Copyright

William Collins

An imprint of HarperCollinsPublishers 1 London Bridge Street London SE1 9GF WilliamCollinsBooks.com This eBook first published in Great Britain by William Collins in 2020 First published in the United States by Houghton Mifflin Harcourt in 2020 Copyright © David Raubenheimer and Stephen J. Simpson 2020 Cover images © Shutterstock David Raubenheimer and Stephen J. Simpson assert the moral right to be identified as the authors of this work. A catalogue record for this book is available from the British Library. All rights reserved under International and Pan-American Copyright Conventions. By payment of the required fees, you have been granted the non-exclusive, non-transferable right to access and read the text of this e-book on-screen. No part of this text may be reproduced, transmitted, down-loaded, decompiled, reverse engineered, or stored in or introduced into any information storage and retrieval system, in any form or by any means, whether electronic or mechanical, now known or hereinafter invented, without the express written permission of HarperCollins. Source ISBN: 9780008359218 Ebook Edition © June 2019 ISBN: 9780008359232 Version: 2020-02-26

To Jacqueline, Gabriel, Julian, Jan, and Fred

–DR

To Lesley, Alastair, Nick, and Jen

–SJS

Contents

Cover

Title Page

Copyright

Dedication

Introduction

1. The Day of the Locusts

2. Calories and Nutrients

3. Picturing Nutrition

4. Dance of the Appetites

5. Seeking Exceptions to the Rule

6. The Protein Leverage Hypothesis

7. Why Not Just Eat More Protein?

8. Mapping Nutrition

9. Food Environments

10. Changing Food Environments

11. Modern Environments

12. A Unique Appetite

13. Moving the Protein Target and a Vicious Cycle to Obesity

14. Putting Lessons into Practice

More on Nutrients

Acknowledgments

Further Reading

Index

About the Author

About the Publisher

Introduction

Stella lived in a community on the outskirts of Cape Town, South Africa. She was one of twenty-five adults who between them had an impressive forty children. It was a serene setting on the foothills of Table Mountain, surrounded by vineyards, pine plantations, groves of eucalyptus trees, stretches of natural fynbos vegetation, and a few suburban settlements.

Caley Johnson was a young anthropology student from New York City. Her graduate thesis was on nutrition of a rural population in Uganda, who lived almost entirely off natural foods. Her advisors suggested that it would be an interesting comparison to include in the study a population that ate not only natural foods but also some sugary and fatty processed foods. This is what brought Caley to Cape Town, where she and Stella met.

Caley’s research approach, standard for her field, involves watching individuals throughout an entire day and recording which foods they eat and how much of each. The foods are then analyzed in a laboratory for their nutrient content to give a detailed daily record of the diet. But this study was radical in one respect: rather than follow several subjects, each on a separate day, the team had decided to study the diet of only one individual for thirty consecutive days. Caley therefore came to know Stella and her eating habits intimately.

What she saw was intriguing. Stella’s diet was surprisingly diverse: she ate many foods, almost ninety different things over thirty days, and on each day, she ate different combinations of natural and processed foods. This suggested that Stella was not particularly discerning, indiscriminately eating whatever she fancied. The numbers from the nutrient laboratory appeared to tell the same story. The ratio of fats to carbohydrates in Stella’s diet varied widely, as might be expected given the variety of foods that she ate and how these differed from one day to the next.

Then Caley noticed something unexpected. When she totaled the combined calories from carbs and fats each day and plotted that figure on a graph against the amount of protein consumed each day, there was a tight relationship. This meant that the ratio of protein to fats and carbs—a very important measure of dietary balance—had remained absolutely consistent over the course of an entire month, regardless of what Stella had eaten. What’s more, the ratio that Stella had eaten each day—one part protein to five parts fats and carbs combined—was the same combination that had been proven to be nutritionally balanced for a healthy female of Stella’s size. Far from being indiscriminate, Stella was a meticulously precise eater who knew which dietary regimen was best for her and how to attain it.

But how did Stella track her diet so precisely? Caley knew the complexities of combining many foods into a balanced diet—even professional dietitians have to use computer programs to manage this. Could it be, she might have been forgiven for wondering, that Stella was secretly an expert in nutrition? Except that Stella was a baboon.

A confounding story, when you consider all the dietary advice we humans seem to require in order to eat properly (not that it does most of us a lot of good).

Meanwhile, our wild cousin, the baboon, apparently has figured it all out by instinct. How could such a thing be so?

Before we begin to explore that question, here’s another tale, even weirder. It starts with a lab scientist named Audrey Dussutour at the University of Sydney. One day Audrey took her scalpel and started preparing an experiment by cutting a gooey blob of slime mold into small pieces. Beside her on the bench sat hundreds of Petri dishes, all set out neatly in rows.

Audrey picked up each fragment of yellow goo with forceps and carefully transferred it into the center of a dish, then covered it with a lid. The dishes contained either small blocks of protein or carbohydrate, or a wheel of eleven tiny bits of jelly-like food medium varying in the ratio of protein to carbs. Once all dishes had received their bit of slime mold, Audrey stacked them in a large cardboard box and left them overnight.

The next day, she opened the box and laid out the dishes again on the bench. When she looked closely, she was astonished. Each bit of goo had changed overnight. When the slime molds were offered two blocks of food—one of protein, the other of carbs—the blobs extended their growing tendrils to both nutrients, reaching out just far enough in each direction to pull in a mix of the two. That mixture contained precisely two parts protein to one part carbs. Even more incredibly, when bits of goo were placed in dishes containing eleven different food blocks, the tendrils grew overnight from the center of the dish to colonize only the blocks containing that same two-to-one nutrient mixture, ignoring the rest.

What is so special about a diet of two parts protein to one part carbs? The answer came when Audrey placed pieces of slime mold into dishes containing differing combinations of protein and carbohydrate. The next day, some bits of slime remained stunted, whereas others had grown dramatically, extending themselves across the dish in a lacy network of pulsing yellow filaments. When Audrey later mapped the growth of the blobs, it was as if she had charted the up-and-down contours of a mountain. Goo placed on a nutrient that was two parts protein to one part carbs sat at the summit of the growth mountain. As the proportion of protein fell and carbs rose, or vice versa, the blobs’ growth decreased. In other words, when the bits of slime mold were given the chance to select their own diet, they chose precisely the mixture of nutrients needed to optimize healthy development.

Audrey’s yellow goo with the remarkable nutritional wisdom is a creature with the scientific name Physarum polycephalum—literally, many-headed slime. It is the real-life version of The Blob of B-movie fame. It is seldom seen, but like other slime molds (including the wonderfully named dog’s-vomit slime mold) and fungi, it lives a secretive life among the leaf litter, logs, and soils of the world’s forest floors. It is a single-celled creature with millions of nuclei, which can regenerate itself from tiny pieces, crawl like a giant amoeba, and grow its own complex, reticulated architecture of tubes that pulse and distribute nutrients around its network. It simply creates tentacles and then reaches out with them to grab whatever it wants to eat. Fascinating, if a little horrifying.

Now, we may be able to accept that Stella the baboon can make some wise nutritional decisions. But how can a single-celled creature without organs or limbs, let alone a brain or a centralized nervous system, make such sophisticated dietary choices and then carry them out?

This puzzled us, too, so, we asked an expert.

Professor John Tyler-Bonner passed Steve a laboratory beaker filled with steaming coffee, freshly brewed on the naked blue Bunsen burner flame that hissed quietly on the teak benchtop. Steve sat discussing Audrey’s results with this venerable guru of slime mold biology in John’s office—a time capsule that has not been refurbished since 1947, when John first arrived on faculty at the Department of Ecology and Evolutionary Biology at Princeton University. He pioneered the study of slime molds, and his work has helped lay the foundation for the study of complex decision-making within distributed entities, such as bird flocks and fish schools, crowds of people, or global corporations.

John explained that each part of the blob senses its local nutritional environment and responds accordingly. As a result, the entire blob acts as if it is a single sentient being, seeking out optimal sources of food—a balanced diet that will ensure favorable health—and rejecting what does not serve that goal.

This, you may agree, is better than what is achieved by some other sentient beings we could name. And this, as you probably realize by now, has everything to do with the subject at hand.

Why have we, two entomologists, written a book about human diet, nutrition, and health, a subject on which quite a few experts have already weighed in (no pun intended)? We didn’t start out meaning to do any such thing. Throughout our lives as scientists, and especially during the first two decades of our thirty-two-year collaboration, we have studied insects in an attempt to solve one of nature’s most enduring riddles: How do living things know what to eat?

Answer that and you’ve learned something very important—possibly even useful—about life itself. And not just for insects. But we’re getting ahead of ourselves now. Better to start at the beginning.

1
The Day of the Locusts

THE YEAR IS 1991. WE ARE SITTING TOGETHER AT Steve’s computer in his office in the Oxford University Museum of Natural History—the same place that in 1860 hosted the “great debate” over Darwinian evolution between Thomas Henry Huxley and the Bishop of Oxford, Samuel Wilberforce. That legendary encounter is best remembered for a heated exchange in which Wilberforce supposedly asked Huxley, who was known as Darwin’s “bulldog,” which of his grandparents was descended from monkeys. Huxley is said to have replied that he would not mind having a monkey as his ancestor, but he would be ashamed to be related to someone who used his great gifts to obscure the truth.

We had just performed the biggest dietary experiments we’d ever attempted. The study involved locusts, which are a special type of grasshopper and, as we will explain below, the ideal animal for our study.

Little did we know that before our session that day was over, the seeds for a new approach to nutrition, one heavily dependent on Darwin’s theory, would be sown.

We wanted to answer two questions. First, do animals decide what to eat based on what’s best for them? And second, what happens if for some reason they fail to follow that diet and eat another one instead?

You can see how these answers might be somewhat important.

Twenty-five foods had been carefully prepared in the lab to differ in the balance of protein to carbs, the two main nutrients consumed by herbivorous insects such as locusts. The foods ranged from high protein/low carb (a bit like meat) to high carb/low protein (more like rice) and everything in between.

Despite their varying compositions, the foods all looked very similar: they were dry and granular, a bit like cake mix before adding the liquid. The insects seemed to like them.

The mixtures were fed to the locusts, each of which could eat as much as it liked, but only of the single food it was given, until it molted to become an adult. This took a minimum of nine days and up to three weeks, depending on the food. Logistically, then, quite a challenge—painstakingly preparing twenty-five different foods, feeding one to each of two hundred insects, and then meticulously measuring how much every individual had consumed each day.

During the experiment, we spent what felt like endless hours together deep in the bowels of the Zoology Department in a cramped, humid room heated to 90 degrees Fahrenheit—a temperature at which desert-living locusts thrive but which can test a human friendship. Music helped—John Cale and Talking Heads kept us sane. Each locust lived within its own plastic box, with a metal perch to rest upon, a small dish of its assigned food that had been weighed to the nearest tenth of a milligram, and a water dish.

Every day we had to remove each locust’s food dish and, like meticulous sewerage workers, pick out any pellets of locust poo from the food dish and box. We measured how much was eaten and digested by weighing food dishes before and after feeding and analyzing excrement. Every food dish had to be placed in a desiccator to dry off any moisture and was then reweighed on a set of electronic scales that could detect a change of one hundred thousandths of a gram. By measuring the difference in weight of the food dish before and after feeding, we calculated how much the insect had eaten that day, and from that we could determine exactly how much protein and carbs it had consumed.

We did this for all two hundred locusts day after day until they either successfully molted to become winged adults or died beforehand. We recorded how many days that took, measured the animal’s weight, and analyzed how much fat and lean tissue they had grown.

And then, at last, we were side by side at Steve’s computer, about to learn the results of the experiment. In order to understand the results, we should first take a look at locusts in their natural context. After all, they didn’t evolve while living in a basement lab at Oxford. And, as we show throughout this book, nothing about nutrition makes sense unless you understand the biological context in which the species evolved, ours included.

Two juvenile locusts, somewhere in North Africa.

One grew up on her own. It hasn’t rained locally for months, and other locusts are few and far between. She is a beautiful shade of green, which allows her to blend in with the vegetation. She has a solitary existence, being shy in her behavior and repelled by other locusts. For good reason: one locust can hide; larger groups will attract unwanted attention from hungry birds, lizards, and hunting spiders.

Elsewhere, another locust was reared in a crowd. It rained not so long ago, and others like her are around in large numbers, feasting on the abundant vegetation. She is a party animal—brightly colored, very active, and attracted into groups. These aggregations form marching bands, and when they become winged adults, flying swarms that migrate across vast areas of Africa and Asia. A plague of the desert locust in North Africa can contain hundreds of billions of insects and eat as much in a single day as the entire population of New York will in a week. When they move into agricultural areas, they are devastating (locusts, not New Yorkers).

The two locusts are not different species (as was thought originally)—they could even be sisters. Every one of their kind has the potential to become either a shy green grasshopper or a gregarious extrovert, depending on whether they grow up alone or in a crowd. The process of changing from one form to the other occurs quickly. If you took the solitary green grasshopper and put her in a crowd, within an hour she would be attracted rather than repelled by other locusts, and a few hours later she could be part of a marching band. Before long she will change from green to being brightly colored.

This transition is known as density dependent behavioral phase change, and Steve’s research group spent years trying to understand it.

One of the initial questions we had was this: What is it about being in a crowd that causes the change? What stimuli are provided by other locusts that might trigger the transition? Could it be the sight of them, their smell, their sound?

As we discovered, touch is what’s critical. When there is a limited availability of suitable food plants, solitary locusts are forced to forage nearer each other than they’d prefer. The congregated insects jostle one another, and this physical contact causes the change from repulsion to attraction.

Once enough gregarious locusts come together, suddenly, as if of one mind, the entire group becomes highly aligned and starts to march.

We found that the collective decision to start marching emerges within a crowd from simple local interactions among locusts. In other words, there is no leader locust or hierarchical control. Marching emerges because the locusts are all following one easy rule: “align with your moving neighbors.” Once a critical density of locusts is reached, just adding one or two more will suddenly cause the transition to collective, aligned movement. The terrible march has begun.

Of course, we still didn’t understand why locusts should follow the simple rule to align with their moving neighbors. We suspected that nutrition may play a role—as it does in most things. The answer came from our study of a related animal called the Mormon cricket, and it turned out that their motive was rather sinister.

The Mormon cricket is a large, flightless insect built like a small tank that lives in the southwestern United States and forms vast marching swarms extending miles. They are called this because they began to devastate the first crops planted by the Mormon pioneers after arriving at Salt Lake in 1848. The community was powerless to stop the destruction and were facing starvation until, in the nick of time, a flock of seagulls came to the rescue and ate the crickets. There is now a monument to the gulls commemorating this event at the Temple in Salt Lake City. The seagull is the state bird of Utah (an odd thing, considering that it’s landlocked, but gulls find their way to any large body of water).

Steve was in Utah, studying swarms of Mormon crickets with colleagues Greg Sword, Pat Lorch, and Iain Couzin, when they discovered the reason behind its sudden decision to align and begin marching. As Steve explains:

We were staying in a truck stop motel, eating junk food washed down with Polygamy Porter (slogan: “Why have just one?”). The crickets were about in huge numbers. Greg and Pat had radio-tracked vast bands moving up to two kilometers each day through the spectacular sagebrush country.

Here’s a clue to why all those crickets were migrating. We recorded a single band of them crossing a main road for five continuous days. When they got squashed by cars, those following behind stopped to eat the corpses. And got squashed by cars. Before long, the mess was ankle deep, and snowplows had to be dispatched to clear the greasy slurry.

But why might herbivorous insects so avidly eat one another, even to the point of mass suicide? After all, with lots of vegetation around, there were plenty of other things for them to consume.

We had brought along to the desert the same dry, powdery feeds used in our big locust study back at Oxford, and we laid dishes of it out in front of the marching cricket bands.

The result was revealing. The crickets ignored the dishes of high-carb food but stopped to eat from the ones containing protein.

And aside from our little buffet, what was the nearest source of high-quality protein to those crickets? The cricket in front. What was forcing the march was simple: if you don’t move forward when your neighbors to the rear do, they will eat you. Meanwhile, of course, if the creature in front of you stops, you may seize upon it as a meal. Cricket cannibalism was driven by a powerful appetite—for protein.

And we discovered that locust habits can be equally gruesome when it comes to hungering for that nutrient. We learned this inadvertently, when Steve was trying to explore the signals that tell locusts when they are full during a meal. In an experiment, he had laboriously cut the nerves carrying feeling from the end of the insects’ abdomens to their brains. After the surgery, he put all the locusts in the same box to recover. Next morning, when Steve looked, he saw that none of the locusts had a body left below the point where the nerve had been cut. The insects had formed a kind of daisy chain, chewing off the hind end of the locust in front (who couldn’t feel a thing) while at the same time having its own numbed abdomen eaten by the locust behind.

What better animal, then, to use for testing big ideas in nutrition science? If any species would be expected to be gluttonous and eat as much as possible of whatever the food provided, then voracious swarming locusts are it. But we knew that locusts are not so simple-minded—they can regulate their intake of nutrients, notably protein, even if that requires consuming their neighbors. What would the results of our big experiment show?

Before we find out, we first need to provide a short primer on nutrition.

CHAPTER 1 AT A GLANCE

1 We began our journey by describing an experiment on locusts, which pioneered a new approach to the study of nutrition.

2 We discovered that an appetite for protein is behind locusts’ reputation as plague-forming scourges of agriculture.

3 Will an appetite for protein play similarly important roles elsewhere in the animal kingdom? Even for us?

2
Calories and Nutrients

GIVEN THAT NUTRITION IS SO INFERNALLY complicated, let’s ask a simple question: Why must we eat?

Certainly, food today has become the source of a great deal of confusion and anxiety, which is a terrible pity because food is also the source of so much that is good—excellent, in fact. Food binds us together socially and culturally. It gives a great deal of pleasure while also providing the stuff that fuels life itself.

Energy is the most familiar of the things we need from food. Not a day goes by without seeing numbers written all over our foods, meals, and now also menus—like mathematical graffiti saying how much energy they contain and stern dietary guidelines warning how much of it we should eat. The labels don’t use the word energy, of course. You’re probably more familiar with the term Calories.

But what exactly is a Calorie?

It’s simply a unit of energy—a single Calorie is the amount of energy needed to raise the temperature of 1 kilogram (2.2 pounds) of water (which is the same as a liter) by 1 degree Celsius, from 14.5 to 15.5 C. Yes, this is a bizarre currency indeed, except, perhaps, if you have ever wondered how much food it takes to heat a bathtub. But it is rigorously exact, which we scientists tend to like. And so, everyone is stuck thinking in calories, even though they are hard to picture.

To confuse things further, you may also see calories written as kilocalories (kcal). This is because 1 Calorie (with a big “C”) equals 1,000 calories (with a small “c”). You may also have seen the energy content of a food presented as kJ—kilojoules, which is what we scientists mainly use, along with kcal. These units have an even more unlikely-sounding definition: 1 kJ is the energy needed to move a 1-kilogram (2.2-pound) weight by a force of 1 Newton (which is itself a measure of gravitational pull), over a distance of 1 meter. One kilojoule equals 0.239006 Calorie (to be exact!).

In this book we will mainly use “kcal” when presenting units of energy, but on occasions when presenting scientific results, we will use “kJ.” Throughout, we will use “calories” with a small “c” as a generic term for “energy.”

This means we determine the energy contained in food based on its theoretical power to fuel action—to heat water or move weights.

All food contains calories, with the exception of water, which is just as well, because without energy, our bodies wouldn’t be able to do anything, including make use of the other important thing we take from food: nutrients. Energy comes from the main nutrients in our diet—the macronutrients, as they are known—each of which is chemically different. Once we consume these nutritional fuels—proteins, carbohydrates, and fats—they are broken down into smaller molecules that are burned within our cells.

Macronutrients deliver more than just energy, however. Proteins and their building blocks, the amino acids, also supply nitrogen, with which we make all sorts of other important things, including hormones, enzymes, and the information-storing molecules DNA and RNA. If we don’t ingest protein, we don’t live.

In the popular mind (and in many diet books), fats and carbohydrates (carbs) have almost become just another way of saying “Calories,” but there is a lot more to them than that. Fats insulate us from the cold, store vitamins, lubricate the skin, and cushion our eyeballs and joints. Their fatty acid building blocks make up the membrane that surrounds every cell in our bodies, and special fats called sterols serve as messengers that help coordinate the complex chemistry that keeps us alive.

We can’t do without fats.

Carbohydrates include sugars, starches, and fibers. Like proteins and fats, most carbs are built of smaller units, in this case, simple sugars such as glucose and fructose. The nutritional properties of different carbs depend on which simple sugars they consist of and how they are strung together. The most abundant carbohydrate on our planet—the plant fiber cellulose—has its glucose units strung together so tightly that we can’t digest it.

Glucose is particularly important because it’s the main carbohydrate on which our bodies depend. In addition to providing energy, glucose partners with the nitrogen from protein to build DNA and RNA.

Our bodies can create glucose by breaking down proteins and fats, so, strictly speaking, we don’t have to eat any carbs to get glucose. But that is not the same thing as saying we don’t need to eat carbs at all—as we will show later.

A schematic showing the relationship between foods, nutrients, and energy.

And those are just the macronutrients. Vitamins and minerals are needed, too, though in tiny amounts compared with the big three, which is why they are called micronutrients. These are used by the body for too many purposes to mention here. But keep in mind that sodium, calcium, magnesium, chloride, and potassium all generate electrical currents that quite literally make us tick—our hearts beat and our nerve cells crackle with electrical impulses.

The diagram above provides a summary of what’s in food. Should you want to know more about the different boxes in the diagram, check out More on Nutrients, which may also be of use at specific points when reading the rest of the book.

As we can see from the diagram, foods are complex mixtures of many nutrients; not to mention diets, which are themselves complex mixtures of foods. To understand nutrition, we need to think not in terms of single nutrients but rather the balance of nutrients in these mixtures.

If an animal is to thrive, it needs to eat macro- and micronutrients in the right amounts—like Goldilocks, not too little, not too much. Some animals, such as parasites living within the body of their host, get all the nutrients they need, and in the right balance, from a single food source. For them, choosing the proper diet is easy. All mammals, including ourselves, are lucky to start life in such ideal circumstances—because mother’s milk is as close as we’ll ever come to a perfectly balanced diet. It contains, in proper proportions, everything a newborn needs to grow. But after a mammal is weaned, nutrition becomes a much trickier undertaking.

It’s easy to see why. The things we eat are made up of nutrients in almost endless combinations. Some foods are richer in protein, others in fats or carbs—but all are mixtures. There are no single-nutrient foods. Pasta and bread certainly live up to their carb-rich reputations, but about 10 percent of the energy they contain comes from protein. A steak is a protein powerhouse but more than half of it is water, along with lots of fat and minerals, too.

We humans complicate matters even further because, unlike other animals, we tend not to eat single foods; rather, we assemble them into recipes and meals. Then we combine meals into varied diets and dietary patterns, sending complex mixtures of nutrients and other substances into our bodies, where they interact with our physiology.

Now, imagine having to consciously navigate and balance the proper mixture of all that on a thrice-daily basis. We would all need PhDs in mathematics and computing, and even then the calculations wouldn’t leave us time to do much else.

Thankfully, as Stella the baboon and the slimy blob showed us, nature is capable of handling complex challenges like this one without mathematics and computers. The solution is simple and elegant—and exists inside every living thing, as we shall see before long. But first, back to Oxford.

CHAPTER 2 AT A GLANCE

1 The key players in nutrition are calories, macronutrients (protein, carbs, and fat), micronutrients, and fiber.

2 You can check out More on Nutrients for extra detail.

3 Nutrition is about more than single things (fat, sugar, protein, or whatever)—it’s about mixtures of dietary nutrients and about their balance.

4 Mixing a nutritionally balanced diet seems daunting, but animals in the wild do it instinctively. How do they do it—and why is it so hard for us?

3
Picturing Nutrition

WITH CALORIES AND NUTRIENTS IN MIND, LET’S return to Oxford, where we left off in Chapter 1 sitting side by side at Steve’s computer to view the results of our big locust experiment. As was (and still is) usual for us, the first step was to make a simple visual representation of the data—a graph.

The graph itself looked like a large letter L. The vertical line, or axis, is where the computer would mark how much carbohydrate an insect ate in milligrams (mg). The horizontal axis would show how many milligrams of protein that locust consumed. Before we show the actual results, to help explain how to read the graph, here’s the hypothetical example of a locust that ate 300 mg of carbs and 200 mg of protein:

A graph showing how the intake of a locust eating 300 mg carbs and 200 mg protein would be plotted.

When we plotted the actual results for all the locusts across all the diets, we saw something fascinating. The intake points fell neatly along a line, rising like a drifting plume from the horizontal axis. So astoundingly simple was the pattern, that at first we suspected there was a problem with our arithmetic. We checked it and double-checked it. All was right.

Then we realized what we were seeing was real and important—although at the time, we didn’t know just how important. We were seeing, for the first time, how appetites for different nutrients interact to deal with nutritional imbalance. And, we already knew, dealing with nutritional imbalance is a big deal, a very big deal, in the natural lives of animals—it is essential for success. More than that, we had invented a new approach, which can be applied to any species, for unravelling the mysteries of eating. We called this Nutritional Geometry.

The plot of results from the locust experiment. Each point shows the protein and carbohydrate intakes (as illustrated in the previous plot) of locusts fed one particular diet. Note how the points rise upward in a plume. Each point shows the average intake of one group of locusts.

Having graphed the results, the next step was to work out which of the diets was closest to being nutritionally balanced for a locust. For that, we identified the mixture of protein and carbs that allowed locusts to grow and survive best—essentially, the healthiest nutrient balance possible. We called this the target diet and have marked it on the next graph with a bull’s-eye.

As you might imagine, the target is rather important not just for the locusts but for the concept of Nutritional Geometry itself. It allows us to see, at a glance, which diets are best balanced (the black points near the bull’s-eye) and which are imbalanced—all the rest. The further from the target, the more imbalanced. We can also see how exactly a diet is imbalanced. Those points above the target show locusts that ate too much carbs; those below ate too little. Only those on the target ate exactly the right amount!

The bull’s-eye shows the diet that supported best survival and growth. Other points can then be interpreted relative to this target diet.

With those simple concepts in place, you can see something else that is important in our results. The locusts that ate too much carbs all line up vertically close to in line with the protein target, getting a similar amount of protein (about 150 mg, which is approaching the target of 210 mg). But to do so, they have had to overeat carbs—by a lot. And eating those extra carbs came at a cost—well, two costs. First, it took time. It meant that locusts on the low-protein, high-carb diets had to extend the period until they molted to become winged adults. The longer a locust delays getting to adulthood, the more likely it is to be eaten by a bird, lizard, spider—or another locust—before getting a chance to reproduce. The second price they paid is something you wouldn’t readily associate with an insect: locusts on the high-carb diets became obese. Granted, it’s hard to tell that a locust is fat, because its skeleton is on the outside. But it’s chubby on the inside, like an overweight knight wedged into a suit of armor a few sizes too small.

Locusts overate on high-carb diets to reach the protein intake target. But what about low-carb diets? Here we need to focus on the locusts below the bull’s-eye in the graph. You can see that the pattern of dots bulges out a bit to the right, meaning that the locusts’ protein intake was a bit higher than their target but way down on carbs. As a result, they were too lean and less likely to survive to adulthood compared with locusts on the target diet. Their body fat stores were so low that they would have been unable to fly far or live for long in the wild.

Once again: on high-carb feed, the insects had to keep eating (in order to get all the protein their bodies demanded), and they ended up consuming more carbohydrate than needed, becoming fat, and having to delay development. On low-carb food, they took in less carbohydrate (because they got their fill of protein sooner) but paid the price of being short of energy.

Our locust experiment had documented for the first time in any animal the battle between two nutrients—protein and carbs—as they competed for control of food intake on imbalanced diets. Protein won in the end. In fact, what we were seeing was not so much a competition between two nutrients but between two appetites—one for protein, the other for carbs. We next wondered whether the two appetites could work together to help the animal achieve its nutrition goal—a balanced diet.

CHAPTER 3 AT A GLANCE

1 The Oxford locust experiment provided a new way to define balanced and imbalanced diets.

2 Locusts had a target mix of protein and carbs for best growth and survival.

3 When their diet didn’t allow them to reach the target, protein was prioritized over carbs but at a cost to growth and survival.

4 We had documented for the first time the battle between two appetites—for protein and carbs. Can these two appetites work together to help the animal achieve its nutrition goal—a balanced diet?

4
Dance of the Appetites

IN THE EXPERIMENT, OUR LOCUSTS WERE EACH given a single food to eat. They could eat as much of it as they wanted, but they couldn’t change the balance of protein and carbs—that was determined by us. We had done this to set up a competition between the two appetites for protein and carbs to see which was more powerful; and as we just saw, protein won.

But what would have happened had the locusts been free to choose from a variety of foods? Would their appetites have worked together to help the insects navigate the proper balance of protein and carbs?

We asked a PhD student in our lab at Oxford, Paul Chambers, to create a nutritional challenge for locusts to solve. He offered the insects choices of two foods differing in their protein and carb content.

In every case, the insects did the exact same thing: they ate an identical balance of protein and carbs, regardless of which foods they were offered. To do so, they had to choose very different amounts of the two foods, depending on which pair was offered. It’s as if, regardless of whether we were offered meat and pasta, or egg and bread, or beans and rice, or fish and potatoes, we always consumed the exact same balance of protein and carbs. For us humans, this might seem a nearly impossible challenge. Somehow, the locusts solved the puzzle with ease.

Even more impressive, the combination of protein and carbs they chose exactly matched the bull’s-eye in our graph from the big locust experiment. They had chosen the healthiest combination of protein and carbs, the one that best supported survival and growth.

Our experiments even showed how the insects could tell if a food contained the nutrient they lacked. Locusts, like other insects, have taste hairs all over their mouthparts as well as on their feet and elsewhere. When these hairs touch something edible, the locust analyzes its chemical content before deciding whether to eat. If, say, the insect has recently taken in enough protein, these sensors will ignore that nutrient. It won’t even recognize that the nutrient is there. If, on the other hand, the locust is protein-deficient, the sensors, upon encountering protein, will send electrical messages to the brain saying, “Eat this”—and that is exactly what ours did, ignoring carbs.

We went one step further and showed that locusts could even learn to associate colors and scents with the protein and carb content of foods. We could train them to go to places where they had come to learn they would find what they craved. That’s a pretty smart thing to do for an animal with a brain the size of a pin head.

This proved that when locusts have a good choice of available foods, their appetite systems collaborate, and the insects combine the foods in exactly the right proportions to consume an optimally balanced diet. But when they are restricted to imbalanced foods, as in our big locust experiment, the appetites for protein and carbohydrate compete. And for locusts, in the end, protein always won.

All this detail about locust feeding was fascinating in itself—for us, at least. But it also raised a much bigger issue relevant to everybody: the possibility that what we had seen in locusts might apply to appetites across the entire animal kingdom, including humans. It is therefore worth looking at exactly what appetites are and how they work their magic (and sometimes, their mischief). This line of inquiry will also help answer a question that we are often asked: How do living things know, innately, what they ought to eat?

The first thing to bear in mind when trying to understand appetite is that nature has provided everything we eat with highly individual tastes—flavors. To us, a hunk of charred flesh tastes different from a handful of berries, which is different again from a bunch of juicy, dark green leaves. All this variety is no accident, nor is it simply to keep us from being bored at mealtime (but it does that, too). The flavor profile of a food indicates its chemical contents—its nutrients.

Given that proteins, fats, and carbs each have their own special roles and significance, both to provide energy and to perform other important functions, it comes as no surprise that nature has equipped us with the ability to tell the difference and thereby detect their presence in food.

We take this talent for granted, but without it, none of us would exist. It helps us to know what nutrients are contained in which foods and what we should eat and avoid. This need to find the proper foods is why we experience sugar as tasting pleasingly sweet, and why high-protein foods have that lip-smacking savory taste that the Japanese call umami, and fats have that rich, buttery mouth feel and flavor. Otherwise, how would we tell the nutrients apart?

We are not alone among the animal kingdom in being able to taste macronutrients, although some other animals possess their taste organs in unlikely places. A female blowfly, like a locust, tastes sugar and amino acids with her feet and with the tip of her abdomen to guide laying eggs on something suitably disgusting (to us at least) for growing her baby maggots. If that sounds gross, consider that we have taste receptors inside our intestines as well as in our mouths to help keep track of nutrients as they are broken down during digestion. After all, our gut is open at both ends—just as we taste food at the front end, we keep track of it all the way through. We even continue to detect nutrients after they leave the gut and enter the bloodstream, using receptors located in various organs—including the liver and the brain. The brain is where the appetite control centers reside. These are the neural circuits that collect together signals from the bloodstream, liver, and gut, generating feelings of hunger and fullness.

As is true for macronutrients, we have taste organs that can detect some of the micronutrients, including mineral salts, both on our tongues and scattered through our bodies.

Specific tastes and flavors provide information about which foods are which and how much of particular nutrients each contains. They are the external side of the feeding equation. This helps an animal decide what to eat, and there’s no need for us to tell you the importance of that. But tastes and flavors are not much good at telling the animal something equally important: how much of each nutrient it needs at a given time. That, the internal half of the equation, is taken care of by appetite systems.

It is a mistake, and one that is much more common than it ought to be, to think of appetite as a single, powerful hunger that drives animals (including us) to eat until they are full. As our locusts taught us, a single appetite would be useless for mixing a balanced diet. Therefore, animals need separate appetites to keep track of the different nutrients they need.

And yet, there is a limit to how complex biological systems can get and still operate efficiently. For this reason, we couldn’t possibly have specific appetites for each and every one of the dozens of nutrients needed to keep us alive and well. It would probably drive us mad at mealtime.

Instead, we found two appetites in locusts—one for protein and the other for carbs. What about more complex species, like humans? How many appetites do we need? Perhaps a better way to ask this is how few nutrient-specific appetites does it take to keep us alive and well?

The answer, it seems, is five. Five appetites are sufficient. They drive us to consume the following nutrients:

Protein

Carbs

Fats

Sodium

Calcium

These are the three macronutrients plus two critically important micronutrients. These correspond precisely to the same nutrients that we are able to taste in foods. A most elegant solution to an otherwise impossible challenge. Our appetites have evolved to target specific flavors and guide us to eat only the things we need to survive.

Those nutrients (the Big Five) have been singled out by our evolution for special reasons. One is that they are needed in the diet at very specific levels—neither too much nor too little. Another is that the things we eat vary widely in their concentrations of these nutrients—we would, for example, need to eat a lot more rice than steak to get the amount of protein we require. Third, some of these nutrients were so rare in our ancestral environments that we needed dedicated biological machinery to seek them out.

For example, sodium and calcium were once so scarce that they were assigned dedicated appetites with their own specific taste receptors—and we are not alone in this. We get the word salary because salt was so prized, it was used in historical times as a monetary currency. Gorillas eat tree bark to get enough salt. Calcium is so prized by giant pandas that it causes them to migrate long distances to get enough to breed.

What about the other essential nutrients—such as vitamins A, C, D, E, K, B1 (thiamine), B2 (riboflavin), B3 (niacin), B5 (pantothenic acid), B6, B7 (biotin), B9 (folate), or B12, or minerals like potassium, chlorine, phosphorus, magnesium, iron, zinc, manganese, copper, iodine, chromium, molybdenum, selenium, and cobalt? Why didn’t we evolve specific appetites for them? One reason is that our natural diets are rich in these nutrients, and by eating the right amounts of the Big Five, we automatically get enough of the rest. That’s a lot of measurements and calculations we’ve been spared.

If all of the above sounds pretty logical, that’s because it is. But it hasn’t always been viewed that way, even by the experts.

For over six hundred years, the word appetite was used in much the same way, both in everyday conversation and by experts. As long ago as 1375, the Scotsman John Barbour wrote in a poem of a hearty feast that needed “no other sauce—except appetite”; the same idea has become immortalized in the idiom “hunger is the best sauce.” A few years later, in 1398, Chaucer observed that the strength of the appetite is dependent on good health: “Weak appetite cometh before sickness”; and in 1789, Benjamin Franklin made the link between appetite and our nutrient needs: “What one relishes, nourishes.”

The scientific study of appetite is more recent. It all started with an important question: Exactly what is it in our bodies that makes us feel hungry? An early theory, which dates to 1912, was what has come to be known as the rumble theory. According to this, stomach fullness is the switch for appetite: hunger is turned on when the walls of an empty, churning stomach rub against each other (“rumble”) and turned off when it is full. The rumble theory took a fatal blow when it was later found that a stomach was not needed to feel hungry: patients who had had their stomachs surgically removed to treat cancer or ulcers continued to experience those familiar pangs.

Several theories followed, each one proposing a different measurement made by the body to tell our brains when we should eat. The thermostatic hypothesis suggested that animals ate to get enough energy to keep warm and stopped eating to prevent overheating; the glucostatic hypothesis identified blood sugar as the important link; the lipostatic theory implicated body fat reserves; and the aminostatic theory argued that amino acids circulating in the blood were responsible. While obviously different, all of these theories had in common that they identified a single component of the diet as the link between appetite and what the body needed: energy, sugars, fats, or amino acids.

In the 1930s, working quietly and inconspicuously with rats in his lab at Johns Hopkins University, was a young scientist named Curt Richter. The son of a German engineer, Richter had less time for theories than for performing clever experiments to measure exactly how the body instructs the brain to perform specific behaviors, and eating was no exception. Over a period of seventy years, working in the same laboratory, Richter made many discoveries that form an important backdrop to our research and the story in this book.

In one experiment, Richter operated on rats to trick their physiology into losing salt from the body at a fatal rate. And yet they didn’t die but rather just ate more salt to compensate for the increased losses. Importantly, they didn’t eat more food overall or more of other nutrients, only salt. He did similar experiments for calcium with the same result: the rats saved their own lives by eating more calcium but no more of other nutrients.

To ensure that what he was seeing was relevant to the normal lives of rats, Richter also studied their pattern of food selection in times when female rats naturally had an increased need for sodium and calcium, during pregnancy and lactation. As he suspected, here, too, they selected diets that were higher than usual in these nutrients. Richter’s experiments had shown that rats have not one appetite but at least two for different nutrients. All those other theories—thermostatic, glucostatic, lipostatic, and aminostatic—needed a rethink. Not because they were all wrong, but perhaps there were elements of truth in each.

This is where our own research on locusts entered the story. We proved that even in insects there are multiple appetites and that these can be used to select a balanced diet.

But appetites don’t exist only to tell us to start eating. Equally important, they also tell us when to stop. This involves nutrients in the food being released by digestion, getting absorbed into the bloodstream, and sending signals of fullness back to the brain. The only flaw is that these signals take time to kick in (in fact, some don’t act until after the end of a meal). The risk is that you will have overeaten by the time you get the message to stop. We all know the sensation of eating so much, so quickly, that we didn’t realize we were full ten minutes ago. In the meantime, we have delivered a calorie bomb to our system.

How can this be avoided? We need something to slow down our eating, fill us up quickly, and allow time for the slowly absorbed nutrients to reach our blood and announce to the brain that they are there. Luckily, nature has provided us that, too, in the form of a gut-stretcher that induces the feeling of fullness and slows the rate of gut emptying.

Fiber.

For herbivores like locusts and omnivores like us, fiber is the major source of bulk in plant foods. It forms the structure of plant cells and tissues and, as we explained in Chapter 2 and More on Nutrients, much of it is based on complex forms of carbohydrate that we are unable to digest using our own digestive enzymes. Some of that fiber, however, is digested by microbes that live in our guts—our microbiome, as those trillions of bacteria are known collectively.

In return, these microbes produce key nutrients (short-chain fatty acids, vitamins, and amino acids) that our bodies need. They also support our immune systems, keeping our intestines healthy, and even benefit our mental health. In addition to all that, gut microbes produce signals that make us feel full. They are an important part of our appetite control system.

Thanks to locusts and some geometry, we had glimpsed the beauty and power of nutrient appetites. We had seen how they worked together in perfect rhythm when possible—when the correct range of foods was available—to help animals solve the complex challenges of eating a balanced diet. We had also seen, in the locust experiment, that when things got rough and it wasn’t possible to eat a balanced diet, the appetites came into conflict. In that case, for locusts, the protein appetite took the lead, and carbs followed more passively.

We began to wonder whether locusts were just an elegant oddity that was not generalizable to the rest of the animal kingdom—let alone to humans. Or were we looking at something like a general rule of nature? If so, that could be important.

CHAPTER 4 AT A GLANCE

1 Animals have evolved separate appetites for protein, carbs, fat, sodium, and calcium. Together, the Big Five can signal a nutritionally balanced diet.

2 Fiber acts as a brake on appetite, preventing overeating and feeding the gut microbiome.

3 When offered an appropriate choice of foods, the protein and carbohydrate appetites work in harmony to guide locusts to consume a balanced diet.

4 But is nutrient balancing universal among all animals?

5
Seeking Exceptions to the Rule

WHEN SCIENTISTS ARE IN PURSUIT OF something potentially important, we are trained to temper our enthusiasms and continually ask: Could we be wrong? For us, that question took this form: Could it be that the power of multiple appetites to serve an organism’s nutritional needs was the exception rather than the rule?

Specifically, in our case, the question was whether the balancing act performed by the feeding locusts in our lab was the rule for other animals, and not just in laboratories but in natural environments. Nutrient balancing using multiple appetites was probably commonplace, we suspected.

This wasn’t merely wishful thinking by a pair of scientists wanting to have discovered something important. We had grounds to believe we might be right. In fact, we reasoned that what we were seeing was more or less a requirement for all living things.

A compelling reason for our belief comes first from the logic of Darwin. The mechanism by which organisms acquire their various features and skills involves a simple numbers game. Any characteristic that aids successful reproduction, provided it is at least partly heritable, will be passed on to the next generation—more so than characteristics that are unhelpful. Because these traits can be inherited, the offspring whose parents had the useful characteristic will themselves be more successful at reproduction, and in this way the helpful trait will eventually become more common and displace its less helpful equivalents in the population.

In terms of our research, everything we knew about biology was pointing us in the same direction: animals that balance their diets would be better equipped to reproduce than those that did not. For those unfortunate ones, eating would be like a lottery, leaving chance to decide which nutrient needs would be met and which would go hungry. Without appetites to guide the way, animals might get lucky some days and eat the mix of nutrients they need, but most of the time they would fail.

But this merely suggested what was likely, not necessarily what was true. How could we test it? The surest way would be to examine every species on the planet. But with the immense amount of work involved in our locust experiments still fresh in mind, we knew this was never going to happen. We hold the record for the number of different species whose nutritional wisdom has been studied (more than fifty by our reckoning—varying in size from ants to moose), and you will read many of their stories in this book. But that simply scratches the surface.

We needed a different approach.

The most effective way to learn whether nutrient balancing is the rule among animals or is restricted to a few, we realized, would be to reverse the question. We’d test the species that seemed to be least likely to balance their nutrient intake. If we were wrong, they’d show us. This kind of self-skepticism, in which theories are tested by seeing how much of a battering they can take and remain standing, is not only usual practice in science but a defining characteristic. This is what makes science science.

Anyway, now we needed to seek species that didn’t engage in nutrient balancing. If even the unlikeliest candidates were found to do so, we could be confident that most if not all do. Which species were particularly likely to disprove our theory? In a sense, we already had studied one of them. Of all animals, locusts were among the most renowned for an indiscriminate greed, devouring everything in their path. Having shown that even they meticulously compiled a precise mix of nutrients in their diet gave us confidence that so, too, would other species, especially those already known to be fussy eaters.

An even stiffer challenge then arose through a chance encounter involving a cacophony of chirping chickens, a student with a philosophical bent, and two halves of bugger-all.

It was 1997, when David was in the Lancaster lab of Oxford Zoology Department teaching a practical course in animal behavior. The students were busy with an experiment involving groups of recently hatched chickens. David was at the front of the class talking to the celebrated evolutionary biologist and devout atheist Richard Dawkins, who had stopped in to see what all the chirping was about.

Seeing his opportunity, an earnest young student named Stephen Jones approached and addressed Richard in a well-spoken English voice: “I am interested in writing an essay on postmodernist science. Would you be prepared to supervise this?”

“What is postmodernist science, in any case?” Richard asked in his characteristic laconic style. Then he immediately answered his own question: “Exactly two halves of bugger-all,” a pungent Britishism we can translate as “fuck-all,” or, if we’re being decorous, absolutely nothing.

Richard well knew—better than most—that “postmodernist science” is a form of cultural relativism, a philosophical view according to which science is just another belief system equivalent to any other, with no monopoly on the truth. This, he knew, was wrong for reasons we discussed above: science’s self-skeptical nature is an efficient filter for eliminating incorrect theories and in this way, over time, separating fact from belief.

Richard declined to supervise Stephen’s essay. But David, having developed an interest in what was often a fine line that separates “belief” from “fact” in nutrition science, accepted.

Stephen did a fine job. Even though his paper didn’t make any game-changing contributions to the philosophy of what is and what is not true, it would indirectly make an important contribution to our search for the truth about feeding.

Through working on the essay, Stephen developed an interest in doing PhD research and wanted to study something of practical importance. He chose to work on cockroaches, those widespread pests with filthy habits, a bad smell, and a reputation for spreading disease. We immediately saw an opportunity: cockroaches were also perfect animals for testing whether nutrient balancing is general to animals.

Here’s why. These unlikable creatures are extremely wily, adaptable, and hardy. They can live in virtually all environments from tropical and temperate forests to salt marshes, deserts, and cities, enduring circumstances that would endanger most species. In cities, they are equally at home scavenging in garbage bins, drains, and sewers as in restaurants, pantries, and, given half a chance, your dinner plate, even moving among these venues in a single sitting. Underlying this flexibility is a remarkable capacity to survive on a very wide range of diets, including no diet at all—they can live for a month without eating or drinking and over one hundred days on water alone. A few very special tricks underpin this nutritional hardiness.

Inside the hindguts of cockroaches are thousands of tiny spines. Each houses millions of bacteria, which can digest sources of carbohydrate that to most animals would be useless. Cellulose, for example, the stuff of which wood, paper, cardboard, and cotton fabric are made, can be eaten by cockroaches and used for energy courtesy of their spine-living bacteria. Considering that cellulose is the most abundant organic compound on Earth and few other animals can use it for energy, this is a handy advantage; it means that for cockroaches there is almost never a shortage of carbohydrate.

It doesn’t end there. All animals need to get rid of nitrogen wastes that result from various metabolic processes involving protein synthesis and breakdown. In mammals, this is the main function of urine, whereas most insects, birds, and reptiles dump it as a white paste of uric acid. If cockroaches eat too much protein, they, too, excrete the excess as nitrogen wastes. But unlike other animals, they don’t excrete it all: some is stored as tiny crystals in specialized cells called urocytes, which are found in the insect equivalent of a liver, the fat body. Alongside the urocytes is another kind of fat body cell, called mycetocytes. These maintain captive populations of bacteria that are unable to live anywhere else in the world. Their job is to use the nitrogen stored in the urocytes as a raw material to make amino acids, which they release into the blood for use by the cockroach to make protein. Mycetocyte bacteria are, in effect, onboard nitrogen recycling plants.

With such flexible carbohydrate and protein processing abilities, we reasoned, cockroaches would not need to bother nearly as much as other animals about eating the precise levels of sugars, starch, and protein required by their tissues. This, we believed, is why cockroaches can live on such a wide range of diets and why they can survive in so many habitats.

It is also why we were excited at the opportunity to test whether they actually do balance their intake of nutrients. If an animal that apparently has no need to eat precisely the right amounts of carbs and protein nonetheless does so, surely then other species that have a greater need would do likewise.

Stephen performed a clever experiment to test this. In a first step, he maintained cockroaches on one of three diets for two days: one group got high protein and low carb, one was fed high carb and low protein, and the third got intermediate levels of both nutrients. In human terms, this would be roughly equivalent to eating either only fish, only rice, or only a mix of fish and rice combined—sushi. After this period, the cockroaches were offered a buffet containing all three diets, from which they could freely select whatever they preferred.

We were surprised by the results. When Stephen plotted the data points in our usual protein-carbohydrate intake graph, we immediately saw that the cockroaches not only balanced their intake of nutrients, but did so with a precision and determination that rivaled anything we’d seen to that point, even to now.

The graph showed that in the final, buffet phase, those cockroaches that had previously been on the sushi-like feed, with balanced levels of protein and carbohydrate, chose from all three foods to compose a diet similar to what they had been eating. The other two groups initially selected only the food with the nutrient they were previously denied: if they had been forced to eat only carbs, they now chose protein, and vice versa. They continued eating this way for 10 hours, after which both groups began to eat all three foods. By 48 hours of buffet, they had hit their target nutrient intakes. From that point on, all three groups ate an identical mix of protein and carbohydrate and continued that way until 120 hours later, when the experiment ended.

The message couldn’t be clearer. Each insect had eaten the precise amounts of the nutrients needed to correct the imbalance we imposed on it, and once that had been achieved, they all selected an identical diet—which maintained the balanced nutritional state. The term nutritional wisdom was at the time in vogue. Here we had seen nutritional genius. The cockroaches had behaved like nutrient-seeking missiles.

Shortly after, Stephen left science to pursue a career in the church. We have yet to tell Richard Dawkins.

Thanks to the cockroaches, we had become more confident that nutrient balancing was not an arcane ability confined to a few species. But these intriguing if unpleasant creatures were of interest mainly to researchers in pest control. To extend our test of the generality of nutrient balancing in nature, we next turned to species that were widely believed not to balance their nutrient intake.

The perfect choice was predators. According to foraging theory, these animals would have no need to feed selectively to balance their nutrient intake because the foods of predators—the bodies of other animals—were thought to contain the same mix of nutrients as the animal eating them (making the axiom “You are what you eat” the literal truth). As a result, scientists believed, it should be effortless for predatory animals to consume a properly balanced diet, while we creatures who eat more than one thing would have to work harder at it.

If this were true, it had obvious implications for our theory of nutrient balancing: it would fail to apply to the very large group of animals that obtain their nutrition from eating other animals.

We needed to test this. A perfect opportunity arose when David examined the PhD thesis of a young Danish researcher, David Mayntz, on spiders.

That was an interesting experience. David’s own PhD defense, at Oxford University, was a serious affair, involving five hours of earnest discussion and argument with a small expert panel of examiners. Only after that was a decision made about whether the candidate had passed. If this is likened (with some justification) to a no-holds-barred kickboxing match, then a Danish PhD defense is more like the charade of professional wrestling. The candidate sits with the examiners at the front of a room, in this case on a stage, before a public audience usually including family and friends. By this point, it has already been decided that the thesis has passed, and the main purpose of the questioning is entertainment: it gives the candidate an opportunity to demonstrate their expertise and prowess in debating their research topic.

With his recently earned PhD degree, David Mayntz moved to Oxford to work with us applying Nutritional Geometry to predators. We designed an experiment like the one Stephen Jones had done on cockroaches. In a stroke of genius, David Mayntz suggested that we include in the experiment not just one but three species of predator, each differing in their hunting strategies. This presented a very stern test of our theory.

The first species, a ground beetle, moves around its environment searching for prey in much the same way that cockroaches forage. In the wild, these animals, theoretically at least, could select among the prey that they capture and eat.

The second was a wolf spider. Like the beetle, this species is mobile; but rather than searching for prey, it sits and waits for dinner to come to it.

The third species was least mobile of all: a web-building spider, which invests in building a trap for its prey.

We reasoned that if predators did balance their nutrient intake, the mobile beetle, which has opportunity to encounter many different prey types, would be the most likely to do so. The web-building spider, which has little choice over what gets trapped in its web, would be least likely to do so. The sit-and-wait predator would be somewhere in between because, even though it has little influence over which prey come within striking range, it can easily move among hunting spots to influence its opportunities.

We tested each species in an experiment that matched its ecology. We offered the mobile beetles a buffet-style test, like the cockroach experiment, in which the different test foods were available together. In the wild, web-building spiders have to make do with whatever happens to wander into their trap. So, rather than offer them a choice of prey in our experiment, we gave each a single victim that was either high or low in the nutrient they were lacking—fat or protein—and measured how the spiders responded to each. Like web builders, in nature, sit-and-wait predators can choose where they lay their ambush but not which prey come within striking distance. They, too, were tested on a single prey that was either high or low in the nutrient they lacked.

(How, you might wonder, did we get prey that differed in the balance of fat and protein they contained? The answer is that we raised the prey—flies—in our lab and gave them different diets. We designed some diets to make flies fat, and these chubby insects provided fatty meals for their predators, while other flies grew lean on low-fat, high-protein feed.)

The roving beetles behaved much like the cockroaches: if they had previously been restricted to low-fat prey, they specifically selected high-fat foods, and if previously restricted to low protein, they chose high protein. The sit-and-wait predator chose its nutrients by eating different amounts of the prey it had been offered, depending on its composition: the spider ate more of fatty animals if fat was needed and more of lean ones when protein was needed.

The web-building spider did the most remarkable thing of all. Its way of feeding is to inject into prey a cocktail of digestive enzymes, then suck out a soup of predigested nutrients from the body, discarding the remaining solids. We found that the discarded part of the body was particularly depleted in the nutrient most needed by the predator, suggesting that they could tailor the cocktail of enzymes they injected into prey in order to meet specific nutrient needs.

David Mayntz’s experiment had shown not only that all three predators balanced their nutrient intake but also that the mechanism for this differed with different foraging strategies. Some selected among prey, some regulated the amount of a specific prey they ate, and others selectively extracted nutrients from whatever prey was captured. It was looking increasingly unlikely that we would find a significant number of animal species that didn’t balance their nutrient intake.

Usually, when people think about predators, their thoughts are not on invertebrates like beetles and spiders but on charismatic examples like lions, tigers, and sharks. Did they, too, carefully mix foods in the exact proportions to balance their nutrient intakes? It seems ridiculous to consider a lion or shark sizing up its prey for body composition, but then in recent years our research had presented a series of surprises.

Even more ridiculous was the thought that we could do locust-like lab experiments on man-eaters. Happily, many of us share our houses with predators that are somewhat less likely to eat their experimenter.

An opportunity arose when we were contacted by Adrian Hewson-Hughes, a research scientist at a prominent pet food company. Adrian had come across our work and wondered whether it applied to domestic cats and dogs. It was the practical implications that interested Adrian and us, too, but we also saw a wonderful opportunity to answer the question of whether vertebrate predators balance their diets.

At the first opportunity, we visited Adrian and his team and helped to design geometric experiments to test the theory. It was some years before the experiments were done, but the results were well worth the wait. In all cases, we found that nutrient balance is the strongest determinant of domestic pets’ food choice and eating behavior. We also found some fascinating differences between these species that relate to their evolutionary history.

Cats selected a diet with 52 percent of energy from protein, which is a typical value for wild predators, including the ancestors of domesticated cats and wolves. Dogs—all five breeds we studied—selected a diet of only 25 to 35 percent protein, much lower than the diets of the wolves from which dogs were domesticated and more like that of omnivores. This suggests that dogs have been altered in the process of domestication to a greater extent than have cats.

Why? Several years later, David witnessed the most likely reason.

He was at Tuanan research station, in the swamp forests of Borneo, studying wild orangutans. At the station were both cats and dogs. Tuanan is no holiday destination (as we will see in Chapter 9), and like everybody else based there, both species had their job to do. Cats were there to catch mice, which otherwise would threaten the precious food supplies, and dogs to alert the researchers when wild animals like leopards approached.

David noticed two important things about these working animals. The first, if he didn’t know better, might have seemed an injustice: only the dogs were fed. The cats were left to fend for themselves, which improved their performance in pest control.

The second is what the dogs were fed. The research station is extremely remote—to get there, the team drove for several hours over rough roads, then traveled for several more on a large motorized wooden canoe up a river through the forest, like a scene from Joseph Conrad’s Heart of Darkness. Space on the boat was at a premium. The human passengers were tightly packed, in physical contact with each other, and all remaining space was filled with valuable supplies and research equipment.

There were, therefore, no cans or bags of fancy-flavored dog meals aboard, and none made their way to the station. The dogs relied on a diet like that of their domesticated ancestors since before the invention of “dog foods,” even before the invention of agriculture: our table scraps.

And this is the likely reason why domestic cats and dogs prefer different macronutrient mixtures. Being small and often valued for their ability to control rodent populations, cats have continued to hunt and eat prey throughout their evolution and domestication. As larger animals, an important (and probably early) priority in the domestication of dogs was to breed out the hunting tendencies for which wolves are renowned, in the interests of human and livestock safety. Instead, dogs were forced to rely on our table scraps, which are much higher in carbs and fat than usual carnivore fare, and therefore became more similar in their nutrient selection to us omnivores, their owners.

Another result of the dietary switch of dogs is that they have developed an ability to digest starch more efficiently than other carnivores through evolving an increased number of genes for producing amylase (starch-digesting) enzymes. Over time, as we’ll see in Chapter 10, humans underwent a similar evolutionary change in response to agricultural production of starchy crops, such as grains. This shows how a shared environment, in this case the carb-rich world occasioned by farming, can produce similar changes in different species, a process called convergent evolution. Our dogs have become more human.

Still, even though they got the proportions of macronutrients in their diet spot on, some dog breeds we tested overshot the mark when it came to the amount they ate. In fact, they ingested far more calories than our calculations suggested they needed. It won’t come as a surprise to anyone who owns one that Labradors ate nearly twice what was necessary. A likely evolutionary reason is that their wolf ancestors are adapted to a “feast and famine” lifestyle in which they compete with others in the pack to gorge on occasional kills, then go long periods without eating. In the context of our story, though, it holds an important message: even gluttons must balance their nutrient intake.

It seemed we had learned something important from the impressive nutrient balancing we observed in predators, but it also got us thinking. Prevailing foraging theory had predicted that predators would have no need to balance their nutrient intake because animal tissues are already balanced to meet the needs of carnivores. But, why then do predators feed selectively to balance their nutrient intake? In this, they behaved much the same way we had observed for herbivores and omnivores.

Then we realized—the initial premise was wrong.

Foraging theory erred in assuming that the body composition of animals is constant. In fact, we realized, there’s a great deal of variation depending on diet, season, health, and many other factors. We saw an example above: by changing the diets of flies, we were able to create fat and thin prey for the spiders in David Mayntz’s experiment. Think also about the fat content of our own species—it can range from a mere 2 percent of body weight in Olympic athletes to over 50 percent among the obese, equivalent to the difference between dry lentils and creamy ranch dressing. In a single species!

Even more important, no single dietary composition would be optimal throughout a predator’s entire lifetime. This is because, like any animal, the nutrient needs of predators change depending on whether they are still growing or fully grown and reproducing; healthy or diseased; young or old; active or sedentary; and so forth. Therefore, like herbivores and omnivores, predators feed selectively to optimize their diets for specific circumstances, and the wide variety of prey available provides plenty of opportunity to do so.

This was illustrated by another study that we did with David Mayntz. It involved the same species of ground beetle from the initial experiment together with spiders, but with a twist. This time, David went out into the field and collected beetles immediately after they emerged from a long hibernation through the cold Danish winter, then brought them into the lab to study.

During hibernation, they eat nothing, living off the fat stores they have accumulated in advance. We knew, therefore, that they would be very lean when collected and urgently in need of some fattening up. Our question, then, was whether this influenced their food choices.

At first, they selected a fat-rich diet. Then, as their own fat stores grew, they gradually toned down that nutrient’s intake and ate more protein. This, too, was no coincidence: at that stage they were preparing to reproduce, which in insects is a protein-intensive process.

The message, of course, is that there is no such thing as a single balanced diet for these beetles—their needs change across the life cycle. Nutrient selection even changes with an animal’s activity level. Another student working with us, Louise Firth, made locusts fly for differing periods and then found that the ones who had flown the longest selected a diet higher in carbohydrate than protein, since carbs provide the fuel used in flight.

For (almost) all animals, then, predators included, feeding is a process of a wobbly gun barrel aimed at a moving target. Specialized stabilizing mechanisms—in the form of interacting appetites—are needed to collaborate if there is to be any hope of success. Exceptions are likely to be few, restricted to very special cases.

One exception is the food designed specifically to meet all the nutrient needs of an animal: mammalian milk. Particularly fascinating is the Australian tammar wallaby. In this species, the young live inside a pouch on the mother’s belly and therefore have no opportunity to eat anything other than milk. But this is a single food only in name: the wallaby mother’s milk undergoes complex changes in composition over time, modifying the mixes of nutrients needed for the specific stage of the baby’s development. For example, differing mixes of amino acids are produced to enable the growth of the brain, lungs, nails, and fur. More than that, females may simultaneously be carrying around two young of different ages. When that happens, each has a dedicated nipple producing the cocktail of nutrients it needs for its specific age. We predict, though, that when the young leave their privileged position in the pouch to fend for themselves, feeding mechanisms would be no different from other species. They, too, will have to develop nutrient-specific appetites.

We had answered our original question: nutrient balancing is widespread across species and not an exception. Our experiments had shown that it occurs in herbivores, omnivores, and carnivores, both domesticated and undomesticated, and we had rethought foraging theory to explain why.

But as biologists with a habit of watching animals in the wild, we realized that only in certain circumstances was nature obliging enough to provide the abundance and diversity of foods that could always ensure a nutritionally balanced diet. Often, in the real world, it is impossible for an animal to eat the correct amount of all nutrients. Such imbalance was so common, we suspected, that animals would have to have a Plan B—meaning that their appetite systems would need a way to respond when getting the desired nutrients was impossible. They would need a response that could compromise and help them balance eating too much of one thing against too little of others.

This was exactly the question we had set about to answer in the locust experiment: What is the nature of Plan B for a locust? The answer was that they ultimately prioritized protein over other nutrients and would even extend their development time and become obese if those were what it took to get to a target intake of protein. What, we wondered, would Plan B be for humans? As far as we knew, the question had never been asked, let alone answered. We decided to find out, and what happened next set the direction for the rest of our careers.

CHAPTER 5 AT A GLANCE

1 Even the most unlikely animal species—from cockroaches to cats—can use their multiple appetites to mix a balanced diet, like nutrient-seeking missiles.

2 However, as we saw in Chapter 3, these appetites compete when the diet is imbalanced—and in locusts, protein wins the competition.

3 What about humans?

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