774 Cordain L. The Evolutionary Basis for the Therapeutic Effects of High Protein Diets. In: The Protein Debate. Performance Menu: Journal of Nutrition and Athletic Excellence. Page 7. Retrieved Oct 29, 2013 from http://www.catalystathletics.com/ articles/downloads/proteinDebate.pdf

775 Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis:Perspectives on Hominin Evolution. Cambridge University Press, 2012. 110. http://books.google.com/books?id=PrJ1lmjMakoCandpg=PA116#v=onepageandqandf=false

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that the genus Pan is highly specialized in this respect and thus not a good model for the common ancestor of extant African apes and humans.”776

Simply put, Pickford suggests that modern chimpanzees may not resemble the last common ancestor of humans and chimpanzees because modern chimpanzees have features that he thinks arose as a result of random mutations and natural selection occurring during the 6 my that have passed since the last common ancestor passed on to the two lineages similar genetic material.

Table C.1: Summary of derived features of chimpanzees (genus Pan) suggesting that they are not a good model for the last common ancestor of hominids and African apes.

Morphology Miocene apes Pan Homo

Splanchnocranium short elongated shortened

Incisor/molar proportions within hominoid variation outside hominoid within hominoid variation variation

Molar wear gradient marked weak marked

Dentine penetrance in low high low molars

Molar enamel thickness thick thin thick

Molar occlusal basins small capacious small

Canine crowns low high (in males) low

Diastema absent present absent

Femoral platymeria present absent present

Source: Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis: Perspectives on Hominin Evolution. Cambridge University Press, 2012. 110.

Grehan and Schwartz have adduced evidence suggesting that humans may be more closely related to orangutans than to chimpanzees.777

“Schwartz and Grehan scrutinized the hundreds of physical characteristics often cited as evidence of evolutionary relationships among humans and other great apes––chimps, gorillas, and orangutans––and selected 63 that could be verified as unique within this group (i.e., they do not appear in other primates). Of these features, the analysis found that humans shared 28 unique physical characteristics with orangutans, compared to only two features with chimpanzees, seven

776 Ibid., 116.

777 Grehan JR, Schwartz JH. Evolution of the second orangutan: phylogeny and biogeography of hominid origins. J. Biogeogr 2009; 36:1823–184

270 – APPENDICES & BIBLIOGRAPHY

with gorillas, and seven with all three apes (chimpanzees, gorillas, and orangutans). Gorillas and chimpanzees shared 11 unique characteristics.

“Schwartz and Grehan then examined 56 features uniquely shared among modern humans, fossil hominids—ancestral humans such as Australopithecus—and fossil apes. They found that orangutans shared eight features with early humans and Australopithecus and seven with Australopithecus alone. The occurrence of orangutan features in Australopithecus contradicts the expectation generated by DNA analysis that ancestral humans should have chimpanzee similarities, Schwartz and Grehan write. Chimpanzees and gorillas were found to share only those features found in all great apes.”778

Humans and orangutans share 97 percent of their DNA sequence.779 Some parts of the human genome resemble the orangutan genome more closely than the chimp genome.780 Features present in both humans and orangutans but absent from other apes include thickly enameled molar teeth with flat surfaces, greater asymmetries between the left and right side of the brain, an increased cartilage-to-bone ratio in the forearm, similarly shaped shoulder blades, a hole in the roof of the mouth, widely spaced mammary glands, growing long hair, and a defined hairline.781 As discussed in Chapter 17, orangutans also outperform chimpanzees on some intelligence tests.

Thorpe et al.782 have argued that hominin bipedalism evolved from hand-assisted bipedalism of a common ancestor of humans and the orangutan. Thorpe et al. point out that orangutans in a bipedal stance have full hip and knee extension, like humans, whereas chimpanzees do not.

Schwartz and Grehan have enumerated at least four flaws in the assumption that allegedly closer matches of DNA between humans and chimps than between humans and orangutans ‘prove’ that humans and chimps are more closely related than humans and orangutans. In particular, geneticists’ claims of 99 percent similarity between chimp and human DNA sequences refer only to a small portion of the 2 to 3 percent of the genome that codes for metabolically active proteins, which may reflect adaptation to similar environmental circumstances, not common descent. Further, they point out that the two species can possess identical genes, without identical function of those genes; for example, although both chimpanzees and humans possess a FOXP2 gene, it functions differently in human and chimpanzee development, probably due to differences in DNA regulatory sequences that comprise much of the other

778 University of Pittsburgh (2009, June 18). Humans More Related To Orangutans Than Chimps, Study Suggests. ScienceDaily. Retrieved September 25, 2013, from http://www.sciencedaily.com/releases/2009/06/090618084304.htm

779 Spencer G. NIH-funded scientists publish orangutan genome sequence. NIH News 2011 January 26.

780 Cold Spring Harbor Laboratory (2011, January 26). Genetic archaeology finds parts of human genome more closely related to orangutans than chimps. ScienceDaily. Retrieved September 19, 2013, from http://www.sciencedaily.com/releases/ 2011/01/110126131548.htm

781 Owen J. Orangutans May Be Closest Human Relatives, Not Chimps. National Geographic News 2009 June 23. Retrieved September 25, 2013, from http://news.nationalgeographic.com/news/2009/06/090623-humans-chimps-related.html

782 Thorpe SKS, Holder RL, Crompton RH. Origin of Human Bipedalism as an Adaptation for Locomotion on Flexible Branches. Science 2007 June 1;316(5829):1328-1331.

PROPOSED HUMAN ANCESTORS – 271

98 percent of the genome and affect when and where FOXP2 gets expressed. In short, Schwartz and Grehan believe that the evolution of human-ape relationships remains open for investigation.783

Assuming that Homo descended from australopithecines, Hawks points out that “orangutans may make a better model for early hominin jaw mechanics than chimpanzees do, because the sizes of jaw musculature and teeth are more comparable. Neither orangutans nor australopithecines have teeth that look well-made for reducing fibrous, tough meat into smaller pieces.”784

Rewriting the evolution story to depict human ancestors as more like orangutans than like chimps might change ideas about ancestral diets. Orangutans consume a diet consisting primarily of fruit, leaves, bark, insects, and small vines, with ripe fruit forming 61% of their diet on average (a higher proportion than chimps).785 Orangutans always prefer eating fruits, but depend more heavily on other plant foods such as bark, pith, leaves, and flowers, and to a lesser extent insects, when fruit is in short supply; and they share with humans a tendency to overeat during times of food abundance, and an efficiency of storing fat reserves, resulting in obesity in captivity.786

As for hunting, according to Hardus et al.:

“Researchers have observed several cases of meat-eating in wild Sumatran orangutans, although not in Bornean orangutans (Pongo pygmeus: Russon et al. 2009). However, meat-eating is rare at the Sumatran orangutan sites where this behavior has been observed despite numerous observation hours (van Schaik et al. 2003).”787

Hardus et al. report a total of 9 cases of meat-eating in orangutans, and found that these occurred only when ripe fruit was in short supply. Only five individual orangutans have been observed hunting. Hawks summarizes the Hardus et al. findings thus:

“They hunt slow lorises, the practice is rare, it occurs at times when their other preferred goods are scarce, some individuals hunt but most don’t.” 788

783 Schwartz JH, Grehan JR. Evolution of human-ape relationships remains open for investigation. J Biogeogr 2011;38:2397-2404.

784 Hawks J. Orangutan loris capture and meat-eating. John Hawks Weblog 2012 Jan 20. Retrieved Oct 29, 2013 from http:// johnhawks.net/weblog/reviews/behavior/orangutans/orang-hunting-hardus-2012.html#ref1

785 Galdikas BMF. Orangutan Diet, Range, and Activity at Tanjung Puting, Central Borneo. Int J Primatol 1988;9(1): 1-35.

786 Cawthon Lang KA. 2005 June 13. Primate Factsheets: Orangutan (Pongo) Taxonomy, Morphology, and Ecology . Accessed October 29, 2013 from .

787 Hardus ME, Lameira AR, Zulfa A, et al.. Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii). Int J Primatol 2012;33:287-304.

788 Hawks J. Orangutan loris capture and meat-eating. John Hawks Weblog 2012 Jan 20. Retrieved Oct 29, 2013 from http:// johnhawks.net/weblog/reviews/behavior/orangutans/orang-hunting-hardus-2012.html#ref1

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Thus, among orangutans, very few individuals eat meat, those individuals do it only very rarely in response to short fruit supplies, and even then, meat is a filler fall-back food, not a staple fall-back food, whereas among chimpanzees, meat-eating occurs more frequently, primarily when fruit supplies are abundant and they can afford to spend the extra energy involved in arboreal pursuit of monkeys.789

If as the quoted experts suggest orangutans provide a better model of human ancestors than chimpanzees, this suggests a far different role for meat-eating in the alleged hominid evolution.

With all this in mind, we can’t be certain that chimpanzee behaviors reliably serve as a very useful analog for any alleged early human ancestor. Consequently, the fact that some chimpanzees do some hunting (see Appendix D) probably does not provide us with good evidence to support the claim that humans have a genetic requirement for an animal-based “paleo” or low-carbohydrate diet.

Orrorin tugenensis

Most accounts of the alleged ancient human lineage start with the apparently bipedal Australopithecus species (e.g. see Tattersall and Schwartz790). However, in 2000, Pickford and Senut791 reported finding remains of a species dubbed Orrorin tugenensis dated to about 6 mya. The specimens include 20 fossils representing at least 5 individuals, including a jaw fragment, teeth and bones of extremities, but no skulls.

Galik et al. examined the best-preserved femur in the Orrorin collection, and determined that the internal and external structure of these bones differs from that of quadrupedal African apes, and provides evidence for frequent bipedal posture and locomotion in this Late Miocene species.792 This means Orrorin may have had bipedal locomotion about 4 million years before the earliest fossils assigned to the human genus. However, Wood and Harrison maintain that Orrorin’s femur features “are also as likely to be functionally and behaviourally associated with arboreal above-branch and terrestrial quadrupedalism as they are with bipedalism.”793

Orrorin’s femur and humerus appear to measure about 1.5 times longer than those of the A. afarensis specimen dubbed Lucy, which suggests an estimated body size larger than afarensis and similar to a modern female chimpanzee or even a small woman, i.e. 30 to 50 kg. Orrorin had small teeth (microdontia), canines with low crowns, and molars with thick enamel, all features in common with hominins and distinct from chimpanzees and Australopithecus species. The jaw fragment suggests that

789 Hardus ME, Lameira AR, Zulfa A, et al.. Op. cit..

790 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92.

791 Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis:Perspectives on Hominin Evolution. Cambridge University Press, 2012. 110.

792 Galik K, Senut B, Pickford M, et al.. External and Internal Morphology of the BAR 1002’00 Orrorin tugenensis Femur. Science 2004 Sept 3;305(5689):1450-1453.

793 Wood B, Harrison T. The evolutionary context of the first hominins. Nature 2011 Feb 16;470(7334): 347-352.

PROPOSED HUMAN ANCESTORS – 273

Orrorin had a short face, whereas Australopithecus had a long face. In dental, facial, manual, and locomotive features, Orrorin apparently had more features in common with modern humans than did any Australopithecus species, and inserting the latter between Orrorin and Homo would involve several highly unlikely evolutionary reversals. The Orrorin fossils may cast doubt on allegations that humans descended from Australopithecus species (Table C.2).

Table C.2: Summary of evolutionary reversals that arise by inserting australopithecines between Orrorin and Homo.

Morphology Orrorin Australopithecus Homo

Molar/body size ratio microdont megadont microdont

Incisor/molar proportions on hominoid regression above hominoid on and slightly below regression hominoid regression

Terminal thumb phalanx human-like extremely spatulate human-like

Femoral head orientation human-like posterior twist human-like

Lesser trochanter medial posterior medial orientation

Source: Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis:Perspectives on Hominin Evolution. Cambridge University Press, 2012. 107.

Of interest to those who think that small teeth (microdontia) unequivocally indicates adaptation to a meat-based diet, paleoanthropologists believe that the small, low-crowned canine teeth and rounded molars of Orrorin indicate adaptation to a plant-based diet consisting of fruit, leaves, seeds, roots, and nuts.794 If an evolutionary account of human origins eventually includes Orrorin, this would probably exclude Australopithecus, and it would follow that humans did not acquire small teeth as an adaptation to eating animal flesh, contrary to the claims of some authors. This illustrates how a single fossil find could invalidate any argument for specific human adaptations to an animal-based diet based on fossil evidence.

At the very least, the Orrorin fossils show the folly of attempting to identify one-to-one relationships between specific, isolated anatomical features (e.g. microdontia) and diet based on limited fossil evidence.

Orrorin may also challenge the hypothesis that bipedalism and other hominin features (such as microdontia) arose as adaptations to roaming an arid grassland searching for wild game. Archaeologists found the Orrorin fossils in association with fossils of fauna and flora indicating that Orrorin occupied a

794 Smithsonian National Museum of Natural History. What does it mean to be human? Orrorin tugenensis: How They Survived. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/orrorin-tugenensis .

274 – APPENDICES & BIBLIOGRAPHY

forested, lakeside environment subjected to a mean annual rainfall of about 1200 mm, probably with two short dry seasons rather than one long one.795

Although similar to humans, none of Orrorin’s features necessarily imply that Orrorin belongs to the alleged human lineage. According to Wood and Harrison, another fossil ape from Italy dubbed Oreopithecus bambolii and dated to 7 to 8 mya also shares many similarities with alleged human ancestors, including some skeletal features that suggested that it may have had the ability to walk on two legs. However, we know enough about its anatomy to classify it as a fossil ape “that is only distantly related to humans, and that it acquired many ‘human-like’ features in parallel.”796 In 2013, Russo and Shapiro reported that an analysis of the lumbosacral region of Oreopithecus does not exhibit adaptations for lumbar lordosis or habitual bipedal locomotion.797 If Orrorin’s human-like features receive further confirmation, it still remains possible that Orrorin belongs to an extinct bipedal species having many human-like features but not ancestral to humans.

As a general lesson from this, Wood and Harrison note that the type of data provided by the fossil record, consisting primarily of skulls and teeth, seems particularly prone to display homoplasy: shared features that don’t necessarily indicate shared ancestry. In their words:

“The relationships among the living apes and modern humans have effectively been resolved, but it is much more difficult to locate fossil apes on the tree of life because shared skeletal morphology does not always mean shared recent evolutionary history. Sorting fossil taxa into those that belong on the branch of the tree of life that leads to modern humans from those that belong on other closely related branches is a considerable challenge.”798

Australopithecus

Most accounts of alleged human evolution begin with several Australopithecus species bridging part of the gap between the LCA and the first proposed members of the Homo genus: A. anamensis, A. afarensis, and A. africanus.

795 Pickford M. Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds.). African Genesis:Perspectives on Hominin Evolution. Cambridge University Press, 2012. 102. http://books.google.com/books?id=PrJ1lmjMakoCandpg=PA116#v=onepageandqandf=false

796 New York University (2011, February 16). Fossils may look like human bones: Biological anthropologists question claims for human ancestry. ScienceDaily. Retrieved October 30, 2013, from http://www.sciencedaily.com/releases/ 2011/02/110216132034.htm .

797 Russo GA, Shapiro LJ. Reevaluation of the lumbosacral region of Oreopithecus bambolii. J Hum Evol 2013;65:253-65.

798 Wood B, Harrison T. The evolutionary context of the first hominins. Nature 2011 Feb 16;470(7334): 347-352. 347.

PROPOSED HUMAN ANCESTORS – 275

A. anamensis remains date to about 4.2 mya, and according to Tattersall look “reassuringly similar” to the 3.8 to 3.0 million-year-old remains of afarensis, which Tattersall describes as a “small-brained, big- faced bipedal species to which the famous ‘Lucy’ belonged.”799

A. afarensis fossils date to 3.85 to 2.95 mya.800 The species had a relatively small body (105-151 cm height, 29-42 kg weight) and brain case (375 to 550 cc, about 1/3 the size of a modern human), and an ape-like face with a flat nose and a projecting lower jaw. A presumably afarensis specimen dated to 3.6 mya had a somewhat less conical, more cylindrical human-like upper rib cage than found in extant apes.801 Like other Australopiths, this species had large molars and small canines, but afarensis canines “were relatively large and pointed, reminiscent of apes.”802 Dental microwear studies indicate that afarensis apparently primarily ate a plant-based diet consisting largely of soft, sugar-rich fruits, leaves, seeds, roots, nuts, and insects, and probably occasional small vertebrates, like lizards.803 Archaeologists found the remains of this species in Eastern Africa, where they have also found evidence that some species, perhaps afarensis, used stones to remove scraps of flesh from carcasses of large mammals about 3.2 mya.804

It appears that A. afarensis could walk upright on two legs, and had foot prints that looked much like human walking,805 although the feet had long, curved toes like those found in tree-climbing primates. This species also had long, strong arms with curved fingers adapted to tree climbing; the wrists have features that some have associated with knuckle-walking.806 However, Kivell and Schmidt claim that these purportedly knuckle-walking features found in hominin wrists actually provide evidence of adaptation to tree-climbing, not knuckle-walking.807 Afarensis also had a developmental process more similar to apes than to humans, with rapid growth and early onset of adulthood. In short, afarensis was a bipedal, but significantly arboreal ape.

799 Tattersall I. Once We Were Not Alone. Scientific American 2000 Jan: 56-62. 58.

800 Smithsonian National Museum of Natural History. What does it mean to be human? Australopithecus afarensis: Overview. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/australopithecus-afarensis .

801 Haile-Selassie Y, Latimer BM, Alene M, et al.. An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia. PNAS 2010 July 6;107(27):12121-12126.

802 Analysis of Early Hominins. Retrieved Oct 29, 2013 from http://anthro.palomar.edu/hominid/australo_2.htm .

803 Smithsonian National Museum of Natural History. What does it mean to be human? Australopithecus afarensis: How They Survived. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/australopithecus- afarensis .

804 Braun DR. Australopithecine butchers. Nature 2010 Aug 12;466(7308):828.

805 University of Arizona (2010, March 20). Evidence indicates humans' early tree-dwelling ancestors were also bipedal. ScienceDaily. Retrieved October 30, 2013, from http://www.sciencedaily.com/releases/2010/03/100319202526.htm .

806 Richmond BG, Strait DS. Evidence that humans evolved from a knuckle-walking ancestor. Nature 2000 Mar 23:404(6776):382-5.

807 Kivel TL, Schmitt D. Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor. PNAS 2009 Aug 25;106(34):14241-14246.

276 – APPENDICES & BIBLIOGRAPHY

A. africanus fossils date to 3.3 to 2.1 mya, thus apparently coexisted with A. afarensis for 350, 000 years, but fossils of this species were found in Southern, not Eastern, Africa.808 Africanus weighed 30-41 kg and stood 115-138 cm in height, virtually the same body size as afarensis. Africanus had a brain size ranging from 420 to 500 cc, within the same range as afarensis. Again like afarensis, this species had a flat nose and a jutting jaw. Africanus had hip girdle and lower limb structure indicating the ability to walk on two legs, but also had shoulder girdle and upper limb structure indicating an ape- like ability to climb trees. Dental microwear patterns indicate that africanus ate a diet similar to chimpanzees: fruit, plants, nuts, seeds, roots, insects, and eggs. Archaeologists have found remains of africanus alongside broken animal bones, but it appears that predators such as lions, leopards, and hyenas had not only left those bones, but also preyed upon africanus individuals.809

It seems possible that afarensis and africanus are not completely different species, but regional variations of the same species.

Lee Berger, a paleontologist at the University of Witwatersrand has suggested that fossils dubbed Australopithecus sediba dated to 1.9 mya represent a missing link between A. africanus and early Homo.810 However, as discussed in the next section, paleontologists have classified some skeletons dated to 2.4 mya as early Homo, making one wonder how sediba can serve as a link between Australopiths and Homo if the latter predates sediba.

Sediba specimens have dental characteristics that suggest a possibility that sediba and perhaps africanus did not descend from the afarensis lineage. Sediba teeth have five distinct similarities to those characteristic of africanus and also five distinct similarities to specimens classified as H. habilis/ rudolfensis or H. erectus; sediba also shares four specific dental features with Homo, including an identical cusp on the first lower molar.811 According to Berger, “Where the sediba mandibles differ from those of Au. africanus, they appear most similar to those of representatives of early Homo.”812 Nevertheless, based on thinness of the lower jaw and other bone features, Donald Johanson of Arizona State University believes that sediba does not belong to Australopithecus at all, but to Homo.813 That might be hard to reconcile with the following.

808 Smithsonian National Museum of Natural History. What does it mean to be human? Australopithecus africanus: Overview. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/australopithecus-africanus .

809 Smithsonian National Museum of Natural History. What does it mean to be human? Australopithecus africanus: How They Survived. Retrieved Oct 29, 2013 from http://humanorigins.si.edu/evidence/human-fossils/species/australopithecus- africanus .

810 Berger LR. The Mosaic Nature of Australopithecus sediba. Science 2013 April 12;340(6129:163-5.

811 Irish JD, et al.. Dental Morphology and the Phylogenetic “Place” of Australopithecus sediba. Science 2013 April 12;340(6129).

812 Berger LR. The Mosaic Nature of Australopithecus sediba. Science 2013 April 12;340(6129:163-5. Italic added.

813 Sample I. Fossil skeletons may belong to an unknown human ancestor. The Guardian 2010 April 8, 10.05 EDT. Retrieved October 24, 2013 from http://www.theguardian.com/science/2010/apr/08/fossil-skeletons-unknown-human-ancestor? guni=Article:in%20body%20link .

PROPOSED HUMAN ANCESTORS – 277

The sediba specimens have the long arms and strong hands typical of australopiths and similar to orangutans: “Au. sediba thus shares with other australopiths an upper limb that was well suited for arboreal climbing and possibly suspension, although perhaps more so than has previously been suggested for this genus.”814 Sediba had a very ape-like shoulder girdle and conical thorax “that is perhaps uniquely australopith and would not have been conducive to human-like swinging of the arms during bipedal striding and running.”815

Although some news accounts state that sediba had “long” legs,816 a skeletal reconstruction and comparison of a sediba specimen with a human and a chimpanzee shows sediba having stature only slightly greater and legs only slightly longer than extant chimpanzees.817 Sediba’s lower limbs probably supported bipedal locomotion but if so the gait involved hyperpronation and probably was distinctly different from that hypothesized for other australopiths, including afarensis (Lucy), leading Walker et al. to suggest that there may have been several forms of bipedalism during the Plio-Pleistocene era.818, 819, 820

Since as stated above afarensis appears to have had a very human-like gait, placing sediba as a descendant of afarensis and ancestor of Homo would mean that the more human-like gait, upper limbs, and rib cage found in afarensis reverted to a more ape-like gait and rib cage in sediba, then from sediba to Homo, these reversed again, an extremely unlikely scenario.

Like other australopiths, sediba specimens have “exceptionally small” brains of about 420 cc, about one-third the size of modern humans, i.e. similar to chimpanzees.821

By calling the sediba specimen Homo based on a few jaw and bone features, Johanson (above) seems to say that the human genus includes creatures that have conical rib cages, upper limbs specialized for climbing, a very non-human bipedal gait, and very small brains.

814 Berger LR. The Mosaic Nature of Australopithecus sediba. Science 2013 April 12;340(6129:163-5. Italic added.

815 Ibid..

816 Sample I. Op. cit..

817 Berger LR. The Mosaic Nature of Australopithecus sediba. Science 2013 April 12;340(6129:163-5. Also,an enlarged photo available at: http://www.sciencemag.org/content/340/6129/163/F1.expansion.html.

818 Sample I. Fossil skeletons may belong to an unknown human ancestor. The Guardian 2010 April 8, 10.05 EDT. Retrieved October 24, 2013 from http://www.theguardian.com/science/2010/apr/08/fossil-skeletons-unknown-human-ancestor? guni=Article:in%20body%20link .

819 American Association for the Advancement of Science (2011, September 8). Australopithecus sediba paved the way for Homo species, new studies suggest. ScienceDaily. Retrieved October 24, 2013, from http://www.sciencedaily.com/releases/ 2011/09/110908104159.htm .

820 Berger LR. The Mosaic Nature of Australopithecus sediba. Science 2013 April 12;340(6129:163-5.

821 Berger LR, de Ruiter DJ, Churchill SE, et al.. Australopithecus sediba: A New Species of Homo-like Australopith from South Africa. Science 2010 April 9;328(5975):195-204.

278 – APPENDICES & BIBLIOGRAPHY

Although we have only two specimens, the Smithsonian Museum of Natural History claims that sediba had a level of sexual dimorphism similar to that found in modern humans,822 i.e. about 20% difference in size. As we shall see below, some evidence suggests that H. erectus had a greater level of sexual dimorphism than modern humans. If sediba did have little sexual dimorphism, then the lineage would have had low sexual dimorphism in sediba, high sexual dimorphism in erectus, then again low sexual dimorphism in modern humans. This also seems a highly unlikely evolutionary trajectory.

Overall, sediba gives the definite impression of an ape. Although it has a number of similarities with Homo specimens, so do orangutans. As made clear by Wood and Harrison, shared features don’t necessarily point to close genetic relation. Although this specimen “makes sense” as an putative ancestor of humans, we have no direct evidence that any of the australopithecus species was an ancestor of Homo.

Hence, Wood and Harrison state:

“Au. anamensis and Au. afarensis are probable time-successive sister taxa, but the relationships of Au. garhi and Au. sediba, as well as the relationship of Australopithecus species to Paranthropus and Homo, are still unresolved.”823

They go further to state:

“Each species manifests morphology that allows them to be diagnosed as separate taxa, but from a phylogenetic perspective the overlapping combinations of features result in high levels of homoplasy that confound phylogenetic analyses.”824

In other words, the limits of fossil evidence and of our methods make it impossible to know with certainty which if any of the ancient species under discussion is in fact an ancestor of modern humans.

Homo habilis and rudolfensis

In the usual evolution story, Homo habilis and rudolfensis serve as the transition species between Australopithecus and H. erectus.

822 Smithsonian National Museum of Natural History. What does it mean to be human? Australopithecus sediba: Height and Weight Supplemental Information. Retrieved October 24, 2013 from http://humanorigins.si.edu/evidence/human-fossils/ species/australopithecus-sediba.

823 Wood B, Harrison T. The evolutionary context of the first hominins. Nature 2011 Feb 16;470(7334): 347-352. 350.

824 Ibid., 350.

PROPOSED HUMAN ANCESTORS – 279

Fossils classified as Homo habilis date from 2.4 to 1.5 million years ago. This species has generated controversy because “it is widely thought that the 'habilis' specimens have too wide a range of variation for a single species, and that some of the specimens should be placed in one or more other species.”825

After describing Australopithecus species as more similar to chimpanzees than to Homo, the biologist Ernst Mayr explains that we have no fossils that can serve as the “missing links” between the former and the latter:

“The earliest fossils of Homo, Homo rudolfensis and Homo erectus, are separated from Australopithecus by a large, unbridged gap. How can we explain this seeming saltation? Not having any fossils that can serve as missing links, we have to fall back on the time-honored method of historical science, the construction of a historical narrative...Readers who are not familiar with this method of historical narratives may say, Why should I believe in any of this, it is nothing by speculation. Yes, you can call it speculation, but this designation ignores that my scenario is based on carefully weighed inferences...It provides a ’most probable’ scenario, which suggests new questions one otherwise might not have thought of.”826

Although Mayr considers rudolfensis a valid taxon, other experts believe that the fossils supposed to represent H. habilis and rudolfensis actually belong to Australopithecus species. Lieberman et al. highlight “the paucity of fossil and archaeological records” and suggest that the alleged evolution of Homo from Australopiths remains unclear at best:

“Of the various transitions that occurred during human evolution, the transition from Australopithecus to Homo was undoubtedly one of the most critical in its magnitude and consequences. As with many key evolutionary events, there is both good and bad news. First, the bad news is that many details of this transition are obscure because of the paucity of the fossil and archaeological records. The oldest known archaeological sites from 2.6 million years ago provide, at best, a sparse and incomplete glimpse of early hominin behavior. In addition, it is unclear who made the oldest tools, and the fossil record itself leaves much to be desired. The genus Homo is probably at least 2.3 million years old, but most of the fossil evidence for early Homo comes from the period between 1.9 and 1.6 million years ago from just a few localities in the East African Rift Valley. In addition, fossils attributed to H. habilis are poorly associated with inadequate and fragmentary postcrania, no fossils attributed to H. rudolfensis are associated with any postcrania, and the earliest material attributed to H. erectus is highly variable, and contemporary with H. habilis and H. rudolfensis. Finally, the relationship between the oldest Homo from Africa and Eurasia (at Dmanisi) remains murky because of their morphological

825 Foley J. Hominid Species. Talk Origins. Retrieved September 18, 2013 from http://www.talkorigins.org/faqs/homs/ species.html

826 Mayr E. What Makes Biology Unique. Harvard University Press, 197-98. http://camscience.files.wordpress.com/2010/01/ what-makes-biology-uniqu1.pdf

280 – APPENDICES & BIBLIOGRAPHY

variability and nearly contemporary ages. When we discuss early Homo, we do not know for sure how many species we are dealing with and how different they are.”827

Tattersall and Schwartz maintain that we have “little morphological basis for extending our genus to any of the ~2.5–1.6-myr-old fossil forms assigned to ‘early Homo’ or Homo habilis/rudolfensis” because “at best these ‘early Homo’ specimens make up a very motley assortment” and in fact they do not have sufficient similarity to humans to qualify for classification as Homo species.828 They accept the conclusion that “anything currently known that was more primitive than Homo ergaster had to be excluded from Homo to make morphological and phylogenetic sense.”829

By 2011, despite the problem of scant evidence – “there are precious few fossils…especially from the neck down” of either habilis or rudolfensis – some experts believed that they had more evidence that H. habilis and rudolfensis matured, moved, and had a dietary range less like a human and more like an australopithecine, enough to consider excluding habilis and rudolfensis from Homo.830

About 1.5 mya, habilis and erectus co-existed for at least half a million years, making it unlikely that erectus evolved from habilis.831 According to the Smithsonian Institution, fossil evidence suggests that Homo habilis probably was not the ancestor of Homo erectus:

“While scientists used to think that H. habilis was the ancestor of Homo erectus, recent discoveries in 2000 of a relatively late 1.44 million-year-old Homo habilis (KNM-ER 42703) and a relatively early 1.55 million-year-old H. erectus (KNM-ER-42700) from the same area of northern Kenya (Ileret, Lake Turkana) challenged the conventional view that these species evolved one after the other. Instead, this evidence – along with other fossils – demonstrate that they co-existed in Eastern Africa for almost half a million years.”832

In short, the paucity and poor quality of evidence for a transition from Australopiths to Homo belies any claims that any specific behavior, such as meat-eating, caused the genetic changes that would be necessary to convert australopithecus species into humans.

827 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009. 1.

828 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92.

829 Ibid., 70.

830 Gibbons A. Who Was Homo Habilis–And Was It Really Homo? Science 2011 June 17:332(6036):1370-71. Retrieved Nov 3, 2013 from http://lists.portside.org/cgi-bin/listserv/wa?A3=ind1107aandL=PORTSIDEandE=0andP=15128andB=-- andT=text%2Fplainandheader=1 .

831 Borenstein S. Fossils paint messy picture of human origins. New findings raise questions about who evolved from whom. Science on NBCNews.com, 2007 Aug 8. Retrieved Oct 24, 2013 from http://www.nbcnews.com/id/20178936/ns/ technology_and_sciencescience/t/fossils-paint-messy-picture-human-origins/#.Umltxhlbv4g .

832 Smithsonian National Museum of Natural History. What does it mean to be human? Homo habilis: Evolutionary Tree. http://humanorigins.si.edu/evidence/human-fossils/species/homo-habilis

PROPOSED HUMAN ANCESTORS – 281

Erectus species

Defenders of ‘paleo’ and low-carbohydrate diets sometimes cite the alleged hunting behaviors of H. erectus as evidence that humans are genetically adapted to meat-eating.

Tattersall and Schwartz question the assignment of many fossils to H. erectus, claiming that “non-Asian pretenders to Homo erectus status not only fail to show the morphological hallmarks of that species as defined by it holotype, but make a very heterogeneous assemblage indeed.”833 They believe that African fossils classified as erectus differ substantially and in important ways from Asian fossils, and favor classifying the former as H. ergaster (see below).

Wolpoff et al. favor eliminating the H. erectus classification, and argue for reclassifying all fossils attributed to H. erectus as H. sapiens.834 They believe that no distinct temporal, spatial, structural, or behavioral boundary separates H. erectus from H. sapiens, and that “there is no speciation involved in the emergence of Homo sapiens from Homo erectus.”

In contrast, Tattersall and Schwartz believe that the assemblage of fossils classified as H. erectus makes “a very heterogeneous assortment indeed; and placing them all together in the same species only makes any conceivable sense in the context of the ecumenical view of Homo erectus as the middle stage” of a single “hypervariable hominid lineage.”835 They don’t favor this approach:

“Viewed from the morphological angle, however, the practice of cramming all of this material into a single Old World-wide species is highly questionable. Indeed, the stuffing process has only been rendered possible by a sort of ratchet effect, in which fossils allocated to Homo erectus almost regardless of their morphology have subsequently been cited as proof of just how variable the species can be.”836

Perhaps to exemplify this point, in 2013, archaeologists reported finding the fifth of five alleged erectus skulls in Dmanisi, Georgia, dating to 1.8 mya. These five skulls included an elderly male, two adult males, a young female, and a juvenile of unknown sex. The latest skull had the largest body of the five, but had the smallest, 550 cc braincase (similar to a large A. afarensis!). The variations among these five skulls are so great that excavation leader David Lordkipanidze of the Georgian National Museum, said: “If you found the Dmanisi skulls at isolated sites in Africa, some people would give them different

833 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 74.

834 Wolpoff MH, Thorne AG, Jelinek J, Yinyun Z. The Case for Sinking Homo erectus. 100 Years of Pithecanthropus is Enough! In:Franzen JL. 100 Years of Pithecanthropus: The Homo Erectus Problem. Courier Forschunginstitute Senckenberg 1994;171:341-361. Retrieved Oct 31, 2013 from http://www-personal.umich.edu/~wolpoff/Papers/Sinking.pdf.

835 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 71.

836 Ibid., 71.

282 – APPENDICES & BIBLIOGRAPHY

species names. But one population can have all this variation. We are using five or six names, but they could all be from one lineage.”837

Comparing Australopithecus to early H. erectus, “although absolute brain size does increase across the transition, larger brains in early Homo apparently scale with body size, so that encephalization quotients (EQs) in the early African and Georgian H. erectus individuals are not much different from those of australopiths.”838

Erectus specimens have skulls distinctly different from sapiens: the former have an ape-like, long, low brain case with a sharply angled rear and forwardly projecting supraorbital ridges; while sapiens specimens have short, high-vaulted skulls without the projecting supraorbital ridges. Furthermore, as noted by Tattersall and Schwartz, we have no evidence indicating that erectus had the symbolic cognitive capacities that “most strikingly demarcate us from all other extant species.”839 Consequently they do not agree with the proposal to reclassify erectus as sapiens.

Lieberman et al. state that “H. erectus life history was apparently much like that of chimpanzees and australopiths…they may not have and a full capacity for language [symbolic cognition], and the extent to which they were able to extract versus collect resources may have been limited.”840

Erectus specimens found in Dmanisi, Georgia seem to have had significant size differences between male and female (sexual dimorphism).841 This is distinctly different from modern humans.

Curiously, fossils suggest that erectus appeared “almost simultaneously” in Africa and Asia.

“This, coupled with the potential dethroning of African H. habilis as H. erectus’s ancestor, opens the door to a once-outrageous possibility: H. erectus, which researchers have long assumed was born in Africa, ‘could have originated in Asia,’ says paleoanthropologist David Lordkipanidze of the Georgian National Museum in Tbilisi. ‘It no longer seems like such a crazy idea.’”842

837 Sample I. Skull of Homo erectus throws story of human evolution into disarray. The Guardian 2013 Oct 17 14:00 EDT. Retrieved October 24, 2013 from http://www.theguardian.com/science/2013/oct/17/skull-homo-erectus-human-evolution .

838 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009.2.

839 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 83.

840 Lieberman et al.. The Transition from Australopithecus to Homo. In: Shea JJ and Lieberman DE (eds.). Transitions in prehistory: essays in honor of Ofer Bar-Yosef. Oxbow, 2009.2.

841 Borenstein S. Fossils paint messy picture of human origins. New findings raise questions about who evolved from whom. Science on NBCNews.com, 2007 Aug 8. Retrieved Oct 24, 2013 from http://www.nbcnews.com/id/20178936/ns/ technology_and_sciencescience/t/fossils-paint-messy-picture-human-origins/#.Umltxhlbv4g .

842 Gibbons A. Who Was Homo Habilis–And Was It Really Homo? Science 2011 June 17:332(6036):1370-71.

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Although perhaps no longer “crazy,” this idea suggests that some erectus (non-African) may belong to a branch of hominin lineage only distantly related to sapiens since archaeological and molecular data agree in indicating that “all extant populations of human beings derive from an exodus of Homo sapiens from Africa that took place some 80-60 kyr ago.”843 Lack of clarity here prevents us from assuming that the dietary habits of this now-extinct Eurasian erectus species provide valuable information about the nutritional requirements of modern humans.

According to Tattersall and Schwartz, unlike Eurasian fossils attributed to H. erectus, the African fossils at one time or another attributed to erectus “show less morphological homogeneity than we see in eastern Asia, span a very substantial amount of time and space, and fail to exhibit significant similarities with their counterparts in Java and China.”844 Due to their distinctiveness, Tattersall and Schwartz, along with some other paleoanthropologists, classify these African fossils as Homo ergaster.

The oldest of these African erectus/ergaster fossils date to 1.9 to 1.5 mya and come from northern Kenya. The cranial volumes of these fossils range from 510 cc to 900 cc. According to Tattersall and Schwartz, the 1.6 myr-old “Turkana Boy” (WT 15000) having an 880 cc brain case is the earliest hominid that qualifies for membership in the genus Homo:

“For, although differing from that of Homo sapiens in numerous features, the WT 15000 skeleton is modern in its basic proportions (Walker and Leakey 1993) and is absolutely without precedent. Hominid postcranial remains are quite rare in the early fossil record; but prior to WT 15000 (or at least to the period, beginning approximately 1.9 myr ago, in which we can reasonably infer from cranial evidence that functionally similar hominids were in existence) there are no convincing indications in the African record that any hominid had departed from the body structure typical of the early bipedal apes.”845

Although modern in proportions, this “Turkana boy” differed from modern humans in developmental schedule and some important details. He died at eight years of age, but had the skeleton of a modern thirteen year-old, effectively adult in most features, demonstrating an ape-like developmental schedule. He measured 1.6 m (5 ft 3 in) tall at death, but scientists estimate that he might have reached 1.85 m (6 ft) with a 909 cc brain case at full adulthood. In the image of the skeleton provided on the Smithsonian Institution’s Human Origins Program, the thorax appears to have a slightly conical shape (wide at bottom, narrow at top) reminiscent of Australopiths and not yet like the cylindrical rib cage of modern humans.846

843 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 83.

844 Ibid., 73.

845 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 74.

846 Smithsonian National Museum of Natural History. What does it mean to be human? KNM-WT 15000. Retrieved Nov 1, 2013 from http://humanorigins.si.edu/evidence/human-fossils/fossils/knm-wt-15000 .

284 – APPENDICES & BIBLIOGRAPHY

Ergaster skulls have large orbits with projecting supraorbital ridges, no forehead, and an ape-like projection of the lower face and jaw, with a mandible significantly larger than found in modern humans. Despite a significantly larger brain compared to other bipedal apes, “there is no immediate signal in the record of any major cognitive improvement with the advent of the new body form.”847

Tattersall and Schwartz assign the Dmanisi hominid fossils to ergaster, and suggest that they represent some of the first hominids to have left Africa for Asia.848 However, the Dmanisi fossils dated to 1.8 mya differ substantially from ergaster as represented by the “Turkana boy” dated to 1.6 mya. The adult male Dmanisi fossils have brain cases as small as 550 cc, while the “Turkana boy” would have had a brain case as large as 909 cc. Adult male H. erectus specimens generally have proportions suggesting a height of 152-168 cm (5-5.5 ft),849 but the “Turkana boy” would have reached 185 cm (6 ft) as an adult. Putting “Turkana boy” and the Dmanisi fossils in the same species seems to require a very flexible conception of morphological similarity. If they truly are the same species, this suggests that African erectus/ergaster underwent a near doubling of brain size and a large increase in body size in just about 200,000 years.

Erectus specimens have small canines and molar teeth, or microdontia, a trait shared with Orrorin and modern humans. As extensively discussed in Chapter 6, Ungar compared the teeth of erectus specimens to those of gorillas, chimpanzees, and Au. afarensis, and found that gorillas had greatest shearing ability, followed by erectus, chimpanzees, and afarensis, in that order.850 Since we lack certainty that Homo descended from afarensis, we can’t say that this means that the evolution of afarensis into Homo involved selection for sharper teeth; and since gorillas eat a plant-based diet but have sharper teeth than erectus, apparently because natural selection favors sharp teeth in leaf-eating species, we can’t say that only increased meat-eating could have selected for the sharper teeth found in erectus.

Homo heidelbergensis

Fossils from this alleged species have 1120 to 1285 cc brain cases, broad and massive lower faces, tall supraorbital margins that peak near midorbit, and twisting anterior supraorbital surfaces. These fossils have been found in Germany, Ethiopia, Greece, France, Zambia, South Africa, and possibly China. According to Tattersall and Schwartz, this material is “poorly dated” but falls in the range of 200- to 600- kyr, overlapping with erectus/ergaster.851

847 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 75.

848 Ibid., 76.

849 Early Human Evolution: Homo ergaster and erectus. Retrieved Nov 6, 2013 from http://anthro.palomar.edu/homo/ homo_2.htm.

850 Ungar P. Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution 2004:46:605-622. 612.

851 I Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 77.

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The heidelbergensis fossils are associated with primitive stone tools and, in Germany, “miraculously preserved 400 kyr old wooden spears.”852 However, according to Tattersall and Schwartz, we cannot be certain that all of the significant technological innovations associated with heidelbergensis fossils were actually made by Homo heidelbergensis, because the latter shared the Earth with other, apparently reproductively distinct types of hominids, including erectus/ergaster.853 As with other hominids, we have no unambiguous evidence that heidelbergensis had symbolic cognition.

Neanderthals

Advocates of low-carbohydrate and animal-based “paleo” diets like to suggest that modern humans have some important genetic relationship to Neanderthals because some lines of evidence suggest that Neanderthals ate largely animal-based diets. However, Neanderthals (Neandertals) and ancestors of modern human populations became isolated from one another at least 350,000 years ago.854

Researchers who sequenced the Neanderthal genome claim that 1–4% of the modern human genome is Neanderthal as a result of interbreeding.855 However, since the Neanderthal samples were contaminated with human DNA and the researchers only read the draft Neanderthal genome 1.3 times, some geneticists not involved in the research considered it “of limited value” and inconclusive.856 Also:

“A challenge in detecting signals of gene flow between Neandertals and modern human ancestors is that the two groups share common ancestors within the last 500,000 years, which is no deeper than the nuclear DNA sequence variation within present-day humans. Thus, even if no gene flow occurred, in many segments of the genome, Neandertals are expected to be more closely related to some present-day humans than they are to each other.”857

Further, mitochondrial DNA (mtDNA) analysis indicated that the Neanderthals and Homo sapiens lineages have been distinct (separated) for between 690 and 550 thousand years, and mtDNA analyses of modern human populations “reveal a total absence of Neanderthal sequences.”858 Finally, the authors of the draft sequencing of the Neandertal genome themselves state that their evidence does not conclusively prove interbreeding:

852 Ibid., 78.

853 Ibid., 79.

854 Weaver TD. The meaning of Neandertal skeletal morphology. PNAS 2009 September 22;106(38):16028-16033.

855 Dalton R. European and Asian genomes have traces of Neanderthal. Nature Online 2010 May 6.

856 Dalton R. European and Asian genomes have traces of Neanderthal. Nature Online 2010 May 6.

857 Green RE, Krause J, Briggs AW, et al.. A Draft Sequence of the Neandertal Genome. Science 2010 May 7;328(5979): 710-722.

858 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 81.

286 – APPENDICES & BIBLIOGRAPHY

“Although gene flow from Neandertals into modern humans when they first left sub-Saharan Africa seems to be the most parsimonious model compatible with the current data, other scenarios are also possible. For example, we cannot currently rule out a scenario in which the ancestral population of present-day non-Africans was more closely related to Neandertals than the ancestral population of present-day Africans due to ancient substructure within Africa (Fig. 6). If after the divergence of Neandertals there was incomplete genetic homogenization between what were to become the ancestors of non-Africans and Africans, present-day non-Africans would be more closely related to Neandertals than are Africans. In fact, old population substructure in Africa has been suggested based on genetic (81) as well as paleontological data (86).”859

Neanderthals were physically distinct from Homo sapiens. Neanderthal skulls have little forehead, and a long, low braincase similar to H. erectus. The Neandertal midface projects whereas the human forehead projects. Neanderthals have a wider pelvis and scapula, longer clavicles, and shorter arms and legs than found in modern humans.860 Neanderthal rib cages have a “hyper barrel-shape” compared to modern human rib cages, probably reflecting a higher body mass to height ratio.861

Apparently the Neandertal lineage separated from the modern human lineage when geographic barriers produced by climate fluctuations isolated European Neandertal populations from southern populations that gave rise to modern humans.862 These two lineages adapted to significantly different ecosystems in apparent reproductive isolation for ~300,000 years. How much can Neandertals tell us about modern humans?

Homo sapiens

At the present time, we have fossils indicating that anatomically modern humans inhabited Ethiopia by about 195,000 years ago.863 At the time, other hominids still walked the Earth:

“When Homo sapiens originated, there were several other hominid species in existence: Homo neanderthalensis, Homo erectus, and probably several others as well, including Homo

859 Green RE, Krause J, Briggs AW, et al.. A Draft Sequence of the Neandertal Genome. Science 2010 May 7;328(5979): 710-722.

860 Weaver TD. The meaning of Neandertal skeletal morphology. PNAS 2009 September 22;106(38):16028-16033.

861 Franciscus RG, Churchill SE. The costal skeleton of Shanidar 3 and a reappraisal of Neandertal thoracic morphology. J Hum Evol 2002 Mar;42(3):303-56.

862 Weaver TD. The meaning of Neandertal skeletal morphology. PNAS 2009 September 22;106(38):16028-16033.

863 University Of Utah (2005, February 28). The Oldest Homo Sapiens: Fossils Push Human Emergence Back To 195,000 Years Ago. ScienceDaily. Retrieved November 1, 2013, from http://www.sciencedaily.com/releases/ 2005/02/050223122209.htm .

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floresiensis, the inscrutable dwarfed hominid from the Indonesian island of Flores described by Brown et al. in 2004.”864

Regarding erectus/ergaster, this/these species appear in the fossil record as late as 143,000 years ago. This implies that modern humans and erectus/ergaster coexisted for at least roughly 50,000 years, and suggests either that erectus/ergaster and sapiens were at the time the same hypervariable species, or that sapiens and erectus/ergaster constitute two distinct, although structurally similar, species. As noted above, Tattersall and Schwartz argue that the former option seems unlikely.

Archaeological and molecular data agree in indicating that “all extant populations of human beings derive from an exodus of Homo sapiens from Africa that took place some 80-60 kyr ago.”865 This implies that if modern humans evolved from any erectus/ergaster groups, it was from one of those who had remained in Africa, not any of those who inhabited Asia or Europe prior to 60 kyr ago.

Zorich gives the following account:

“Homo sapiens was not the first group of hominins to journey into the world beyond Africa. Groups of the now-extinct species Homo erectus are known to have lived in what are now Spain and the Republic of Georgia around 1.8 million years ago. Homo sapiens likely evolved some time around 200,000 years ago from the groups of Homo erectus who had remained in Africa.”866

If Homo sapiens evolved from African erectus/ergaster and emerged 200,000 years ago, but did not reach Eurasia until about 80, 000 years ago, then the Eurasian erectus species may have lived in reproductive isolation from H. ergaster, the African stem for H. sapiens for at least 200,000 years and possibly for as much as 1.8 million years.

As noted by Tattersall and Schwartz, symbolic cognition characterizes Homo sapiens on the basis that we have no evidence of this ability for H. erectus, and all claimed instances of this ability for Neanderthals are strongly disputed. The earliest evidence we have for this ability dates to about 100 kyr ago “well after the point at which we can be reasonably certain that anatomically modern humans were already in existence.”867

Homo sapiens has had control of fire and used it to cook foods for all of its existence. As Wrangham et al. have stated, cooking is a human universal. Modern humans have smaller teeth, jaws, and faces than

864 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92. 85.

865 Ibid., 83.

866 Zorich Z. New Evidence for Mankind’s Earliest Migrations. Archaeology 2011 May/June;64(3). Retrieved Nov 1, 2013 from http://archive.archaeology.org/1105/trenches/homo_sapien_migration_africa_arabia.html .

867 Tattersall I, Schwartz JH. Evolution of the Genus Homo. Ann Rev Earth Planet Sci 2009 May 30;37:67-92.84.

288 – APPENDICES & BIBLIOGRAPHY

any previous hominid, and Wrangham et al. and others suggest that these features arose as a result of using fire and other methods to process foods before consumption.868

The Limits of Archaeology

As discussed above, Wood and Harrison have pointed out that fossil evidence is plagued by the problem of homoplasy: skeletons having significant structural similarities may not have shared evolutionary history because, from a Darwinian perspective, similar environments may select for similar traits in only distantly related lineages. Since the fossil record presently only yields skeletal remains, Wood and Harrison admit that providing convincing evidence for hypothesized evolutionary relationships may actually be impossible:

“So why do researchers persist in trying to solve a phylogenetic problem that may well be at the limits of, or even beyond, the analytical capabilities of the data and the available methods? The reason is that our own ancestry matters to [some of] us. Most vertebrate palaeontologists would be content to accept that the ancestry of Homo resides in Australopithecus, without needing or expecting to unravel the topological complexity of the different species within the latter genus. We are not advocating that researchers abandon trying to draw inferences about the phylogenetic relationships of hominins at the finest scale possible. However, we do suggest that those who present and accept these hypotheses need to be aware that such inferences, especially ones about stem taxa, are likely to be inherently prone to refutation and subsequent revision.”869

In contrast, the study of modern human nutritional requirements using living humans is not “at the limits of, or even beyond, the analytical capabilities of the data and the available methods.”

Given the severe limits on archaeological research in comparison to epidemiological and clinical research, and the substantial disagreements and uncertainties in the field of paleoanthropology, I do not understand why anyone attempting to determine the nutritional requirements of modern humans would consider tenuous hypotheses of prehistoric human evolution offered by paleoanthropologists and evolutionary biologists more informative than historic and contemporary reports and research. On the contrary, our well-established knowledge of the nutritional requirements of modern humans should guide any hypotheses about the subsistence strategies and biological evolution of alleged human ancestors.

868 Wrangham et al.. The Raw and the Stolen; Cooking and the Ecology of Human Origins. Current Anthropology 1999 Dec; 40(5):567-594.

869 Wood B, Harrison T. The evolutionary context of the first hominins. Nature 2011 Feb 16;470(7334): 347-352. 350.

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Appendix D: Chimpanzees

Since some chimps hunt and eat some insects and flesh, some people believe that insects and animal flesh play an essential nutritional role in chimp diets. Further, since chimpanzees and humans have a DNA sequence similarity of 95 to 96 percent 870, some people seem to believe that the fact that some chimpanzees hunt and consume flesh provides evidence that such behavior is natural and necessary not only for chimps, but also for humans.

In Appendix C, I briefly discussed the fact that humans also share a DNA sequence similarity of about 96 percent with orangutans. As mentioned, some scientists argue the DNA data does not unequivocally point to chimps as our closest primate relative, and study of morphological, biomechanical, behavioral, and cognitive similarities between orangutans and humans leads to the conclusion that humans have a closer evolutionary relationship to orangutans than to chimps.

Nevertheless, here I want to discuss the relative importance of animal tissue in chimpanzee diets, because so many scientists and lay people believe that the fact that some chimpanzees eat meat tells us something important about human dietary requirements.

Quantity

How much flesh finds its way into the average chimpanzee diet? Apparently, so little that a respected guide to caring for chimpanzees emphasizes their frugivory, and identifies the diet as essentially 100 percent herbivorous:

“The chimpanzee diet consists mainly of fruit (48%), but they also eat leaves and leaf buds (25%), and around 27% of their diet consists of a mixture of seeds, blossoms, stems, pith, bark and resin. Chimpanzees are highly specialized frugivores and preferentially eat fruit, even when it is not abundant. They supplement their mainly vegetarian diet with insects, birds, birds' eggs, honey, soil, and small to medium-sized mammals (including other primates).”871

According to The Pictorial Guide To The Living Primates, wild chimps get 95 to 100 percent of their food from plants, primarily fruits; animal prey, including grubs, wasps, termites, ants, ten bird species, and mammals, composes zero to five percent of the diet.872

Strangely, given the information that chimps spend zero to five percent of their time procuring animal prey, some people seem to focus on the 5 percent figure and ignore the zero percent figure. But this

870 Preuss TM. Human brain evolution: From gene discovery to phenotype discovery. PNAS 2012 June 26;109(Suppl 1): 10709-10716.

871 The Chimpanzee Species Survival Plan. Caring For Chimpanzees. http://www.lpzoosites.org/chimp-ssp/chimpanzees.htm

872 Rowe N. The Pictorial Guide to the Living Primates. Pogonias Press, 1996. 230.

291

range actually suggests that chimpanzees may not require animal prey in their diet, since their diet doesn’t always contain it.

So, does the fact that some chimpanzees hunt animals and eat flesh actually indicate that they have biologically adapted to eating flesh or must eat flesh to meet some nutritional requirement not satisfied by plant foods?

Measuring Wild Chimpanzee Diets

Have you ever wondered how primatologists estimate the proportions of wild chimpanzee diets? In human studies, we can ask people to weigh and measure their food, or do it for them. Can you imagine following any wild animal in its natural habitat, and, every time it goes to eat something, attempting to interrupt it so that you can measure the exact amount of food it consumes?

Since it is practically impossible to interrupt a wild chimp to weigh its food before the chimp consumes the food, in studies of wild chimpanzee feeding behavior, observers record the amount of time the chimps spent pursuing and feeding on each type of food, not the actual amount of each food consumed.873

Details of Jane Goodall’s report on the behavior of the chimpanzees of Gombe indicate that this approach probably significantly overestimates the proportion of chimpanzee diet or nutrition actually derived from animals.

Chimpanzee Insectivory

According to Jane Goodall, in 1978, the Gombe chimpanzees spent some time eating insects in eight of twelve months and some time eating meat in seven of twelve months. In 1979, they spent some time eating insects in ten of twelve months and some time pursuing meat in seven of twelve months. In every month, they spent the vast majority of their time feeding on plant source foods.874

So was this time feeding on insects well spent from a nutritional perspective?

Nearly ninety percent of the total time that Gombe chimpanzees spent feeding on insects, they were eating termites, and fifty to sixty percent of days on which they ate insects, they were eating termites.875 Females spent more time eating insects than males, and time spent fishing for insects typically increases in the dry season when fruits may be less abundant. This alone indicates that chimps prefer fruit to insects. Further, according to Jane Goodall:

873 Ibid., 232

874 Goodall J. The Chimpanzees of Gombe. Harvard University Press, 1986. 233.

875 Ibid., 248

292 APPENDICES & BIBLIOGRAPHY

“In the dry season, when termites are in the lower levels of their nests, females spend long periods searching for them and, when they find a productive heap, long periods feeding on them. So far, precise data on the number of termites per tool, or the percentage of times that any termites at all are captured per prove, have not been collected. However, it is not uncommon for a female at this time of year to continue fishing for an hour or more even when this is getting only a few termites every ten minutes. The longest session recorded during the two years was in May 1980, when Passion (with Pom and their offspring) worked a mound for a total of four hours, twenty-nine minutes. Unfortunately, we do not know Passion’s total intake during all that time, but it is certain that she was catching very few termites.”876 [Italic added]

This passage suggests that much of the time spent by chimpanzees in search of and feeding upon insects is, practically speaking, nutritionally fruitless.

According to Goodall’s report, a chimp might spend an hour fishing for termites while collecting only “a few every ten minutes.” The word “few,” which means “more than one, but not many,” lacks precision. Typically this means less than a dozen, and usually only three or four, but out of generosity to those who think insectivory plays an important role in chimp nutrition, I will for purposes of this discussion very generously assume that “a few” termites means as many as one hundred.

One large soldier termite (preferred by chimps877) weighs about twenty to twenty-five milligrams.878 One hundred soldier termites would weigh about 2.5 grams, so if a chimp gets one hundred termites every ten minutes over the course of an hour, she gets perhaps 15 grams of termites in one hour. (If she really gets only “a few,” like four, every ten minutes, then she gets only 600 milligrams of termites in one hour.)

Fresh live insects supply about 1.2 kcalories, 0.22 g protein, and 0.04 g fat per gram of fresh weight 879, so an hour of termite fishing with a success rate of one-hundred termites every ten minutes would yield 18 kcalories, 3 g protein, and 0.6 g fat. (Divide by twenty-five and we find out that if she gets only four termites every ten minutes, closer to the usual meaning of “a few” as stated by Goodall, she would get only seven-tenths of a kcalorie, one-tenth of a gram of protein, and 0.02 g of fat for a whole hour of termite fishing!)

A 75 kg chimpanzee requires 1800 to 2600 kcalories daily, so an hour of termite fishing that captures 100 termites every ten minutes yields a meager one percent (or less) of her daily energy requirement, a very poor return on time investment. (If the catch consists of only four termites every ten minutes, the hour yields 0.03 percent of the chimp’s daily caloric requirement.)

876 Ibid., 258.

877 Goodall J. The Chimpanzees of Gombe. Boston, Harvard University Press, 1986. 251.

878 University of Florida Institute of Food and Agricultural Sciences, Department of Entomology and Nematology. Featured Creatures: Western Drywood Termite. http://entnemdept.ufl.edu/creatures/urban/termites/western_drywood_termite.htm

879 Eaton SB, Shostak M, Konner M. The Paleolithic Prescription. New York, Harper and Row, 1988. 70.

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Compare this to gathering figs, a fruit commonly eaten by chimps. A single large fig provides 47 kcalories and 0.5 gram of protein.880 In ten minutes, a chimp could easily pick and eat four figs, supplying ten times the food energy and two-thirds the protein provided by one hundred termites. On most days chimpanzees spend about half of their waking hours feeding.881 If a chimp spent eight hours daily fishing for termites, with a success rate of one hundred termites per ten minutes, she would obtain only about eight percent of her caloric requirements and 24 grams of protein. If a chimp spent the eight hours collecting figs at the rate of only four every ten minutes (twenty-four per hour), she would garnish 9024 kcalories and 96 grams of protein.

This all indicates that although chimps spend some significant amounts of time fishing for insects, they probably don’t get much in return for their effort. More importantly, it is clear that ten minutes spent eating fruit will usually supply a chimp with a much higher food value than ten minutes eating termites. Most likely, this explains why chimps devote the most time to termite-fishing when they have a shortage of fruits; termites constitute a nutritionally inferior food that chimps will pursue only when they can’t get their hands on sufficient fruit (something to eat is better than nothing to eat). Thus, measuring the role of insects in chimp diets by recording the amount of time they spend eating insects dramatically overestimates the nutritional importance of insects in chimp diets.

By the way, eating raw insects presents a number of health risks not incurred when eating fruits:

“Some insects secrete toxins, produce toxic metabolites or sequester toxic chemicals from food plants (Blum, 1978; Duffey, 1980; Wirtz, 1984). Defensive secretions that may be reactive, irritating or toxic include carboxylic acids, alcohols, aldehydes, alkaloids, ketones, esters, lactones, phenols, 1,4-quinones, hydrocarbons and steroids, among others. Phytochemicals sequestered by various insects include simple phenolics, flavin, tannins, terpenoids, polyacetylenes, alkaloids, cyanogens, glucosinolates and mimetic amino acids. Insects are also a source of injectant, ingestant, contactant and inhalant allergens (Wirtz, 1984; Gorham, 1991 ), and some insects serve as vectors or passive intermediate hosts of vertebrate pathogens such as bacteria, protozoa, viruses or helminths (Gorham, 1991). More attention should be directed toward assessing these risk factors in the edible insect groups.”882

Do Chimpanzees Scavenge?

As discussed in Chapter 7, some people believe that early human ancestors, who descended from the common ancestor of chimpanzees and humans, ventured into eating the flesh of large game animals by route of scavenging flesh. If so, we might reasonably expect chimpanzees to enjoy scavenging meat.

880 USDA.

881 Goodall J. The Chimpanzees of Gombe. Harvard University Press, 1986. 231.

882 DeFoliart G. Insects as Human Food. Crop Protection (1992) 11: 395-399. Accessed on September 18, 2012 at http:// www.food-insects.com/Insects%20as%20Human%20Food.htm

294 APPENDICES & BIBLIOGRAPHY

However, chimpanzees rarely engage in scavenging and do not show strong interest in it when given the opportunity:

“Contrary to recent statements in the scavenging literature (Blumenschine and Cavallo 1992), scavenging in chimpanzees and other nonhuman primates is noteworthy mainly by its rarity (Hasegawa et al. 1983); in Gombe national Park, Tanzania, in over 34 years and an estimated 250,000 person hours of observation, fewer than 20 incidents of scavenging of animal carcasses have been recorded (Gombe Stream Research Centre, unpublished data; Goodall 1986). This is not simply because carcasses of large mammals are rarer in the woodland habitat of Gombe than they are in the savanna; Muller et al. (in press) present evidence that Gombe chimpanzees are equivocal in their treatment of carcass meat as a food source.” 883

Chimps may have an excellent reason for not feeling excited about carcass flesh as a food source: such flesh, found in a warm, moist climate, will certainly have large colonies of highly infectious and even deadly microbes. Chimpanzees who chose to use scavenged flesh on a regular basis would risk life- threatening gastrointestinal infections, dramatically reducing their chances of leaving a large number of offspring. As noted in Chapter 7 of this book, proponents of the idea that early human ancestors depended upon scavenging to an extent great enough to influence the evolution of human biology will need to account for the selection pressure that pathogens present in scavenged flesh would exert on the population.

Chimpanzee Hunting

Jane Goodall provides a table (Table D.1) of numbers of different species caught and eaten by Gombe chimpanzees during twenty-two years of observation.884 This provides some remarkable data, which I have re-tabulated (Table D.2) with some calculations.

883 Stanford CB. The hunting ecology of wild chimpanzees: Implications for the evolutionary ecology of Pliocene hominids. American Anthropologist 1996 March; 98(1): 96-113.

884 Goodall J. The Chimpanzees of Gombe. Harvard University Press, 1986. 269.

CHIMPANZEES – 295

Table D.1: Numbers of different prey species observed to have been caught and/or eaten by Gombe chimpanzees, 1960-1981. Year Number Red Bushpig Bushbuck Baboon Monkey Chimpanzee Rodent Bird Unidentified Total of months colobus 1960-63 33 4 3 2 0 1 0 0 8 5 23 1964-67 45 6 4 5 4 1 0 0 3 4 27 1968-69 24 3 2 1 12 0 0 0 0 1 20 1970-71 24 5 6 2 1 0 1 0 0 1 16 1972-74 36 42 9 9 1 4 0 1 4 1 70 1975 12 18 5 3 0 0 2 1 0 0 29 1976 12 19 10 3 0 0 2 0 1 0 35 1977 12 37 10 6 0 0 0 0 0 0 53 1978 12 32 9 6 0 0 0 0 4 0 51 1979 12 25 2 5 3 0 1 0 2 0 36 1980 12 16 0 4 2 0 0 0 0 0 22 1981 12 14 6 3 2 1 0 0 4 1 31 Note: From 1960 to 1974, researchers compiled data continuously but recorded it in larger blocks of time than in the years 1975-1981.

If animal flesh provided any essential nutrient for chimps, they all would need to eat it several times weekly, if not daily, but between 1960 and 1971, the Gombe chimps made less than one kill per month.

Further, even when some members of the troop have killed an animal, not all will consume meat. Goodall recorded the meat consumption of one chimp named Passion:

“Passion attended only 19 percent of the [meat-eating] sessions, was only seen eating meat during less than one third of these, and was never seen with large amounts.”885

Put this in context: Chimps spend at most about five percent of their feeding time eating animal flesh. Passion attended only 19 percent of this five percent, so she spent less than one percent of her feeding time at meat-eating sessions. Finally, she ate meat at only one-third of these sessions, which means she spent less than one-third of one percent of her feeding time eating animal flesh.

According to Wrangham and Gilby, well-fed adult males, who have the least nutritional need, eat most of the flesh consumed by troops, and the low-ranking females and young, who have the greatest need for additional energy and macronutrients, eat “little or no flesh.”886 That strongly suggests that chimpanzees do not have a nutritional requirement for animal flesh, protein, or fat.

885 Goodall J. The Chimpanzees of Gombe. Harvard University Press, 1986. 311.

886 Gilby IC, Wrangham RW. Risk-prone hunting by chimpanzees (Pan troglodytes schweinfurthii) increases during periods of high diet quality. Behav Ecol Sociobiol (2007) 61:1771–1779.

296 APPENDICES & BIBLIOGRAPHY

Remarkable Variations In Chimpanzee Hunting

The hunting behavior of chimpanzees at Gombe between 1960 and 1981 displayed some very interesting variations which suggest that this so-called hunting actually represents defense of food resources more than a drive for consuming animal flesh (Table D.1, originally provided by Jane Goodall). More recent observations of chimpanzee violence against humans support this interpretation.

According to Goodall’s data, in the period 1972-1974, the average kills per month more than doubled, and that was largely due to a four to five times increase in kills of red colobus monkeys (Table D.1). Thereafter, the average kills per month continued to increase through 1978, when it reached a high of 4.4, more than seven times the low of 0.6 in the period 1964 to 1967. Again, almost all of this was due to an increase in kills of red colobus monkeys. Colobus kills reached a high average of 3 monkeys killed per month in 1977, compared to a low average of only 0.12 kills per month in the period 1960 to 1963––a twenty-five times increase.

Chimpanzee hunting of colobus begs special explanation because it differs markedly from that of other mammals such as pigs and antelope, in that the former appears more deliberate and the latter more accidental:

“Hunts of red colobus frequently involve planning of execution: typically the hunters, in the course of plant food foraging, encounter a tree holding colobus and scan the tree crown for desired victims. By contrast, kills of pigs and antelope usually occur spontaneously as a chimpanzee party travels through undergrowth and happens upon a litter of piglets or a lone hidden bushbuck fawn, whereupon the prey is quickly grabbed and the hunters attempt to avoid defensive attacked by adults.”887

Note that chimps only hunt when they find prey while already foraging for plant foods, and that colobus hunting differs in that when a chimp troop sees a single colobus in the trees, the chimps pause to look for others and plan their attack on several of the monkeys. Thus, chimps hunt monkeys as a response to the presence of monkeys in the chimpanzee territory. This suggests that monkey hunting may arise from a need to defend territory and food resources.

Kortlandt has noted that by killing colobus monkeys chimps eliminate a potential food competitor.888 A comment by Stanford also suggests that chimpanzee hunting revolves around protection of plant food resources:

“The red colobus monkey composes more than 50 percent of the vertebrate prey items taken by all three best-studied chimpanzee populations; at two of them (Gombe and Tai) the species is

887 Stanford CB. The hunting ecology of wild chimpanzees: Implications for the evolutionary ecology of Pliocene hominids. American Anthropologist 1996 March; 98(1): 96-113.

888 Kortlandt A, cited by: Stanford CB. The hunting ecology of wild chimpanzees: Implications for the evolutionary ecology of Pliocene hominids. American Anthropologist 1996 March; 98(1): 96-113.

CHIMPANZEES – 297

approximately 80 percent of all kills…At Gombe, this is in contrast to early studies of predation (Teleki 1973) in which baboons (Papio cynocephalus anubis) were the major prey [Table D.1]. During the era of systematic banana provisioning at Gombe before 1971, baboons that were also attracted to the bananas were eaten regularly. Once provisioning was curtailed, baboons became a rare prey item and red colobus took over as the most frequently observed prey. It is likely that during the provisioning era, predation on red colobus was relaxed because the chimpanzees spent so much time in proximity to the feeding era where baboons were abundant but red colobus were seldom encountered.”889

In the provisioning era, they preyed upon baboons because the baboons invaded their banana supply. After the provisioning era, colobus monkeys invaded their territory as competitors for food resources, and they preyed upon those colobus monkeys. Thus, it seems possible that chimps have preyed primarily on those animals that intrude upon their food resources.

Table D.2: Numbers of total and red colobus kills by chimpanzees at Gombe, 1960-1981 (adapted from Table D.1). Year Number of months Red colobus kills Red colobus kills Total kills Kills per month per month 1960-63 33 4 0.12 23 0.7 1964-67 45 6 0.13 27 0.6 1968-69 24 3 0.13 20 0.8 1970-71 24 5 0.21 16 0.7 1972-74 36 42 0.86 70 1.9 1975 12 18 1.5 29 2.4 1976 12 19 1.6 35 2.9 1977 12 37 3.0 53 4.4 1978 12 32 2.7 51 4.3 1979 12 25 2.1 36 3.0 1980 12 16 1.3 22 1.8 1981 12 14 1.2 31 2.5

In fact, chimpanzee predation on colobus results in death of as much as 41 percent of the colobus population each year, and at Gombe, it appears to limit the red colobus population more than any other factor.890

“Since Gombe chimpanzees most often kill immature colobus (76 percent of all colobus kills….), it appears to be the hunting pattern of the chimpanzees that largely determines the size and composition of red colobus groups.”891

889 Stanford, The hunting ecology of wild chimpanzees , American Anthropologist 1996 March; 98(1): 96-113.

890 Ibid..

891 Ibid..

298 APPENDICES & BIBLIOGRAPHY

Thus, chimpanzees do limit the population of a major food competitor by preying upon the colobus.

Habitat and range loss presents another factor to consider. Over the years represented by the data in Tables D.1 and D.2, human encroachment continued to shrink the wild forest that includes Gombe chimps’ natural range. I would guess that the shrinkage of the forest led to a loss of habitat for the red colobus monkeys, which drove the monkeys to foraging in the chimp’s habitat, and this led to more contact and conflict between monkeys and chimps, many of these ending with chimps killing a monkey.

In support of this, in October 2012 the New Scientist reported that “Habitat loss may be to blame for an apparent spate of violent attacks by chimpanzees on humans in the war-torn eastern region of the Democratic Republic of the Congo (DRC).”892

“Reports of the scale and number of attacks are probably exaggerated, says Richard Wrangham of Harvard University, but he concedes that there has been an increase in tension between humans and chimps in that corner of the DRC – although only in areas where chimp habitat has been lost….

“Vernon Reynolds, a biological anthropologist at the University of Oxford, and author of The Chimpanzees of Budongo Forest, says he is aware of a few past incidents around Kasowka Forest in Uganda in which chimps have attacked humans after losing much of their food supply to farming.” 893

Local media in the Congo reported that chimps may have killed as many as ten people and injured seventeen more. If so, does anyone think that chimps have started hunting humans because human flesh contains some nutrient that chimps suddenly can’t get from any other source?

If habitat loss can drive chimps to attack the humans who have stolen the chimps’ habitat, then it seems plausible that the sudden, twenty-five times increase in incidents of chimps killing red colobus monkeys resulted from chimps and monkeys fighting over a shrinking food supply. The increase in bushpig killings probably also arose from an increase in encounters of chimps with bushpigs due to shrinkage of the bushpig range.

Stress due to the chimps being constantly under surveillance by the well-intentioned Goodall and other primatologists may also have contributed. Imagine having your every move tracked by another species day after day for a decade, and decide if it might not make you a little crazed.

892 Abraham C and O’Callaghan. Chimps attack people after habitat loss. New Scientist, 14:39 October 2012. Retrieved from http://www.newscientist.com/article/dn22369-chimps-attack-people-after-habitat-loss.html.

893 Ibid..

CHIMPANZEES – 299

In any case, the fact that the chimps dramatically increased their killing of other species in a very short period of time, with a focus on killing a potential competitor for food, suggests strongly that chimps kill other species for non-nutritional reasons, not because they require any nutrient found in animal flesh.

Chimps Probably Do Not Hunt To Obtain Macronutrients

For chimps, hunting has a high risk of injury, a high energy cost, and a low return on investment, making animal flesh a high-risk food item.

“Chimpanzees prey most frequently upon red colobus monkeys, Procolobus spp. (Uehara 1997; Mitani and Watts 2001). Meat of these and other species is clearly prized by chimpanzees…However, it is also risky to acquire because many hunts fail completely. The failure rate is roughly 50% at Taï National Park, Côte d’Ivoire (Boesch and Boesch-Achermann 2000) and Gombe National Park, Tanzania (Gilby et al. 2006) and 16% at Ngogo, Kibale National Park, Uganda (Mitani and Watts 2001). Hunts of red colobus involve frequent rapid climbing, indicating high-energy expenditure (Pontzer and Wrangham 2004). They average 18.9 min in duration and can last for as long as 120 min (Goodall 1986; Boesch and Boesch 1989). Thus, meat is a high-risk food item compared to plant matter.”894

The hypothesis that chimps pursue animal flesh to secure specific essential macronutrients provided by flesh lacks evidential support:

“In theory, it is possible that chimpanzees hunt in response to shortages of specific macronutrients rather than energy in general. Protein is the most likely candidate, but Conklin- Brittain et al. (1998) demonstrated that protein intake varies little for the Kanyawara chimpanzees and is always high in relation to nutritional needs. Also, the individuals most at risk of specific macronutrient shortage would presumably be low-ranking females and young. However, meat is eaten mainly by adult males, whereas some females and young eat little or no meat. Thus, it is unlikely that hunting patterns are driven by specific macronutrient deficiencies as opposed to an appetite for energetically valuable food.”895

The idea that they pursue prey to obtain a high energy or fat intake also fails to fit the evidence. Palm nuts provide a much higher energy return than meat with much less risk:

“At least one important food in the chimpanzee diet, the oil palm nut (palmae, Elaeis guineensis), is known to have eight times as many calories per kilogram and to be higher in unsaturated fat than monkey meat.... Oil palm trees are abundant and at least some are

894 Gilby IC, Wrangham RW. Risk-prone hunting by chimpanzees (Pan troglodytes schweinfurthii) increases during periods of high diet quality. Behav Ecol Sociobiol (2007) 61:1771–1779.

895 Ibid.

300 APPENDICES & BIBLIOGRAPHY

in fruit year-round at Gombe. Any cost-benefit analysis of foraging decisions by chimpanzees at Gombe or elsewhere must take into account the tradeoff between easily available palm nuts and more energetically expensive hunts for colobus meat.”896

Since palm nuts provide far more energy than monkey flesh, and only a very small percent of the chimpanzee diet consists of flesh, it seems unlikely that chimps hunt monkeys primarily to obtain food, and more likely that they hunt monkeys primarily to protect their higher value plant resources from those competitors.

Moreover, chimpanzees spend the most time hunting when they have abundant supplies of high-quality fruits, and when supplies of high quality fruits have waned and the chimps have a relatively low energy and macronutrient intake, they focus their efforts on gathering fruits or nuts, not on hunting. 897

This indicates that the chimps will invest in hunting only when they have a surplus of high quality fruits which can energetically subsidize hunting, allowing them to take a risk and “splurge” on a nutrient and caloric expenditure that might not provide a nutritional return equivalent to the expenditure.

An animal nutritionally dependent upon flesh would not show this variability in pursuit of prey, but would hunt with equal frequency regardless of the supply of plant foods.

How Well Do Chimpanzees Digest Animal Flesh?

This gains plausibility when we consider that an obligate omnivore would have no difficulty consuming or digesting flesh, but chimps have notable difficulty with it. Jane Goodall reports the following:

“Almost every morsel [of meat] is chewed up together with a wadge of leaves, sometimes dead ones. These wadges, although they may be swallowed, are usually discarded along with any unwanted portion of the meat, such as pieces of bone or skin…Chimpanzees suck, chew, and may even swallow small bones and bone fragments, as well as pieces of skin, especially individuals who have been unable to acquire juicier portions. They also chew the leaf-meat wadges that have been discarded by their luckier companions.”898

This suggests that chimps don’t always succeed in swallowing the chewed meat, but suck the juice out then discard the “leaf-meat wadges.” This would likely occur because the chimp has relatively blunt, non-shearing molar teeth that would mash but not efficiently cut raw meat into small enough bites to swallow. As discussed in Chapter 6, chimpanzees teeth have a lower shearing quotient than gorilla teeth. In addition, this passage emphasizes that some of the time that some chimp spends “eating meat”

896 Stanford CB. The hunting ecology of wild chimpanzees. American Anthropologist 1996 March; 98(1): 96-113.

897 Gilby IC, Wrangham RW. Risk-prone hunting by chimpanzees (Pan troglodytes schweinfurthii) increases during periods of high diet quality. Behav Ecol Sociobiol (2007) 61:1771–1779.

898 Goodall, op. cit., 296.

CHIMPANZEES – 301

actually records the time he spent eating the “leaf-meat wadges” discarded by some other chimp. In other words, it represents one piece of meat “eaten” twice.

Goodall provides further evidence of the difficulty chimps have with meat-eating:

“Meat is eaten slowly. One old male, Hugo, fed on the body of a large infant baboon for almost nine hours. When he finally abandoned the carcass to the other chimpanzees present (who had been able to obtain only very small scraps before), the head, arms, legs, and part of the torso still remained.”899

A large infant baboon weighs about one kilogram (2.2 pounds).900 About sixty percent of the live weight of a mammal consists of edible tissue; hence a large infant baboon could have a total of about 600 grams (1.3 pounds, or 21 ounces) of edible tissue. Wild mammalian flesh supplies only about 140 kcalories per 100 gram portion, so this baboon would have had about 840 total kcalories if consumed completely.

Assuming a chimp could successfully chew the flesh into small enough bits to swallow, and he consumed all of the edible portions of the baboon carcass, he would have spent more than half of his waking hours to obtain less than half of his daily caloric requirement, a ridiculously inefficient enterprise that could only be sustained if plenty of more digestible foods, i.e. fruits, were available.

Also, assuming that Hugo ate all of the flesh on the baboon carcass, his rate of consumption would have amounted to sixty-six grams per hour, a very slow pace indicating poor equipment for consuming flesh.

However, Goodall states that Hugo left the arms, legs, and part of the torso, despite spending nine hours feeding upon it. This means that he derived far less than 840 kcalories from it. One large fig supplies about 47 kcalories.901 A chimp (or human) can easily eat twenty figs in one hour, obtaining 940 kcalories. Then consider that to get meat often requires considerable energy expenditure in chasing and subduing the animal, compared to picking fruit, which doesn’t run or resist capture. For chimps, the cost-benefit ratio of meat-eating certainly lies much higher than that for fruit-eating.

Even if chimps succeed in swallowing some of the meat they eat, it appears that some portion of it goes completely undigested, according to Goodall’s report:

“During the year when chimpanzee feces were regularly examined, we could tell immediately when chimpanzees had been eating meat, as the sample were full of hair, bones, even lumps of flesh. One sample yielded a monkey finger, another an ear, and a third an incredible five inches

899 Goodall, op cit., 296.

900 Primate Portal: An Introductory Guide to Resources in Nonhuman Primate Research. Normal body weight of the infant baboon. http://www.primateportal.org/normative-values/normal-body-weight-infant-baboon .

901 USDA Food Nutrient Database

302 APPENDICES & BIBLIOGRAPHY

of tail, bone, and all! One morning, after Mike had been eating bushbuck meat, he picked pieces of flesh out of his own dung and ate them.”902

Since these chimpanzees do not even completely digest the flesh that they eat, we can’t estimate its nutritional contribution to their diet based on the known nutritional value of animal flesh. We would need a controlled study in which we fed chimps a defined amount of raw flesh, then measured how much of that flesh passed undigested into the feces, to have the ability to calculate the efficiency of chimpanzee digestion of raw flesh.

Nevertheless, Goodall’s reports drive home a very important point: although chimps eat flesh, they may not digest it very well. Since clearly chimps spend a lot of time eating insects or meat with little nutritional return, representing the role of flesh in the chimpanzee diet by citing hours spent in feeding grossly overestimates the nutritional contribution of insect or animal flesh to the chimp diet.

In short, chimpanzees have just enough physiological equipment to engage in flesh-eating, but probably not enough to survive on hunting and meat-eating, which explains why they all focus on gathering plants, not on hunting, when they have low supplies of high-quality fruits.903

Since both insect- and meat-eating have poor nutritional return for time investment compared to eating fruit, and some chimps, particularly females, spend very little if any time eating flesh, we can conclude that chimps do not require animal flesh.

Stanford summarizes the caloric contribution of flesh to the diets of chimpanzees and early hominids:

“In both chimpanzees and many hunter-gatherer societies, the dietary contribution of calories from meat is relatively small, with the amount of meat consumed varying seasonally according to the availability of prey animals and alternative plant foods. Presumably, early hominids also had a diet largely made up of plant foods (Sept 1992, 1994).”904

902 Goodall, op cit., 298.

903 Gilby IC, Wrangham RW. Risk-prone hunting by chimpanzees (Pan troglodytes schweinfurthii) increases during periods of high diet quality. Behav Ecol Sociobiol (2007) 61:1771–1779.

904 Stanford CB. op. cit..

CHIMPANZEES – 303

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