Gut Thinking

What makes fruit-eating spider monkeys so much smarter than leaf-eating howlers? Their gourmet diet, apparently--it's gone to their heads.

By Peter Radetsky|Monday, May 01, 1995
Life should be a breeze in the tropical forest. The weather is warm, and there’s plenty of food for the asking. In theory, you need only reach out and luscious fruits and other tidbits will fall into your hands. Sadly, it’s not so, says Katharine Milton--particularly if you’re a monkey. Milton, a physical anthropologist at the University of California at Berkeley, has spent the last 20 years studying howler and spider monkeys in the forests of Panama. Life, she’s concluded, is tough in the forest-- animals need to devise all sorts of ingenious tactics just to get enough food to survive. Finding food is so tough, Milton thinks, that successful strategies have driven the evolution of the species. It is the solutions to the problems of diet that have made primates primates, she says. And what pertains to forest primates pertains as well to their city-slicker cousins--us. In other words, the food we eat has made us human.

Milton began her observations in 1974 on the island of Barro Colorado in Panama. For the fledgling anthropologist--Milton was then a New York University graduate student--it was an ideal spot. The island offered a protected forest inhabited by numerous species of wild animals, including howler monkeys--13- to 18-pound primates notorious for their terrifying, unearthly howls. It was also the site of a Smithsonian Institution research station, complete with an extensive herbarium for identifying indigenous plants.

Milton threw herself into her work. I’d get up every morning at 4:30, go to the dining hall, stuff as much food in my face as I could, make a bunch of peanut butter sandwiches, fill my water bottle, then walk into the forest to where I’d left the monkeys the night before, she recalls, in the twang of her native Montgomery, Alabama. I’d sit on a log in the dark, and as soon as they started to wake up at dawn, about 6, I’d start taking notes. She would then follow the monkeys as they meandered along the forest canopy some 80 feet above, note where they stopped to eat, and collect the scraps of food that dropped to the ground.

I’d follow them until 6 P.M., when it got dark, and watch them settle down for the night. Then I’d run back with a flashlight, jumping down the trail like a little goat. I’d get to the dining hall, nobody there, but the cook would have made a plate for me and covered it with tinfoil. I’d gobble down my dinner, run to the herbarium and identify my plant scraps, take a shower, and go to bed. And the next day the same thing.

Thus passed the bulk of three years. Milton found that most of the time the howlers ate leaves and fruit in almost equal measure, but when seasonal fruits were in short supply, the animals filled up on leaves. Howler monkeys were finicky, though. They ate only tender, young leaves, and only the tips at that.

Typically, soon after awakening, a howler troop of 19 individuals would set off through the trees in single file. The group traveled with no apparent leader, but after about 45 minutes, they’d arrive at a source of food.

They know where they’re going, says Milton. I don’t know how, but they know. They appear to use a collective information pool to locate their foods. They’ll just set off in a straight line right to it.

For example, one of the howlers’ favorite delicacies was the leaf of the Ceiba pentandra tree, a 100-foot-tall monster with room-size buttresses and limbs large enough for a grown man to walk on. It has a five-fingered leaf that’s pinkish brown when it first comes out on the tree but within hours turns green, Milton says. After that, the monkeys don’t want it anymore. Somehow they know how to get there just when the emerging leaves are beginning to expand. They eat the tips, which are far more nutritious than the middles or bases.

The howlers conducted these expeditions over 75 acres, searching out as many as 25 species of plants daily. Some, like the Ceiba pentandra tree, were edible for only a few hours a year; others were available more often. Unerringly, the howlers tracked them down. The ranges of various howler troops overlapped, so Milton would occasionally come upon a tree filled with monkeys, with other groups in adjoining trees politely waiting their turn at the table. All of which suggested that the animals had an extraordinary collective memory, an unfailing sense of direction, refined social manners, and a built-in barometer of what foods were good for them.

This aggregate intelligence allows infant howlers to mature quickly. After 12 to 14 months, howler mothers don’t want to see their babies again, Milton says. The babies soon declare independence and rely on the group for support.

Still, despite the obvious group intelligence, the monkeys individually didn’t seem particularly smart to Milton. They were relatively dull and placid--and unobservant. I ate lunch for months in full view of dozens of howlers, and not one ever seemed to realize that I was eating, much less that what I was eating might be something they would enjoy, too, she says. You could make noises and slurp and carry on--whatever cognitive processes are required to identify the act of eating, they don’t seem to use them.

But spider monkeys did. I saw them all the time when I was studying howlers, says Milton. They’d go roaring by like greased lightning. Spider monkeys are the same size as howlers, and the two animals share parts of each other’s ranges on Barro Colorado. But there the similarities end. Whereas howlers travel through the canopy on all fours, spiders swing along like Tarzan. Unlike the placid howlers, spiders are playful and mischievous. They’re terrible teases, says Milton. And they’re mean little devils. They remind me of people, she confides with a laugh. Although not specifically any of my close friends.

Spider monkeys had no trouble recognizing Milton’s lunch. ‘Food!’ they’d shout. ‘Let’s see if we can get it!’ They’d swing down toward you; they’d threaten you. They know what a banana is. They have a keen idea of what a peanut butter sandwich is. You simply cannot eat in front of them.

Intrigued, Milton decided she’d add spider monkeys to her observations. She thought it might be interesting to compare how the two species evolved from a common ancestor. But while the comparatively sedate howlers were a researcher’s dream, dealing with the spider monkeys was something else again. They were too fast for me, says Milton. So I hired a young man to work with me. He would run through the forest as fast as he could, following the monkeys, and I would come behind. We communicated by calls. ‘Whooooo!’ Like that. The sound really carries through the forest.

When the barnstorming spider monkeys found food, they’d finally screech to a stop, allowing Milton to catch up. They’d just stuff themselves. Then they’d lie around and take naps.

Unlike the howlers, Milton discovered, the spider monkeys almost exclusively ate fruit, which often made up 90 percent of their diet. Even when fruit was out of season or in short supply, it constituted over half their food. But ripe fruit is even harder to find than tender leaves. To get enough, the 18 spider monkeys on the island would resort to splitting up and trying their luck on their own. During most of the year the distribution patterns of their foods are such that if they went around in a big group, there wouldn’t be enough at any one site to feed everyone, says Milton. So they’d spend almost the whole day foraging in small subunits or by themselves. Then around twilight they’d begin to call and coalesce, and then they’d spend the night together.

As a result of this extended exploring, the spiders’ territory was huge, some 750 acres, ten times that of the howler monkeys. And that’s a conservative estimate, says Milton. Two thousand acres might be right. If the howlers displayed impressive feats of memory and direction by finding young leaves, the spider monkeys’ long-distance forays after fruit were astounding. Within an enormous area they had to remember at least 100 species of fruit and where to find thousands of fruit-bearing trees. They had to remember when each fruit was ripe, how best to approach the site, and how best to return home. If a howler forgot a food source or a travel route, the others were there to take up the slack. The spiders, though, had to fend for themselves.

And they had to know how to stay in touch. Howler monkeys tended to be quiet, communicating through subtle clucks and rattles in the throat, except at daybreak, when their eerie howls declared This is where we are this morning. (All the howler troops on the island participate, says Milton. It’s called the dawn chorus. The sound comes rolling by as light moves across the forest.)

Spider monkeys, on the other hand, were conspicuously noisy. They’d yelp and cry, whinnying like horses, barking like dogs--sometimes for hours at a time. When they’re cross about something, says Milton, they’ll bark incessantly, until you think they’re going to fall out of the tree. And in contrast to the howlers’ community messages, spider monkeys believed in individual expression. Spider monkey vocalizations are generally individualistic. It’s George giving a food call, or Mary hailing Susie, whereas a howler monkey is not saying ‘Hi, Susie’ but rather ‘Okay, everyone, we’re getting ready to move to a new food tree.’

All that variety and independence requires lots of training. As a result, infant spider monkeys mature slowly. They are nursed and carried by their mothers for two years, and they continue to associate almost exclusively with her until they’re about three or three and a half years old. Milton remembers watching female spider monkeys patiently waiting for their offspring to take off into the trees. The mother would then slowly tag along behind, she says. It was her way of instructing the youngster, forcing it to become independent by learning to move through the trees on its own.

Always, of course, leaving time for mischief. For example, spider monkeys loved to torment howlers. They would steal howler babies, says Milton. A howler mother doesn’t know what to do--she’s too dopey to get her baby back. Howlers would move out of the tree when they saw spiders coming. They’d sit quietly and hope the spiders didn’t pick on them.

Why were the two monkeys so dissimilar? Milton wondered about the differences in their diets. Howler monkeys ate mainly leaves, sometimes exclusively leaves, a low-quality source of nutrition. Leaves are plentiful and relatively high in protein, but they’re low in energy-rich carbohydrates. They also consist of some 60 percent indigestible fiber and sometimes contain toxic chemicals. How in the world did howlers get enough energy from this unpromising diet? And why did they stick to it even during seasons when there was plenty of ripe fruit in the forest?

Fruits are loaded with easily digested carbohydrates and are relatively low in fiber--they’re high-quality, nutritious food. They mean instant energy. On the other hand, fruits provide little protein. So, Milton wondered, how did spider monkeys get enough protein? And why, when fruits were scarce, didn’t they fill up on leaves, as howlers did? Why did they go to such extremes to find fruits?

Milton began finding some answers to these questions in 1977, when she returned to Barro Colorado after completing her doctoral thesis. She soon conducted an experiment measuring how long it took the monkeys to process their food. I needed to look at internal features of the monkeys, she says. I thought that perhaps the structure of their guts or efficiency of their digestion might be influencing their behavior.

She trapped howler and spider monkeys, confined them in pens, and fed them food in which she had concealed tiny plastic markers. I used a type of thin plastic material that I cut with very fine manicure scissors into little colored plastic worms, she explains. When the monkeys excreted the remains of their food, out came the markers. Milton could therefore measure the time it took any one meal to pass through a monkey’s digestive tract. The results were dramatic: howlers took 20 hours to digest their food, five times as long as spiders. That was a humongous surprise, says Milton. The difference in transit times blew me away. There had to be an explanation--they don’t have a door in there. So I went in and looked at their guts.

When Milton came upon monkeys that had died in the forest, she took them back to the research station, dissected them, and measured their gastrointestinal tracts. She then confirmed her figures against published material on differential gut measurements in various primates. She found that the colons of howlers were considerably wider and longer than those of spider monkeys. Food had to travel much farther and remained much longer in howler guts, and the monkeys had room for much more bulk. As a result, bacteria had a chance to ferment masses of fibrous leaves in the monkeys’ colons, producing energy-rich fatty acids. Milton eventually found that howlers receive more than 30 percent of their daily energy from such fatty acids.

In contrast, spider monkey food resembled the speedy monkeys themselves, hurtling through the animals’ more compact guts. Spiders were far less efficient at extracting energy from the fiber in their diet--but they didn’t have to be efficient. They ate easily digestible fruits. By moving a steady stream of fruit through their gastrointestinal tracts every day, they obtained all the carbohydrates they needed and some of the protein. The rest came from supplements of young, tender leaves.

It was a striking example of evolutionary adaptation. Each monkey’s physiology fit its particular diet. Spider monkeys couldn’t get away with eating a howler diet of mostly leaves. With their smallish guts, they’d never keep enough bulk around long enough for fermentation to provide energy. And howlers wouldn’t manage for long if they used the spider monkey tactic of eating fruit--their slow digestive tracts couldn’t process nearly enough of it.

Besides, it took smarts to track down sufficient fruit, and Milton thought it unlikely that the howlers were up to the job. Nor was the howler diet of leaves up to the job of fueling the amount of brainpower necessary. The brain, a big, hungry organ, requires a disproportionate amount of energy, and leaves just don’t provide enough. All of which led to the second part of the puzzle: the difference in the monkeys’ mental capacities.

I kept thinking, spider monkeys are so smart, and howler monkeys don’t seem so smart. The more I thought about it, the more it seemed to make sense that if you have a high-energy diet and widely distributed foods, you’re going to need a certain amount of ability to locate those foods. I became curious--I wondered how big their brains were.

Luckily for Milton, that information was available without her having to cut apart more monkeys. A scientist named Daniel Quirling had published extensive statistics about the sizes of primate brains. Spider monkey brains, he had determined, weigh twice those of howlers, 107 grams compared with 50.4. No wonder spiders are smarter.

With that, everything came together. It was a eureka moment, says Milton. Here were two monkeys, the same size, living in the same forest, but so different. Compared with the howlers, spider monkeys were brighter and more lively. They matured more slowly and had more to learn; they made more ruckus, with a greater variety of vocalizations; they ate widely dispersed, high-energy foods that were harder to find--and their brains were twice as large. Why?

As far as Milton was concerned, diet was the key to these discrepancies. Eating fruits fueled the evolution of the spider monkeys’ large brains. Says Milton, It would have been a feedback process in which some slight change in the monkeys’ foraging behavior conferred a benefit, which in turn permitted a modest improvement in the quality of their diet, which led to an excess of energy. Over generations, the monkeys that spent the energy on making their brain slightly bigger and more complex had an evolutionary advantage. Their improved brain allowed for more helpful changes in their behavior, and so on.

Milton realized that if such a scenario was correct, similar differences in brain size should show up in other primates with similar differences in diet--monkeys and apes that eat fruits should have larger brains than their leaf-eating counterparts. Sure enough, when Milton checked the literature, she found the pattern held true. For example, of the three great apes, lively, quick chimpanzees, our closest animal relatives, have a bigger brain for their body size than do the slower, more placid gorillas and orangutans. Chimps take some 94 percent of their diet from plants, largely in the form of ripe fruits. Gorillas and orangutans eat 99 percent plant foods, but mainly lower-quality leaves, pith, even bark. Diet had to be the key to their disparate evolution.

And what about the primate with the largest brain of all? Might large human brains also have initially been the result of a high-quality diet? Milton thinks so. I view dietary conditions as the key pressure leading to the emergence of humans.

Her scenario goes like this: When our australopithecine ancestors emerged in Africa more than four and a half million years ago, their brains were not appreciably larger than those of today’s apes, and they had massive, grinding jaws and molar teeth, suggesting that they ate mostly tough, low-quality plant material. Eventually the australopithecines were supplanted by another series of early humans with increasingly larger brains and smaller jaws and teeth, indications that their diet had become higher in quality, less fibrous and abrasive. In time these brainy ancestors refined their diet. With the introduction of meat, early humans started to eat in ways that no primates had before.

The fossil evidence offers strong support for the view that early humans made a dietary breakthrough, Milton says. No longer were we, like spider monkeys and chimps, primarily fruit eaters. Now, drawing on the power of our large brains, we introduced tools to help us prepare food and learned to divide the responsibility for meals--a uniquely human characteristic--so that different people became experts in different diets. Eventually we became what Milton calls cultural omnivores. We will eat anything, from other human beings to sea squids, she says. But if our culture tells us not to eat something, it doesn’t matter if it is the most nutritious, digestible food in the world--we won’t eat it. Food for humans is more in the mind than in the item.

A case in point may involve meat itself. It is usually thought that early humans began eating meat to satisfy their need for protein, but ongoing research by Milton’s former student Craig Stanford, now an anthropologist at the University of Southern California, suggests that eating meat is as much a social gesture as a dietary necessity. With Jane Goodall, Stanford studies chimpanzees at Gombe National Park in Tanzania. He has found that Gombe chimps eat about 3 percent of their diet as meat; primarily they hunt colobus monkeys.

Chimps don’t routinely hunt monkeys, though. They separate into small groups to forage for fruits, and they go after a monkey only when they come upon it by chance. Even then they might not hunt--they tend to do so when a female in heat happens to be part of the foraging group. Then, once a male makes the kill, a fascinating ritual often ensues. Immediately, within seconds, the female comes racing over with her hand out, says Stanford. The male pulls away the carcass until the female allows him to copulate with her. Then the male shares the meat. Sometimes he will induce her to copulate, then wave the carcass in her face and pull it away until they copulate again. Then she gets some meat.

The chimps thus use meat as a commodity exchange--in this case, to elicit sexual favors. Stanford has found that foods more nutritious than meat, such as oil palm nuts, are available year-round. Such immobile foods are much easier to procure than monkeys, which fight like the dickens and provide no more than a few ounces of meat per chimp. It’s not just a nutritional decision when they decide to hunt, Stanford says. They have more in mind.

Chimps appear to eat meat for social reasons more than nutritional reasons, agrees Milton. It’s kind of like a date. It’s a party, a community event.

Did we humans start eating meat for similar reasons? Stanford wouldn’t be surprised: Other researchers have shown that dominant chimps withhold meat from enemies and dole it out to allies, using it in a cleverly calculated political way.

The similarity to people is reinforced by other chimp behaviors. The whole life cycle of chimps is not that different from people’s, says Stanford. Chimp babies, for example, are totally dependent on their mothers for their first four years, and they continue to hang around Mom until the age of 10 or 11. Females become sexually mature at about the age of 12; males go out into the world with the other guys at about 15. Chimps defend their territory with lethal aggression, says Stanford. Humans are the only other primates to do so.

Milton sees strong parallels between humans and chimps, and spider monkeys as well. Similar diet; similar aggressive, individualistic bent; similar long-term rearing of young; similar social system--and similarly large brains. All of us--spider monkeys, chimps, and humans alike--are what we eat. The behaviors and physiology that define us are the consequences of dietary-driven evolution.

Everything comes back to diet, says Milton. It’s the pivotal feature, the kickoff. When you get right down to it, the way we behave had better translate ultimately into groceries--or we’re not going to be around to behave that way much longer.
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