Amazing Animals (Scientific American Special Online Issue No. 16)

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COPYRIGHT 2004 SCIENTIFIC AMERICAN, INC.

ScientificAmerican.com

AMAZING ANIMALS

exclusive online issue no. 16

We humans tend to think of ourselves as Nature’s ultimate creation. A quick survey of the creatures with which we share the planet suggests that’s a myopic view of things. Billions of years of evolution has produced a rich diversity of animals, each exquisitely adapted to its ecological niche. This exclusive online issue celebrates some of the more spectacular results. In the pages that follow, leading biologists share their insights into beasts both familiar and foreign. Some are remarkable for their physical characteristics. Take, for example, the basilisk lizard, best known for its ability to walk on water. Or the star-nosed mole, whose stellar accessory works uncannily like an eye in its dark, damp environs. And then there’s the komodo dragon, a rare reptile whose stealth, power and supersized proportions have earned it a fearsome reputation indeed. Other creatures amaze with their behavior. Some ants conduct warfare that would have given Genghis Khan pause. Parrots match wits with dolphins and nonhuman primates. Lions cooperate, but only when they stand to benefit. And chimpanzees pass social customs down from generation to generation--in other words, they have culture. Animals fascinate us with the ways in which they resemble and differ from our kind, yet they are neither mirror nor measuring stick. Perhaps American author Henry Beston put it best: "They are other nations, caught with ourselves in the net of life and time, fellow prisoners of the splendor and travail of the earth." —The Editors

TABLE OF CONTENTS 2

Beasts in Brief • Fido Found to Be Wiz with Words • King of Beasts Suffers to Be Beautiful • Crafty Crow Rivals Primates in Toolmaking • How Bears Power-Nap

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• The Cultured Orangutan • Dolphin Self-Recognition Mirrors Our Own • How Geckos Get a Grip • Brainy Bees Think Abstractly

Running on Water BY JAMES W. GLASHEEN AND THOMAS A. MCMAHON; SEPTEMBER 1997 The secret of the basilisk lizard's strategy lies in its stroke

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The Nose Takes a Starring Role BY KENNETH C. CATANIA; JULY 2002 The star-nosed mole has what is very likely the world's fastest and most fantastic nose

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The Komodo Dragon BY CLAUDIO CIOFI; MARCH 1999 On a few small islands in the Indonesian archipelago, the world's largest lizard reigns supreme

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Slave-Making Queens BY HOWARD TOPOFF; NOVEMBER 1999 Life in certain corners of the ant world is fraught with invasion, murder and hostage-taking. The battle royal is a form of social parasitism

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Divided We Fall: Cooperation among Lions BY CRAIG PACKER AND ANNE E. PUSEY; MAY 1997 Although they are the most social of all cats, lions cooperate only when it is in their own best interest

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Talking with Alex: Logic and Speech in Parrots BY IRENE M. PEPPERBERG; SCIENTIFIC AMERICAN PRESENTS: EXPLORING INTELLIGENCE 1998 Parrots were once thought to be no more than excellent mimics, but research is showing that they understand what they say. Intellectually, they rival great apes and marine mammals

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The Cultures of Chimpanzees BY ANDREW WHITEN AND CHRISTOPHE BOESCH; JANUARY 2001 Humankind's nearest relative is even closer than we thought: chimpanzees display remarkable behaviors that can only be described as social customs passed on from generation to generation

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AUGUST 2004

BEASTS IN BRIEF Fido Found to Be Wiz with Words Dogs may be able to understand far more words than a typical owner teaches them during obedience training. Scientists experimenting with a nine-and-a half-year-old border collie in Germany have discovered that the dog knows more than 200 words for different objects and can learn a new word after being shown an unfamiliar item just one time. The dog's ability shows that advanced word recognition skills are present in animals other than humans, and probably evolved independently of language and speech.

COURTESY OF SUSANNE BAUS

Rico, the border collie, was taught to retrieve different objects by his owners, who placed various balls and toys around their apartment and asked Rico to fetch specific ones. Rico gradually increased his vocabulary to about 200 words that he could match to objects. To make sure Rico's owners weren't giving him subconscious cues that helped him find the right item, Julia Fischer and her colleagues at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, tested Rico's knowledge in a lab, where he retrieved 37 out of 40 items correctly. "Rico's 'vocabulary size' is comparable to that of language-trained apes, dolphins, sea lions, and parrots," the authors write in their report, published in the June 11, 2004, Science. The team then tested Rico's ability to employ fast mapping, a neurological process that toddlers use to quickly guess the meaning of new words. The researchers put an unfamiliar object in a room with other things he did know and, without teaching Rico the name of the novel item, asked him to get it. Seven times out of 10 he returned with the correct object. Four weeks later, the scientists tested Rico's ability to recall what he had learned. The objects that he had seen only once during the previous experiment were placed among eight other things, some familiar and some completely new. In this trial, Rico retrieved the correct item three out of six times, a feat of learning never before seen in a dog. Rico's performance was comparable to that of a three-year-old toddler, the scientists observe. Fischer and her collaborators note that they're not sure whether Rico is exceptionally smart or exceptionally well trained, but they hope they can use this experiment to further probe how the brain learns to understand words. Rico's powers of comprehension, they say, show that the processes the brain uses to discern words are not the same as those used to produce speech. Says Fischer: "You don't have to be able to talk to understand a lot." --Elizabeth Querna

King of Beasts Suffers to Be Beautiful It's not easy being beautiful, especially when you're a male lion. New research suggests that what lady lions love most and what other males fear most is a leo with a long, dark mane--which is precisely the worst sort of 'do to have in Africa's often sweltering environs. Biologists have long pondered the purpose of the lion's hot, conspicuous mane, which seems at first glance like more trouble than it's worth. Evolutionary theory holds that there should be some benefit gained from it, but what might that be? Two hypotheses have been put forth. The first holds that the extra fur protects the lion from injuries to the neck and shoulders. The second posits that the mane makes the lion more attractive to lionesses and more intimidating to other males. In recent work, Peyton M. West and Craig Packer of the University of Minnesota studied the reactions of male and female lions to various types of manes, using dummy lions to model the various coifs. They found that whereas females fell for dummy males with dark manes (as opposed to blondes), males avoided the brunettes. Males also avoided dummies sporting 2 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE


AUGUST 2004

long manes. As it turns out, mane color and length may be pretty good indicators of a lion's health and fitness. "Dark color tends to be found in high-testosterone males," West observes. "Therefore, it isn't surprising that females would prefer darker manes and males would be intimidated. But there is no correlation between testosterone and mane length." Males pay more attention to mane length because recently injured lions have shorter manes, she explains. The males' dark allure comes at a significant cost. "A male with a dark mane may have to work harder to stay cool, behaviorally or physiologically, and is advertising that toughness, along with his toughness in battle," West remarks. (Longer manes, on the other hand, do not appear to retain additional heat.) In some especially hot regions, however, all that fur costs too much, and the males go maneless. "As climate changes, things like lion manes, the brightness of bird plumage and the size of deer antlers may be sensitive bioindicators, Packer muses. "They can tell you how well an animal is doing in the environment." The team's findings were published in the August 23, 2002, Science. --Kate Wong

Crafty Crow Rivals Primates in Toolmaking COURTESY OF SCIENCE

The ability to make tools was once thought to lie solely within the purview of humans. Then in the 1960s Jane Goodall discovered that chimpanzees, too, fashion implements to perform certain tasks. Since then, researchers have observed tool use in a variety of animals. Nonhuman primates are widely thought to be the most sophisticated toolusers after us. Observations of an innovative New Caledonian crow named Betty could alter that view. New Caledonian crows are known to make hook tools with natural materials in the wild. But Oxford University zoologists writing in the August 12, 2002, Science report that Betty, a captive crow, spontaneously performed an unexpected variation on this theme, coaxing a piece of straight wire into a hook to retrieve a small bucket of food. In a subsequent experiment, the clever crow repeated the feat in nine out of 10 valid trials. To bend the wire, Betty anchored one end either in the sticky tape holding the experimental apparatus together or between her feet, and then manipulated the other end with her beak. Remarkably, although Betty had previously used supplied wire hooks, she had never seen the process of bending and had no prior training with pliant material. "Purposeful modification of objects by animals for use as tools, without extensive prior experience, is almost unknown," the team writes, noting that even our primate kin often fail to show such talent in the absence of explicit coaching. "Our finding, in a species so distantly related to humans and lacking symbolic language, raises numerous questions about the kinds of understanding of 'folk physics' and causality available to nonhumans, the conditions for these abilities to evolve, and their associated neural adaptations," the authors conclude. Birdbrain might not be an insult after all. --Kate Wong

How Bears Power-Nap For most people, staying in shape means getting regular exercise. Take a vacation from the gym and your hard-earned sixpack goes soft. But imagine if you could sleep for five months and still wake up fit as a fiddle. According to research described in the February 23, 2001, Nature, this is in fact just how bears emerge from hibernation. Henry J. Harlow of the University of Wyoming and his colleagues found that hibernating black bears lose less than 23 percent of their strength during their 130-day winter slumber. Humans, in contrast, would experience a 90 percent strength loss if they were immobile for so long. Incredibly, when the team took muscle biopsies from denned bears in early and late winter, they found that the skeletal muscle cells did not dwindle in size or number-nor did they lose their protein content or oxidative capacity. The researchers suggest that the bears may be maintaining their muscles by drawing on protein reserves from elsewhere in the body, and by shivering. "Understanding these processes in hibernating bears," the team writes, "may provide new insight into treating muscle disorders and into the effects of prolonged hospital bed confinement, antigravity and long-distance space travel on humans." --Kate Wong



AUGUST 2004

For humans, the sputtering sound known as a raspberry is commonly considered a contemptuous gesture. But among some orangutans, the expression seems to simply signify that the utterer is turning in for the night. Not all orangutan groups mark the end of the day this way, however. In fact, according to a report published in the January 3, 2003, Science, a raspberry before bed is one of 24 socially transmitted behaviors that scientists say may represent cultural variation in the great apes. If the findings are confirmed by additional field observations, they could push the origin of culture back nearly seven million years to the last common ancestor of orangutans and the African apes. Man's closest living relative, the chimpanzee, provides the best evidence for the existence of nonhuman culture: scientists have identified 39 behavior patterns that vary culturally among the animals. To investigate whether similar conduct exists in orangutan groups, Carel P. van Schaik of Duke University and his colleagues assessed previously collected data on six different wild populations in Borneo and Sumatra. "Culture requires more than just a mother-infant bond, but also extensive social contact, and orangutans are at the low end of the sociability spectrum," van Schaik says. Nevertheless, the team identified two dozen behaviors that fall into three of the four categories of cultural elements: labels, signals and skills (The fourth category is symbols, which only humans employ). Van Schaik notes that the group found "the biggest behavioral repertoires within sites that showed the most social contact, thus giving the animals the greatest opportunity to learn from one another." Examples of culturally-based behaviors that the scientists distinguished include using leaves as napkins, using leafy branches to ward off attacking insects and riding "snag" (dead trees that are falling toward the ground) for sport. --Sarah Graham

Dolphin Self-Recognition Mirrors Our Own Whether we're assessing our physiques or checking for food stuck in our teeth, most of us consult a mirror regularly to make sure we appear the way we expect. Though it may seem an unremarkable feat, the ability to recognize oneself in the mirror is actually exceptionally rare among animals. Indeed, only humans and their closest kin, the great apes, have shown this capacity, suggesting that factors specific to great apes and humans drove its evolution. Findings announced May 1, 2001, online edition of the Proceedings of the National Academy of Sciences, however, indicate that we and our primate relatives are not alone. According to the report, dolphins, too, exhibit mirror self-recognition. To test for dolphin self-awareness, Diana Reiss of Columbia University and Lori Marino of Emory University exposed two bottlenose dolphins to reflective surfaces after marking the dolphins with black ink, applying a water-filled marker (shammarking) or not marking them at all. The team predicted that if the dolphins-which had prior experience with mirrors-recognized their reflections, they would not show social responses; they would spend more time in front of the mirror when marked; and they would make their way over to the mirror more quickly to inspect themselves when marked or shammarked. The experiments bore out all three predictions in both dolphin subjects. Moreover, the animals even selected the best reflective surface available to view their markings. Intriguingly, whereas chimpanzees take interest in marks on fellow chimps in addition to marks on their own bodies, the dolphins focused on themselves. "Dolphins may pay less attention to marks on the bodies of companions because, unlike primates, they do not groom each other," the researchers write. "This difference makes our findings even more interesting because dolphins clearly are interested in marks on their own body despite the fact that they do not have a natural tendency toward social grooming." The extent of dolphin self-awareness remains to be explored. But the fact that they have passed the mirror test means that self-recognition may result from large brains and advanced cognitive ability, as opposed to being a by-product of primatespecific factors. That dolphins and primates-which differ profoundly in their brain organization and their evolutionary histories-should both exhibit this unusual ability, the authors note, represents "a striking case of cognitive convergence." --Kate Wong 4 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE

AUGUST 2004 COPYRIGHT 2004 SCIENTIFIC AMERICAN, INC.

COURTESY OF DUKE NEWS SERVICE

The Cultured Orangutan

In the movie Spider-Man, Peter Parker looks down at the palms of his hands to find that they have sprouted thick, black hairs, giving him a firm grip on walls and ceilings. A growing body of evidence indicates that gecko lizards, too, cling to surfaces with the help of hairlike projections. The gecko hairs are so tiny, however, that they operate not by catching on substrate irregularities, but by facilitating the formation of molecular bonds that create electrodynamic attraction between the gecko's feet and the surface upon which it is walking. As a result, the charismatic creatures can crawl upside down even on polished glass. Previous research, conducted by Kellar Autumn of Lewis and Clark College and his colleagues, had suggested that the gecko's foot-hairs, or setae, stick to surfaces by virtue of these so-called van der Waals forces. But the team had been unable to reject a competing hypothesis, which holds that the adhesion arises from water-based forces. The results of the scientists' subsequent study, detailed in a report published on August 27, 2002, by the Proceedings of the National Academy of Sciences, disproves that theory. The researchers reasoned that if water-based forces, such as capillary adhesion, were the secret to gecko grip, then the animal's toes--each of which bears hundreds of thousands of setae--should not stick to hydrophobic ("water-fearing") surfaces. In subsequent experiments, however, the gecko toes clung equally well to hydrophobic and hydrophilic ("water-loving") substrates. Single, isolated setae were likewise effective on both types of surfaces. Autumn and his collaborators further determined that the size of the setal tips--the hundreds of spatulae that branch from each hair, increasing surface density--is remarkably close to what one would expect if van der Waals forces are the principle mechanism underlying the gecko's sticking power. That implied that it is the size of the setal tip, not the nature of the setal material, that gives the lizard its toehold. Verification of this idea came when the researchers fabricated setal tips from two different materials and found that both adhered to surfaces as predicted. According to the investigators, the finding not only provides insight into the function of setal structures in geckos and other creatures, it hints at how synthetic dry adhesives could be improved: subdividing their surfaces into small, setal tip-like protrusions, thus increasing surface density, might enhance stickiness. --Kate Wong

Brainy Bees Think Abstractly The capacity for abstract thinking does not belong to humans alone, as studies of other vertebrates, such as primates, pigeons and dolphins, have shown. Researchers have found that invertebrates, too, possess higher cognitive functions. A report in the April 32, 2001, Nature indicates that the humble honeybee can form "sameness" and "difference" concepts-an ability that may help them in their daily foraging activities. To probe the honeybee's mental prowess, Martin Giurfa of the Free University of Berlin in Germany and his colleagues first trained the insects to associate certain stimuli with a reward: sugar. For example, in one experiment bees saw the color blue at the entrance to a so-called Y-maze. The entrance led to a decision chamber, where the bees could choose between two paths: one carried a blue target, the other carried yellow. The bees received a reward only if they chose blue, the same color as that seen at the entrance. The team then tested whether the bees could apply what they had learned to a new situation. Blue and yellow patches were replaced with black and white patterns of vertical and horizontal bars. The bees passed with flying colors, heading straight for the pattern that matched what they saw at the entrance. Moreover, other experiments revealed that the insects could even transfer their knowledge across the senses: bees that learned about sameness through olfactory training were able to apply that concept to situations involving visual stimuli. These results, the authors conclude, demonstrate that "higher cognitive functions are not a privilege of the vertebrates." Moreover, because the honeybee nervous system is relatively simple, they write, "there is a realistic chance of uncovering the neural mechanisms that underlie this capacity." --Kate Wong



COURTESY OF THE PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES

How Geckos Get a Grip

Originally published in September 1997

Running The secret of the basilisk lizard’s by James W. Glasheen and Thomas A. McMahon

T

he basilisk lizards of Central America are renowned for their seemingly miraculous flight across water. When startled, these green or brown reptiles scamper over ponds or lakes on their hind legs—the younger ones appearing virtually airborne, the larger ones sinking down somewhat. By videotaping seven Basiliscus basiliscus captured in a Costa Rican rain forest and by constructing mechanical models in order to understand the underlying physics, we have been able decipher the mystery of these lizards’ magnificent movements. It all begins with a slap of the foot. The basilisk lizard strikes the water to create upward force. This force, in turn, provides a medium-size, or 90-gram, lizard with as much as 23 percent of the support it needs to stay on the water surface. Then, a split second later, comes the stroke. As the foot crashes down, it pushes water molecules aside and creates a pothole of air. In addition to

the forces generated by accelerating water out of the foot’s way, the lizard obtains support from forces created by the difference in pressure between the air cavity above the foot and the hydrostatic pressure below. Together the slap and subsequent stroke can produce 111 percent of the support needed to keep an adult lizard striding along the surface. Smaller lizards, those weighing two grams or less, should be able to create 225 percent of the support they need—and consequently, their runs across the water appear freer and less cumbersome. All these gains would be lost, however, if the lizard did not pull its foot out of the hole before the water closed in around it. By slanting its long-toed foot backwards and by slipping it out while it is surrounded only by air, the creature avoids the drag that would result from pulling its foot through water. A tiny fringe that surrounds the basilisk’s five toes may facilitate this motion. Like a parachute, the fringe flares out as the foot is



on Water strategy lies in its stroke

slapped down, thus creating more surface area—all the better to hit the water with. Then, as the foot is pulled up, the fringe collapses, and the long toes are withdrawn just before the hole closes. Although their secret is now unveiled, the lizards are likely to remain alone on top of the water. Some web-footed birds can achieve similar runs on water, but their dynamics are

SA

The Authors: JAMES W. GLASHEEN and THOMAS A. MCMAHON worked on the watery capabilities of the basilisk at Harvard University, where McMahon is a professor in the division of engineering and applied science. Glasheen, now a consultant with McKinsey and Company, was a doctoral student at the time of their collaboration.

RACHEL TAYLOR

ADULT BASILISK LIZARDS usually run on water only when startled; young ones, however, will do so simply to get from one place to another. A medium-size lizard takes about 20 steps a second when running (sequence below); with each of these steps the lizard’s foot creates an air pocket from which the foot is withdrawn before water rushes back in. Tiny collapsible fringes around the basilisk’s foot (right) may help in this process.

slightly different and not well understood. As for humans, they have nothing to learn from the lizards except to stay ashore: an 80-kilogram person would have to run 30 meters per second (65 miles an hour) and expend 15 times more sustained muscular energy than a human being has the capacity to expend. The basilisks bask singularly in the liminal world between water and air.



The

NOSE

Originally published in July 2002

STARRINGRole Takes a

THE STAR-NOSED MOLE HAS WHAT IS VERY LIKELY THE WORLD’S FASTEST By Kenneth C. Catania


he renowned physicist John Archibald Wheeler once suggested, “In any field, find the strangest thing and then explore it.” Certainly it is hard to imagine an animal much stranger than the star-nosed mole, a creature you might picture emerging from a flying saucer to greet a delegation of curious earthlings. Its nose is ringed by 22 fleshy appendages that are usually a blur of motion as the mole explores its environment. Add large clawed forelimbs, and you’ve got an irresistible biological mystery. How did this creature evolve? What is the star? FANTASTIC NOSE How does it function, and what is it used for? These are some of the questions that I set out to answer about this unusual mammal. It turns out that the star-nosed mole has more than an interesting face; it also has a remarkably specialized brain that may help answer long-standing questions about the organization and evolution of the mammalian nervous system. It may comfort you to know that star-nosed moles (Condylura cristata) are small animals, tipping the scales at a mere 50 grams, about twice the weight of a mouse. They live in shallow tunnels in wetlands across much of the northeastern U.S. and eastern Canada and hunt both underground and underwater. Like the other roughly 30 members of the mole family (Talpidae), the star-nosed mole is part of the mammalian order Insectivora, a group known for its high metabolism and voracious appetite. So the tiny star-nosed mole with its big appetite must locate enough prey to survive cold northern winters. It finds earthworms in soil, as other moles do, but in addition it has access to a host of small invertebrates and insect larvae found in the rich mud and leaves of its wetland habitat and in the ponds and streams where it swims along the murky bottom to root out prey. And seeking prey is where the star comes into play. The star is not part of the olfactory system—which governs smell—nor is it an extra hand used to gather food. Instead the star is a touch organ of unsurpassed sensitivity.

T

AND MOST

PINK STAR makes this mole’s nose unmistakable. It also makes it one of the most sensitive touch organs observed in the animal kingdom—one that works uncannily like an eye.


a PREY IDENTIFICATION by the star-nosed mole

b Front view

takes place in less than half a second. When the longer appendages touch an interesting object (a), the nose moves so that the shortest and most sensitive appendage can rapidly touch and identify the item (b), which is immediately consumed.

Getting Close to the Star to explore the anatomy of the star with a scanning electron microscope— an instrument that reveals the microscopic structure of the skin surface— I thought I would see touch receptors here and there in various places across the skin. Instead I was surprised to find that the star, like the retina in the human eye, is made up entirely of sensory organs. The surface of each of the 22 appendages that ring the nostrils is composed of an aggregation of microscopic protuberances, or papillae, called Eimer’s organs. Each Eimer’s organ, in turn, is made up of an array of neural structures that signal different aspects of touch. Three distinct sensory receptors accompany each Eimer’s organ. At the very bottom of the organ is a single nerve ending that is encircled by many concentric rings, or lamellae, of tissue formed by a Schawann cell, a specialized support cell. This lamellated receptor transmits relatively simple information about vibrations or about when an individual organ first contacts an object. Above this receptor is another nerve fiber that makes contact with a specialized cell called a Merkel cell. Unlike the lamellated variety, the Merkel cell-neurite complex signals only the sustained depression of the

THE AUTHOR

WHEN I BEGAN

skin. Both of these receptors are commonly found in mammalian skin. At the top of each Eimer’s organ, however, lies a receptor unique to moles. A series of nerve endings forms a circular pattern of neural swellings in a hub-andspoke arrangement just below the outer skin surface. Our recordings from the brains of star-nosed moles suggest that this latter sensory component provides the most significant aspect of touch perception: an index of the microscopic texture of various surfaces. More than 25,000 Eimer’s organs form the star, although it has a surface area of less than one square centimeter. Together these sensory organs are supplied by more than 100,000 nerve fibers that carry information to the central nervous system and eventually to the highest mammalian processing center, the neocortex. With this formidable array of receptors, the mole can make incredibly fast sensory discriminations as it prowls its haunts looking for prey. The star moves so quickly that you can’t see it with your naked eye. A high-

KENNETH C. CATANIA first encountered star-nosed moles when he worked at the National Zoo in Washington, D.C., many years ago. Catania, who is assistant professor of biological sciences at Vanderbilt University, studies the sensory system of mammals and the organization of the neocortex. He received his undergraduate degree in zoology from the University of Maryland and his Ph.D. in neuroscience from the University of California, San Diego. Catania has received the Capranica Foundation Award in Neuroethology and the International Society of Neuroethologists/ Young Investigator Award and is a Searle Scholar.


speed camera revealed that the star touches 12 or more areas every second. Scanning its environment with a rapid series of touches, a star-nosed mole can find and eat five separate prey items, such as the pieces of earthworm we feed them in the laboratory, in a single second.

Acting Like an Eye E V E N M O R E S U R P R I S I N G than this astonishing speed is the manner in which the mole uses the star. The star functions like an eye. Try reading this sentence without moving your eyes, and you will soon appreciate that your visual system is divided into two distinct functional systems. At any given time only a small portion of a visual scene (about one degree) is analyzed with the high-resolution central area of your retina, the fovea. The much larger low-resolution area of your retina locates potentially important areas to analyze next. The characteristic rapid movements of the eyes that reposition the high-resolution fovea are called saccades. Just as we scan a visual scene with our eyes, star-nosed moles constantly shift the star to scan tactile scenes as they travel through their tunnels, quickly exploring large areas with the Eimer’s organs of all 22 appendages. But when they come across an area of interest— such as potential food— they always shift the star so that a single pair of appendages can carry out more detailed investigations. Humans have a fovea for sight, and star-nosed moles have a fovea for touch. The mole’s fovea consists of the bottom pair of short appendages, located above the mouth, each designated as the 11th appendage. Like the retinal fovea, this part of the star has the highest density of sensory nerve endings. Moreover, the rapid movements of the star that reposition this tactile fovea onto objects of interest are analogous to saccades in the visual system. The analogy goes even further. In our visual system it is not only the movements of the eyes and the anatomy of the retina that revolve around the high-resolution fovea; human brains are specialized to process information predominantly from this part of the visual scene. A characteristic feature of information processing in mammalian sensory


KENNETH C. CATANIA (preceding pages); PORTIA SLOAN (above)

Top view

How the Nose Knows systems is the topographic organization of information from sensory receptors. Visual areas contain maps of the retina, auditory areas provide maps of the cochlea (the receptors in the ear, which are maps of tones), and touch areas contain maps of the body’s surface. Such mapping is perhaps nowhere better illustrated than in the somatosensory system of the starnosed mole.

MICROGRAPHS BY KENNETH C. CATANIA; ILLUSTRATIONS BY PORTIA SLOAN

Charting Touch W O R K I N G W I T H my Vanderbilt University colleague Jon H. Kaas, I was able to explore the organization of the starnosed mole’s neocortex. By recording the activity from neurons that compose different cortical areas, we charted the neural representation of the star, showing where and how neurons in the cortex respond to tactile stimulation of the Eimer’s organs. We identified three separate maps of the star where the responses of neurons reflect the anatomy of the nose on the opposite side of the face. (In all mammals, the left half of the body is represented predominantly in the right side of the cortex, and vice versa.) To our amazement, we also found that these maps are visible in sections of the brain that were stained for various cell markers— we could literally see a star pattern in the cortex. When we compared the sizes of cortical brain maps with the appendages of the star, we noticed an obvious discrepancy. The 11th appendage, which is one of the smallest parts of the star, had by far the largest representation in the cortex. The discrepancy is a classic example of what has been termed cortical magnification: the most important part of the sensory surface has the largest representation in the brain, regardless of the actual size of the sensory area on the animal. The same phenomenon occurs in the visual system, in which the small retinal fovea has by far the largest portion in visual cortex maps. We also discovered that neurons representing the 11th appendage responded to tactile stimulation of very small areas, or receptive fields, on the 11th appendage, whereas neurons representing the other appendages responded solely to stimulation of larger areas. The smaller receptive fields for the 11th appendage re-

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Star-nosed mole

5 6 7 8 Schematic of anatomy in cortical space

9 11

10

CORTICAL MAPS of the star-nosed mole reveal the

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7 5 6

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3

importance of the 11th appendage. As this schematic shows, the most sensitive appendage gets the most space in the cortex (above). The same is true for the most sensitive part of the human eye. The organization of the cortex also beautifully mirrors the position of the appendages (right) and their relative importance.

2 11

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Right cortex

2 1 3 4

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6 11

7 10 8 9 Appendages

APPENDAGES of the star are made up entirely of sensory organs. These Eimer’s organs have elements that are common to many animals’ skin receptors: a single nerve ending at the very base (a), which relays information about vibrations and initial contact with an object, and another nerve fiber that records sustained pressure (b). But the very tip of the Eimer’s organ is found only in moles: neural swellings arrayed just below the outer skin, which are amazingly sensitive to the details of surfaces (c).

c

b a Eimer’s organs


It is staggering to consider just how much larger the human brain would have to be if the entire retina were to have the same resolution as the fovea. To accomplish this, the human brain would have to be at least 50 times bigger. Your head would no longer fit through a doorway. Clearly, it is more efficient to devote a large part of the computational resources of the brain to a small part of the sensory system and then to move that area around like a spotlight to analyze important aspects of the world.

Space Race in the Brain A S O F T E N O C C U R S , our observations about the star-nosed mole’s sensory system raised as many questions as they answered. How does part of a sensory surface acquire such a large section of the brain’s map in the first place? The traditional understanding has been that each sensory input acquires the same average amount of area in a cortical map during development, and thus the enlarged representation of a sensory fovea simply reflects the greater number of neurons collecting information from the foveal region. This theoretical framework, suggesting that each input has equal squatter’s rights in the brain, is appealing in its simplicity. But a number of studies have recently challenged this democratic assessment of cortical parcellation in the primate visual system by showing that inputs from the fovea are allocated more cortical territory than those containing peripheral information. To see what was happening in the star-nosed mole, we decided to measure the cortical representations of the 22 appendages and to compare those areas with the number of nerve fibers collecting information from each appendage. It was obvious (after counting more than 200,000 nerve fibers!) that sensory neurons collecting information from the 11th appendage are granted far more cortical territory in the brain maps than inputs from the other appendages. This is another parallel between the mole’s somatosensory system and primate visual systems, and it shows not only that important areas of a sensory surface can have the highest number of sensory neurons collecting


information per unit area but also that each of these inputs can be allocated extra computational space in the brain. This observation, however, does not explain how these sensory inputs manage to take the most territory in cortical maps. The question belongs to one of the most fascinating areas of current research in neuroscience, because changes to cortical maps could be a critical component of learning complex skills and recovering from brain injuries or strokes. Several studies indicate that a combination of intrinsic developmental mechanisms and experience-dependent plasticity affects the shape and maintenance of brain maps. These findings are especially intriguing in the case of the star-nosed mole, because the pattern of use of the nose— as measured by how the mole touches prey

with the different appendages— very closely matches the pattern of magnification for the appendage representations in the cortex. The correspondence suggests that behaviors may shape the way the cortex is organized. Alternatively, intrinsic developmental mechanisms may match the size of cortical maps to their behavioral significance. It is the classic question of nature versus nurture.

The Developing Star L O O K I N G A T H O W the star develops in mole embryos can help clarify this matter. Because the star develops before its representation in the cortex, sensory inputs from the star have an opportunity to influence the way that the cortical maps form during potentially critical periods of development.


MICROGRAPHS BY KENNETH C. CATANIA

flect a greater acuity for this region and mirror the organization of visual systems. The discovery of a somatosensory fovea in the star-nosed mole suggests that this organizational scheme is a general evolutionary solution to constructing a high-resolution sensory system. Visual systems with a fovea are the most familiar, but auditory systems can have an acoustic fovea as well, as has been elegantly demonstrated by Nobuo Suga of Washington University in mustached bats. Many bats emit an echolocation call that contains a narrow frequency range and then analyze returning echoes to navigate and to detect prey. A large proportion of the bat’s auditory receptors (hair cells in the cochlea) and large areas in the bat’s brain are devoted to analyzing a narrow frequency range corresponding to a single harmonic of the returning echo. This is an example of an acoustic fovea. Although it is hard to imagine, bats have an auditory version of a saccade as well. This is necessary because returning echoes are Doppler-shifted to different frequencies— depending on the speed of the bat and its target, usually an unfortunate insect—and often fall outside the frequency range of the acoustic fovea. Because the hunting bat cannot change its acoustic fovea, it constantly changes the frequency of its outgoing pulses so that the Doppler-shifted returning echo will be at the frequency of its acoustic fovea. The behavior is called Doppler-shift compensation and is the acoustic equivalent of moving the eyes, or the star, to analyze a stimulus with the high-resolution area of the sensory surface and the corresponding computational areas of the brain. The presence of a sensory fovea in the mammalian visual system, auditory system and somatosensory system is a dramatic case of convergent evolution and points to common constraints in the way evolution can construct a complex brain. After all, why not just wire the entire sensory system for high-resolution input and eliminate the need to constantly shift the eyes, star, or echolocation frequency? One reason, of course, is that it would take a massive enlargement of the brain— and the nerves carrying sensory inputs to it— to accomplish this task.

cortex during development. But it is also possible that early behavioral patterns in star-nosed moles— which use the 11th appendage to suckle— contribute to activity-dependent expansion of the fovea in the cortical maps. Sorting out the relative contributions of these different influences is one of our goals.

How the Mole Got Its Star

STAR-NOSED EMBRYO provides clues to the animal’s evolutionary history. The appendages start as tubes embedded in the mole’s face. They break free of the skin before birth. Two weeks after birth, they begin to bend forward. Perhaps these unusual noses began as organs that lay flat against the snout, just as they do in the adult coast mole (left).

Star-nosed mole embryos come in about the strangest-looking varieties imaginable. Although most embryos look odd, star-nosed moles appear especially weird because the embryonic hands are gigantic—all the better to dig with later— and the nose is obviously unique. Studies of the embryos revealed that appendage 11 was the largest appendage during early development, despite its relatively small size in adults. It also became clear that Eimer’s organs on the star, and the neural structures within each Eimer’s organ, matured first on the 11th appendage. It is as if this appendage gets a head start compared with all the other ones, which later overtake it in size and number of Eimer’s organs. As it turns out, the retinal fovea in the visual system also matures early.

When we examined the corresponding patterns in the somatosensory cortex, we found that markers for metabolic activity appear first in the representation of the 11th appendage. This suggests that the early development of the fovea results in greater activity in the developing cortical representation of this area, which could allow these inputs to capture the largest area in the cortical map. Strong evidence from the developing visual system of primates indicates that sensory inputs with the greatest level of activity are able to capture the largest areas in the

O N E C A N ’ T H E L P but wonder how the star-nosed mole evolved. Examining the embryos provided a road map to starnosed mole evolution, or at least to that of its enigmatic nose. The appendages that form the star develop unlike any other known animal appendage. Rather than growing directly out of the body wall, the star appendages form as cylinders, facing backward and embedded in the side of the mole’s face. In the course of development, these slowly emerge from the face, break free from the skin and then, about two weeks after birth, bend forward to form the adult star. The backward developmental sequence suggests that ancestral star-nosed moles might have had strips of sensory organs lying flat against the sides of the snout. These might have been slowly raised up over many generations until the star was formed. Of course, without further evidence, this might remain a “Just So” story. But there exist two mole species— the coast mole (Scapanus orarius) and Townsend’s mole (S. townsendii) — that have short strips of sensory organs lying flat against the upper side of their noses, and these adult noses bear an uncanny resemblance to the embryonic star. These intermediate forms strongly suggest that such an ancestor gave rise to the fullfledged star we see today. However they came to be, these unlikely noses may help reveal much about the influence of innate developmental mechanisms and behavioral patterns on the organization of the cortex.

MORE TO E XPLORE The Natural History of Moles. Martyn L. Gorman and R. David Stone. Cornell University Press, 1990. Sensory Exotica: A World beyond Human Experience. Howard C. Hughes. MIT Press, 1999. A Nose That Looks Like a Hand and Acts Like an Eye: The Unusual Mechanosensory System of the Star-Nosed Mole. K. C. Catania in Journal of Comparative Physiology, Vol. 185, pages 367–372; 1999.

13 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE COPYRIGHT 2004 SCIENTIFIC AMERICAN, INC.

AUGUST 2004

THE

Originally published in March 1999

KOMODO DRAGON On a few small islands in the Indonesian archipelago, the world’s largest lizard reigns supreme by Claudio Ciofi


AUGUST 2004

A

deer nimbly picks its way down a path meandering through tall savanna grasses. It is an adult male of its species, Cervus timorensis, weighing some 90 kilograms (about 200 pounds). Also known as a Rusa deer, the animal knows this route well; many deer use it frequently as they move about in search of food. This Rusa’s home is the Indonesian island of Komodo, a small link in a chain of islands separating the Flores Sea from the Indian Ocean. Most wildlife find survival a struggle, but for the deer on Komodo, and on a few of the nearby islands, nature is indeed quite red in tooth and claw. This deer is about to encounter a dragon. The Komodo dragon, as befits any creature evoking a mythological beast, has many names. It is also the Komodo monitor, being a member of the monitor lizard family, Varanidae, which today has but one genus, Varanus. Residents of the island of Komodo may call it the ora. Among some on Komodo and the islands of Rinca and Flores, it is buaja darat (land crocodile), a name that is descriptive but inaccurate; monitors are not crocodilians. Others call it biawak raksasa (giant monitor), which is quite correct; it ranks as the largest of the monitor lizards, a necessary logical consequence of its standing as the biggest lizard of any kind now living on the earth. (A monitor of New Guinea, Varanus salvadorii, also known as the Papua monitor, may be longer than the lengthiest Komodo dragons. The former’s lithe body and lengthy tail, however, leave it short of the thickset, powerful dragon in any reasonable assessment of size.) Within the scientific

community, the dragon is Varanus komodoensis. And most everyone also calls it simply the Komodo. The Komodo’s Way of Life

T

he deer has wandered within a few meters of a robust male Komodo, about 2.5 meters (eight feet) long and weighing 45 kilograms. The first question usually asked about Komodos is, How big do they get? The largest verified specimen reached a length of 3.13 meters and was purported to weigh 166 kilograms, which may have included a substantial amount of undigested food. More typical weights for the largest wild dragons are about 70 kilograms; captives are often overfed. Although the Komodo can run briefly at speeds up to 20 kilometers per hour, its hunting strategy is based on stealth and power. It has spent hours in this spot, waiting for a deer, boar, goat or anything sizable and nutritious. Monitors can see objects as far away as 300 meters, so vision does play a role in hunting, especially as their eyes are better at picking up movement than at discerning stationary objects. Their retinas possess only cones, so they may be able to distinguish color but have poor vision in dim light. Today the tall grass obscures the deer. Should the deer make enough noise the Komodo may hear it, despite a mention in the scientific paper first reporting its existence that dragons appeared to be deaf. Later research revealed this be-

JOSE AZEL Aurora

KOMODO DRAGON flicks his foot-long, yellow forked tongue to taste the air.



AUGUST 2004

BORNEO

NEW GUINEA SULAWESI

JAVA TIMOR

KOMODO ISLAND has an area of about 340 square kilometers (130 square miles) and is clearly hilly. The highest points are about 735 meters above sea level. Komodo dragons tend to stay below 500 meters but are found at all elevations. The creatures live only on a few Indonesian islands. As shown on the map, Australia is 900 kilometers southeast, with Java some 500 kilometers to the west and New Guinea 1,500 kilometers to the northeast.

KOMODO HABITAT

LAURIE GRACE

AUSTRALIA

lief to be false, although the animal does hear only in a restricted range, probably between about 400 and 2,000 hertz. (Humans hear frequencies between 20 and 20,000 hertz.) This limitation stems from varanids having but a single bone, the stapes, for transferring vibrations from the tympanic membrane to the cochlea, the structure responsible for sound perception in the inner ear. Mammals have two other bones working with the stapes to amplify sound and transmit vibrations accurately. In addition, the varanid cochlea, though the most advanced among lizards, contains far fewer receptor cells than the mammalian version. The result is an animal that is insentient to such sounds as a low-pitched voice or a high-pitched scream. Vision and hearing are useful, but the Komodo’s sense of smell is its primary food detector. Its long, yellow forked tongue samples the air, after which the two tongue tips retreat to the roof of the mouth, where they make contact with the Jacobson’s organs. These chemical analyzers “smell” the deer by recognizing airborne molecules. The concentration present on the left tongue tip is higher than that sampled from the right, telling the Komodo that the deer is approaching from the left. This system, along with an undulatory walk in which the head swings from side to side, helps the dragon sense the existence and direction of odoriferous carrion from as far away as four kilometers, when the wind is right. The Komodo makes its presence known when it is about one meter from its intended victim. The quick movement of its feet sounds like a “muffled machine gun,” according to Walter Auffenberg, who has contributed more to our knowledge of Komodos than any other researcher. Auffenberg, a herpetologist at the University of Florida, lived in the field for almost a year starting in 1969 and returned for briefer study periods in 1971 and again in 1972. He summed up the

bold, bloody and resolute nature of the Komodo assault by saying, “When these animals decide to attack, there’s nothing that can stop them.” That is, there is nothing that can stop them from their attempt— most predator attacks worldwide are unsuccessful. The difficulties in observing large predators in dense vegetation turn some quantitative records into best estimates, but it is informative that one Komodo followed by Auffenberg for 81 days had only two verified kills, with no evidence for the number of unsuccessful attempts. For the sake of instructive exposition, the Komodo that has ambushed the deer reaches its target. It attacks the feet first, knocking the deer off balance. When dealing with smaller prey, it may lunge straight for the neck. The basic strategy is simple: try to smash the quarry to the ground and tear it to pieces. Strong muscles driving powerful claws accomplish some of this, but the Komodo’s teeth are its most dangerous weapon. They are large, curved and serrated and tear flesh with the efficiency of a plow parting soil. Its tooth serrations harbor bits of meat from the Komodo’s last meal, either fresh prey or carrion. This proteinrich residue supports large numbers of bacteria, which are currently being investigated by Putra Sastrawan, once Auffenberg’s student, and his colleagues at the Udayana University in Bali and by Don Gillespie of the El Paso Zoo in Texas. They have found some 50 different bacterial strains, at least seven of which are highly septic, in the saliva. If the deer somehow maneuvers away and escapes death at this point, chances are that its victory, and it, will nonetheless be short-lived. The infections it incurs from the Komodo bite will probably kill it within one week; its attacker, or more likely other Komodos, will then consume it. The Komodo bite is not deadly to another Komodo, however. Dragons wounded in battle with their


comrades appear to be unaffected by these otherwise deadly bacteria. Gillespie is searching for antibodies in Komodo blood that may be responsible for saving them from the fate of the infected deer. Should the deer fail to escape immediately, the Komodo will continue to rip it apart. Once convinced that its prey is incapacitated, the dragon may break off its offensive for a brief rest. Its victim is now badly injured and in shock. The Komodo suddenly launches the coup de grâce, a belly attack. The deer quickly bleeds to death, and the Komodo begins to feed. The muscles of the Komodo’s jaws and throat allow it to swallow huge chunks of meat with astonishing rapidity: Auffenberg once observed a female who weighed no more than 50 kilograms consume a 31-kilogram boar in 17 minutes. Several movable joints, such as the intramandibular hinge that opens the lower jaw unusually wide, help in the bolting. The stomach expands easily, enabling an adult to consume up to 80 percent of its own body weight in a single meal, which most likely explains some exaggerated claims for immense weights in captured individuals. Large mammalian carnivores, such as lions, tend to leave 25 to 30 percent of their kill unconsumed, declining the intestines, hide, skeleton and hooves. Komodos eat much more efficiently, forsaking only about 12 percent of the prey. They eat bones, hooves and swaths of hide. They also eat intestines, but only after swinging them vigorously to scatter their contents. This behavior removes feces from the meal. Because large Komodos cannibalize young ones, the latter often roll in fecal material, thereby assuming a scent that their bigger brethren are programmed to avoid consuming. More Komodos, attracted by the aromas, arrive and join in the feeding. Although males tend to grow larger and bulkier than females, no obvious morAUGUST 2004

phological differences mark the sexes. One subtle clue does exist: a slight difference in the arrangement of scales just in front of the cloaca, the cavity housing the genitalia in both sexes. Sexing Komodos remains a challenge to researchers; the dragons themselves appear to have little trouble figuring out who is who. With a group assembled around the carrion, the opportunity for courtship arrives. Most mating occurs between May and August. Dominant males can become embroiled in ritual combat in their quest for females. Using their tails for support, they wrestle in upright postures, grabbing each other with their forelegs as they attempt to throw the opponent to the ground. Blood is usually drawn, and the loser either runs or remains prone and motionless. The victorious wrestler initiates courtship by flicking his tongue on a female’s snout and then over her body. The temple and the fold between the torso and the rear leg are favorite spots. Stimulation is both tactile and chemical, through skin gland secretions. Before copulation can occur, the male must evert a pair of hemipenes located within his cloaca, at the base of the tail. The male then crawls on the back of his partner and inserts one of the two hemipenes, depending on his position relative to the female’s tail, into her cloaca. The female Komodo will lay her eggs in September. The delay in laying may serve to help the clutch avoid the brutally hot months of the dry season. In addition, unfertilized eggs may have a second chance with a subsequent mating. The female lays in depressions dug on hill slopes or within the pilfered nests of Megapode birds. These chicken-size land dwellers make heaps of earth mixed with twigs that may reach a meter in height and three meters across. While the eggs are incubating, females may lie on the nests, protecting their future offspring. No evidence exists, however, for parental care of newly hatched Komodos. The hatchlings weigh less than 100 grams and average only 40 centimeters in length. Their early years are precarious, and they often fall victim to predators, including their fellow Komodos. They feed on a diverse diet of insects, small lizards, snakes and birds. Should they live five years, they can weigh 25 kilograms and stretch two meters long. By this time, they have moved on to bigger prey, such as rodents, monkeys, goats, wild boars and the most popular Komodo food, deer. Slow growth continues throughout

their lives, which may last more than 30 years. The largest Komodos, three meters and 70 kilograms of bone, teeth and sinew, rule their tiny island kingdoms. The Komodo’s Past

K

omodos, as members of the class Reptilia, do have a relationship with dinosaurs, but they are not descended from them, as is sometimes believed. Rather Komodos and dinosaurs share a common ancestor. Both monitor lizards and dinosaurs belong to the subclass Diapsida, or “two-arched reptiles,” characterized by the presence of two openings in the temporal region of the skull. The earliest fossils from this group date back to the late Carboniferous period, some 300 million years ago. Two distinct lineages arose from those early representatives. One is Archosauria, which included dinosaurs. The ancestor of monitor lizards, in contrast, stemmed from primitive Lepidosauria at the end of the Paleozoic era, about 250 million years ago. Whereas some dinosaurs evolved upright stances, the monitor lineage retained a sprawling posture and developed powerful forelimbs for locomotion. During the Cretaceous, and starting 100 million years ago, species related to present-day varanids appeared in central Asia. Some of these were large marine lizards that vanished with the dinosaurs, about 65 million years ago. Others were terrestrial forms, up to three meters in length, that preyed on smaller animals and probably raided dinosaur nests. About 50 million years ago, during the Eocene, these species dispersed throughout Europe and south Asia and even into North America. Wolfgang Böhme of the museum of natural history in Bonn has contributed much to our understanding of the rise and evolution of the Varanus genus, based on morphological data. Dennis King of the Western Australian Museum and Peter Baverstock and his colleagues at Southern Cross University are continuing research into the evolutionary history of the genus through comparisons of DNA sequences and chromosomal structure of varanid species and related families. They have concluded that the genus originated between 40 and 25 million years ago in Asia. Varanids reached Australia by about 15 million years ago, thanks to a collision between the Australian landmass and southeast Asia. Numerous small varanid species, known as pygmy moni-


tors, quickly colonized Australia, filling multiple ecological niches. More than two million years later a second lineage differentiated and spread throughout Australia and the Indonesian archipelago, which was at the time far closer to Australia than it is today, because much of the continental shelf was above water. V. komodoensis is a member of that lineage, having differentiated from it about four million years ago. The Indo-Australian varanids could take advantage of their unique faunal environment. Islands simply have fewer resources than large landmasses do. Because reptilian predators can subsist on much lower total energy requirements than mammals can, a reptile will have the advantage in the race for top predator status under these conditions. In such a setting, reptiles can also evolve to huge size, an advantage for hunting. A varanid called Megalania prisca, extinct for around 25,000 years, may have reached a length of six meters and a weight of 600 kilograms; the late extinction date means that humans may have encountered this monster. Komodos adopted a more moderate giantism. Reasons for the Komodo’s current restricted home range— the smallest of any large predator— are the subject of debate and study. Various researchers subscribe to alternative routes that the dragons’ ancestors may have taken to their present locale of Komodo, Flores, Rinca, Gili Motang and Gili Dasami. Komodo has a different paleogeography from its neighbors. According to worldwide sea-level changes over the past 80,000 years and bathymetric data of the study area, Flores and Rinca were joined until 10,000 years ago. Gili Motang was connected several times to their combined landmass. Komodo was long isolated but appears to have joined its eastern neighbors about 20,000 years ago, during the last glacial maximum. That association may have lasted 4,000 years. (This scenario is based on my calculations of the effect of sea-level variations of about 130 meters during the last Pleistocene glaciation, combined with available bathymetric data for the area.) Tantalizing fossil evidence supports the notion that today’s Komodo populations are relics of a larger distribution that once reached Timor, to the east of Flores. Fossils of two identical forms of a now extinct pygmy elephant, Stegodon, about 1.5 meters at the shoulder, on both Timor and Flores suggest that those two islands might have been AUGUST 2004

From Grad Student to Dragon Wrangler

I

became interested in Komodos as a graduate student at the University of Kent at Canterbury in England. My doctoral thesis, in conservation biology, required me to perform field research on a rare or endangered species. I wished to work with reptiles, and I wanted to combine fieldwork with state-of-the-art molecular biological techniques, which are useful in determining genetic relationships and divergences between populations. Such studies require collecting blood from a study specimen. Based on these parameters, the creatures that would have most benefited from study were limited to two species. The first was a tortoise, Testudo hermanni, that is distributed throughout southern Europe. I instead chose the Komodo both for the challenge and because it is still one of the world’s least studied large predators. I would discover many of the reasons for this continuing ignorance. All the materials needed for fieldwork must be shipped in or created from scratch; building Komodo dragon traps is arduous and time-consuming; while rare, attacks by Komodos on humans are not unheard of; and then there is the smell. I wanted mobile traps and immobilized Komodos. I therefore built devices along the lines of humane mousetraps, only my mice might reach lengths of three meters. I made the devices with local timber and ironmesh fencing material. Each trap measured three meters by a half meter by a half meter and had a closable door. Goat served as both bait and as rations for me and a local ranger assistant. Komodos would force them-

sufficiently close in the Pleistocene to allow migration. The limited resources of an island could have driven the evolution of the pygmy elephants, because smaller individuals, with lower food requirements, would have been selected for. In contrast, today’s Komodo dragon may have evolved from a less bulky ancestor; the availability of the relatively small elephants as prey may have been a driving force in the selection of largeness that resulted in the modern three-meter Komodo. (A large reptile still needs far less food than a mammal of similar size.) Auffenberg suggests that the Komodo could once “have been a highly specialized pygmy stegodont predator,” although prey species similar to modern deer and boars may also have been present before the arrival of modern humans within the past 40,000 years. Further attempts to reconstruct the Komodo’s evolutionary history require more comprehensive fossil finds and accurate dating of the islands that harbor extant populations. The work of King and Baverstock, as well as the integration of paleogeographic data and genome analysis, should shed more light on the origin of the species. The World Discovers a Dragon

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he West was unaware of the Komodo until 1910, when Lieutenant van Steyn van Hensbroek of the Dutch colo-

selves into the trap as far as they could to get to the meat at the other end. Once they touched the bait, which was connected to a trigger mechanism, the entrance to the trap closed.

At this point, we would hang the entire trap on a balance, thus determining the weight of the captured individual. Then we would open the door at the tail end and pull the Komodo out. Komodos smell quite intense to begin with, what with their oral bacterial factories and their frequent association with carrion. The rotting goat meat adds to the aroma, and punctuating the olfactory experience is the habit of the threatened Komodo to immediately vomit and defecate, in preparation for fight or flight. Once the rear legs were free, we would tie them together. We would then continue to pull the Komodo from the trap until the front legs appeared, and we tied those. Finally, we would tape the mouth shut, allowing us to do a quick physical examination and take blood. We went through this routine on animals smaller than about 2.5 meters in length. When we happened to trap any of the largest individuals, we contented ourselves with drawing blood while the Komodo remained ensnared. Using these techniques, I was able to get blood samples from 117 Komodos over five months in 1994 and 1997, and I am currently analyzing them. Also in 1997 I attached transmitters to eight Komodos to obtain information about movement and home-range size. —C.C.

nial administration heard local stories about a “land crocodile.” Members of a Dutch pearling fleet also told him yarns about creatures six or even seven meters long. Van Hensbroek eventually found and killed a Komodo measuring a more realistic 2.1 meters and sent a photograph and the skin to Peter A. Ouwens, director of the Zoological Museum and Botanical Gardens at Bogor, Java. Ouwens recruited a collector, who killed two Komodos, supposedly measuring 3.1 and 2.35 meters, and captured two young, each just under one meter. On examination of these specimens, Ouwens realized that the Komodo was in fact a monitor lizard. In the 1912 paper in which Ouwens introduced the Komodo to the rest of the world, he wrote simply that van Hensbroek “had received information . . . [that] on the island of Komodo occurred a Varanus species of an unusual size.” Ouwens ended the paper by suggesting the creature be given the name V. komodoensis. Understanding the Komodo to be rare and magnificent, local rulers and the Dutch colonial government instituted protection plans as early as 1915. After World War I, a Berlin Zoological Museum expedition roused worldwide interest in the animal. In 1926 W. Douglas Burden of the American Museum of Natural History undertook a well-equipped outing to Komodo, capturing 27 dragons and describing anatomical features based on examinations of some 70 individuals.


The Komodo’s Future

M

ore than 15 expeditions followed Burden’s, but it was Auffenberg who performed the most comprehensive field study, looking at everything from behavior and diet to demographics and the botanical features of their territory. Auffenberg determined that the Komodo is, in fact, rare. Recent estimates suggest that fewer than 3,500 dragons live within the boundaries of Komodo Island National Park, which consists of the islands of Komodo (1,700 individuals), Rinca (1,300), Gili Motang (100) and Padar (none since the late 1970s), and some 30 other islets. A census on Gili Dasami has never been done. About another 2,000 Komodos may live in regions of the island of Flores. The Komodo is now officially considered a “vulnerable” species, according to the World Conservation Union; it is also protected under the Convention on International Trade in Endangered Species of Wild Fauna and Flora. The Komodo dragon has faced major challenges during the past 20 years that threaten its survival in part of the national park and on Flores. The disappearance of dragons on Padar probably stems from poaching of their primary prey, deer. Policing this rugged and sometimes inaccessible habitat is difficult; two days after I finished a census of the island in 1997, 10 deer were AUGUST 2004

POSSIBLE ROUTES (right) by which Komodo ancestors traveled to their current island habitat are still the subject of debate. Whether they came from Asia directly or through Java or Australia first is not clear. Certainly the lower sea levels of the past made more routes possible than are obvious today. The more recent research in the region has updated the decadesold knowledge that we had of the Komodo’s current territory (below).

BORNEO

KOMODO DRAGON RANGE FROM 1970 DATA KOMODO DRAGON RANGE FROM 1997 DATA ? AREAS TO BE EXPLORED

REO

SULAWESI

POTA RIUNG

KOMODO LABUANBAJO FLORES

WAE WUUL RESERVE

? PADAR RINCA

? GILI DASAMI

? ?

GILI MOTANG

150 kilometers along Flores’s northwest coast. Populations on the north and west coasts are also threatened by deforestation and indirectly through deer hunting. The fortunes of the Komodo dragon are inexorably linked with those of numerous other species of fauna and flora, and measures to protect this giant lizard must take into account the entirety of its natural habitat. For example, although central Flores is inhospitable to dragons, the southern and eastern regions of the island may harbor scattered populations, still unknown to researchers, that could act as “umbrellas” to protect the ecosystem as a whole. The charismatic dragon already draws some 18,000 visitors a year to the area, and patches of forest containing Komodos could be the cornerstone of an economically viable protection plan for the entire habitat, based on ecotourism. In addition, I hope to save the extant populations of Komodos by altering the current usage patterns of natural re-

LAURIE GRACE

poached. Nevertheless, a trend toward less poaching overall on Padar has moved officials to discuss a reintroduction program. Padar covers an area of only about 20 square kilometers and supports no more than 600 deer, in turn limiting the number of Komodos. Consequently, genetic diversity, as insurance against inbreeding, would be highly desirable among a new, small Komodo population. To assist this plan, I started a genetic study of the remaining Komodo populations in 1994 to determine the degree of genetic similarity within and between the existing groups. I am currently analyzing DNA from blood samples of 117 dragons drawn in 1994 and 1997 [see box on opposite page]. The findings should eventually allow the authorities to choose the most appropriate source populations for restocking Padar, based on genetic diversity. Sex ratio and age structure will also be factors in the choice of individuals. Komodos on Flores face the twin threats of prey depletion and habitat encroachment by humans. New settlers slash and burn the monsoon forest, and Komodo dragons are among the first species to disappear. In 1997 I set up a biotelemetric study to look at movement and home-range size of adult dragons in areas with differing degrees of human presence, both inside and outside the national park. A data collection covering a number of consecutive years can show conclusively whether human interference drives Komodos simply to migrate to different areas or to extinction. I also initiated a long-term survey to obtain information on the distribution and level of threat to Komodo populations throughout Flores. The survey relies on traps set in localities chosen on the basis of habitat and on sighting reports by local people. Over the past 20 years, habitat loss has caused the species to vanish from an area stretching for

sources, in a transition to sustainable land use. Local officials have already expressed interest in such a plan. For example, slash-and-burn agriculture could be superseded by the cultivation of plant species that do not require clearing of the canopy to be economically useful. A technique as simple as instruction in the manufacture and laying of brick could save hardwood now harvested for house construction. The fate of the world’s few thousand Komodos, living out their lives in a tiny corner of the earth, is probably now in human hands. Policy decisions, as in so many wildlife conservation issues, will be as much aesthetic as scientific or economic. We can choose to create a homogeneous world of stultifying sameness. Or we can choose to maintain a remnant of the mystery that provoked medieval cartographers to mark the unexplored territories of their maps with the exhilarating warning, “Here there be dragons.” SA

The Author

Further Reading

CLAUDIO CIOFI received his undergraduate education at the University of Florence. In 1998 he completed his Ph.D. at the Durrell Institute of Conservation and Ecology at the University of Kent at Canterbury in England. He is now based at the Zoological Society of London. Ciofi has worked in collaboration with the University of Gadjah Mada in Java and with Udayana University in Bali. His Komodo project, originating as a population genetic study, has broadened to include behavioral ecology and demography and the consequent protection of habitat and involvement of indigenous people. His research has been supported by the Zoological Society of London, the Wildlife Conservation Society, the Smithsonian Institution, Earthwatch Institute and British Airways.

A Modern Dragon Hunt on Komodo. L. Broughton in National Geographic, Vol. 70, pages 321–331; 1936. Zoo Quest for a Dragon. David Attenborough. Lutterworth Press, 1957. Reprinted by Oxford University Press, 1986. The Behavioral Ecology of the Komodo Monitor. Walter Auffenberg. University of Florida–University Presses of Florida, 1981. Komodo: The Living Dragon. New edition. Dick Lutz and J. Marie Lutz. Dimi Press, Oregon, 1996. A lecture by Walter Auffenberg is available (in RealAudio) at www.si.edu/natzoo/hilights/lectures.htm on the World Wide Web.


Slave-Making Queens Life in certain corners of the ant world is fraught with invasion, murder and hostage-taking. The battle royal is a form of social parasitism Originally published in November 1999

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by Howard Topoff

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ILLUSTRATION BY ROBERTO OSTI

n the animal world, both predators and parasites survive at the expense of other species. Nevertheless, they don’t get the same press. I am besieged with mail containing pleas for money on behalf of wolves and killer whales, but I have yet to see a T-shirt with the slogan “Long Live the Hookworm.” The problem is, of course, that humans associate a parasitic lifestyle with disease. Our perception is of a furtive organism that insinuates itself inside us and, unlike a decent predator, intends to destroy us ever so slowly. But there exists a form of parasitism considerably less macabre. Social parasitism, as it is called, has evolved independently in such diverse creatures as ants and birds. A female cuckoo, for instance, lays her egg in the nest of another species, such as a warbler, and leaves it for the host to rear. The brown-headed cowbird does the same. Each bird has evolved so that it produces eggs that match those of its chosen baby-sitter. Even more varied than these avian parasites are the slave-making ants. The unusual behavior of the parasitic ant Polyergus breviceps—which I have been studying for 15 years in Arizona at the American Museum of Natural History’s Southwestern Research Station— offers a perfect ex-

SLAVE RAID by Polyergus ants on a Formica ant colony can be a complex undertaking. The Polyergus workers charge into a Formica nest (1), stealing pupae that they will take back home and enslave. Meanwhile young Polyergus queens mate amid this warring frenzy, and then each one sets off alone to establish her own colony (2). The newly mated queen battles Formica workers at the entrance of their burrow some distance from her natal nest (3), fights her way to the Formica queen in the chamber below and kills her (4). By licking the dying queen, the Polyergus queen acquires chemicals that win over the Formica workers, and so they tend to her eggs as well as those of their deceased queen (5).


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COURTESY OF HOWARD TOPOFF

These ants have completely lost the ability to care for themselves. The workers do not forage for food, feed the young or the queen, or even clean up their own nest.

FORMICA PUPA (left) is carried by a Polyergus worker to the Polyergus nest, where it will become part of a brood that the previously captured Formica slaves attend to. Formica worker (right) emerges from its pupal state and views itself as a Polyergus, because that is the only life it knows. It cares for the Polyergus workers and queen, feeding them, cleaning the nest and even moving the nest if it becomes too crowded. A colony of 2,000 Polyergus may have as many as 3,000 Formica slaves. Without them, the colony would perish.

ample. Like the other four species of Polyergus found throughout the world, these ants have completely lost the ability to care for themselves. The workers do not forage for food, feed the young or the queen, or even clean up their own nest. To survive, Polyergus ants must get workers from the related ant genus Formica to do their chores for them. Thus, Polyergus workers periodically undertake a slave raid in which about 1,500 of them travel up to 150 meters (492 feet), enter a Formica nest, expel the Formica queen and workers, and capture the pupae. Back at the Polyergus nest, slaves rear the raided brood until the young emerge. The newly hatched Formica workers then assume all responsibility for maintaining the mixedspecies nest. They forage for nectar and dead arthropods, regurgitate food to colony members, remove wastes and excavate new chambers. When the population becomes too large for the existing nest, it is the 3,000 or so Formica slaves that locate another site and physically transport the approximately 2,000 Polyergus workers, together with eggs, larvae, pupae and even the queen, to the new nest. This master-slave arrangement is not unique. Of the approximately 8,800 species of ants, at least 200 have evolved some form of symbiotic relationship with one another. At one end of the behavioral continuum are facultative parasites, such as the ant Formica wheeleri. These ants are capable of caring for themselves but undertake periodic slave raids on different ant species to supplement their labor force. In contrast, Polyergus and other dulotic (from the Greek word for “servant”) ants are obligatory social parasites. The workers and queen cannot survive without the assistance of slaves. My field research on Polyergus has been guided by one stubborn objective: to determine the most important adaptations in the evolution of obligatory social parasitism. Accordingly, I have homed in on the one behavior that is truly specific to Polyergus ants: the capacity of a queen to take over a

Formica nest single-handedly. Because, in addition to the large slave-capturing raids that can be seen in some other ant species, Polyergus has developed an unusual way for a new queen to establish her own colony. In most ant species, the process of setting up a new nest is straightforward. After flying away from her natal colony and mating, a queen tears away her wings, excavates a chamber, lays a few eggs and nourishes her larvae with stored nutrients. When the brood matures, the adult workers immediately assume the job of colony maintenance. But a parasitic queen like Polyergus is incapable of rearing her first brood without slaves. So she is confronted with a seemingly impossible mission: to invade a colony of Formica, kill the resident queen and become accepted by the workers. Moreover, she must accomplish all this without the assistance of a single soldier ant. For several weeks every year, a few hundred eggs laid by an established Polyergus queen develop into males and into queens that leave the parent colony and attempt to form a new one. In Arizona the young queens of P. breviceps have waived even the most traditional sexual ritual among ants: the mating flight. Instead of soaring off, winged Polyergus queens embark with workers in a well-timed slave raid. Amid the tumult of the advancing swarm, a primed queen will stop running, attract a male with a pheromone from her mandibular gland, mate with him and then pull off her wings. (Clandestine it’s not.) Two strategies of colony founding are now available to this just-inseminated queen. First, she may continue in the slave raid and arrive in an invaded colony of Formica whose workers and queen are scattered across the terrain. Such disorganization could facilitate the queen’s mission, but success is usually short-lived. The problem is that colonies of Polyergus are extremely territorial and will not tolerate other colonies of the same species within their raiding turf. The next time this (now usurped) nest is raided by the parent Polyer-


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gus colony, the new Polyergus queen, along with any workers she has produced, will be destroyed. The alternative tactic for an up-and-coming Polyergus queen is to bolt from the raiding column and on her own locate a more distant colony of Formica. Although there are no guarantees, this behavior at least increases the likelihood of finding an appropriate host nest outside the raiding territory of a resident Polyergus population. Killing Machines

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fter locating a suitable Formica nest, the serious business of colony usurpation begins. Because this takes place underground, where direct observations are not possible, my graduate students and I conducted our studies using trans-

and I added a twist to our original study: we killed the Formica queen— by freezing and defrosting her— immediately prior to introducing the Polyergus female. Our hypothesis predicted that the Polyergus queen would still have to attack the dead host queen, pierce her exoskeleton and ingest her body fluids. The results were exactly as we had anticipated. On entering the nest, the Polyergus queen pounced on the motionless Formica queen and started to bite and lick her for about 25 minutes, just as if she were alive. As soon as she finished “killing” the lifeless Formica queen, the Polyergus queen was groomed by the Formica workers and permanently accepted as their new ruler. A second prediction of the “chemical acquisition” hypothesis is that it would be difficult for a Polyergus queen to be welcomed by Formica workers if no Formica queen were

To unravel the mystery, it became clear that we had to start thinking like an ant. parent laboratory nests. Before each test we placed 15 Formica gnava workers in a nest with 15 pupae and one queen. (In contrast, a wild colony of F. gnava contains about 5,000 workers.) We then placed a newly mated Polyergus queen just outside the nest. In most cases the Polyergus queen quickly detects the entrance and erupts into a frenzy of ruthless activity. She bolts straight for the Formica queen, literally pushing aside any Formica workers that attempt to grab and bite her. Our earlier studies had shown that the Polyergus queen’s two main defensive adaptations are powerful mandibles for biting her attackers and a repellent pheromone secreted from the Dufour’s gland in her abdomen. With worker opposition liquidated, the Polyergus queen grabs the Formica queen and bites her head, thorax and abdomen for an unrelenting 25 minutes. Between bouts of biting she uses her extruded tongue to lick the wounded parts of her dying victim. Within seconds of the host queen’s death, the nest undergoes a most remarkable transformation. The Formica workers behave as if sedated. They calmly approach the Polyergus queen and start grooming her— just as they did their own queen. The Polyergus queen, in turn, assembles the scattered Formica pupae into a neat pile and stands triumphantly on top of it. At this point, colony takeover is a done deal. The Royal Feast

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ur next goal was to find the key to this remarkable brainwashing of the Formica workers. One hypothesis was “chemical acquisition,” whereby the Polyergus queen acquires Formica queen chemicals during the act of killing and licking her. To test this idea, my student Ellen Zimmerli

present in the nest. So in our next series of laboratory studies we simply removed the Formica queen before introducing the Polyergus female. Sure enough, this act provoked the proverbial battle royal. Fighting between the Formica workers and the Polyergus queen was relentless. Although neither species has a stinger, the mandibles of the workers are sufficiently formidable to pin the queen down by the legs and bite her until she dies. Wanted: Single Queen with Workers

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ecause mature Formica nests often have many queens— unlike Polyergus colonies—we were also curious to see what would happen when a newly mated Polyergus queen invaded a polygynous nest. We established a series of Formica colonies that contained between two and 25 queens. Surprisingly, the number of Formica queens was of no consequence to the Polyergus queen. Because she is accepted as the royal party once she dispatches the first Formica queen, she is in no rush. Hour by hour, day by day, she methodically locates and kills every Formica queen, sometimes taking several weeks to clear out all remnants of the opposition. Although our tests had uncovered this suite of behavioral adaptations on the part of Polyergus queens, we also discovered that success was not routine. Sometimes the phalanx of Formica workers in the queen’s path was simply too powerful, and she was ripped to pieces. Perhaps, I thought, queens have another strategy. Because the mating seasons of Polyergus and Formica queens overlap, it seemed reasonable to postulate that they must, at least occasionally, encounter one another on the ground shortly after mating. Suppose a Polyergus queen killed a Formica queen in the field? Having thus


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deed, it took an additional five months, by which time 19 young Formica workers were present, before the Polyergus queen assaulted the Formica queen. Despite her previous disinterest, it was clear that the Polyergus queen had retained her regicidal inclination and aptitude. The Formica queen was killed, and the handful of newly emerged workers accepted the Polyergus as their new queen. We concluded that the chemistry of the Formica queen must change dramatically between the moment of fertilization and the time she has an established nest. But it appears that the change is a maturational one brought about by internal processes, not by merely having a brood. Elucidating the nature of this chemical transformation should prove a fruitful path for future studies. A Dangerous Living

TOM MOORE

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FORMICA NESTS (red) that are attacked often lie within 150 meters (492 feet) of a Polyergus nest (center). This particular Polyergus colony conducted 14 raids on 12 Formica colonies in the course of about six weeks between July 15 and August 24.

acquired the relevant chemicals, the victorious Polyergus queen should immediately be able to enter any Formica colony with impunity. Without worker attacks to contend with, this queen could leisurely embark on her killing spree, eliminating any resident Formica queens. Not so. When we introduced a newly mated Polyergus queen to a newly mated queen of F. gnava, the result was a nonevent. The two spent a few seconds checking each other out with their antennae, but we never witnessed a single aggressive interaction between any of the opposing queens we tested. These results suggested that young Formica queens do not possess the same chemical signature found in more mature queens. To figure out when a Formica queen takes on the aura, or “aroma,” of an established queen, we set up another experiment. Christine A. Johnson and I kept newly mated Formica queens in laboratory nests until they laid their eggs. Then we repeated the earlier test. Still no interest on the part of Polyergus. After several weeks the eggs hatched into larvae, and we conducted yet another round of tests. The Polyergus queens continued to ignore their Formica counterparts. To unravel the mystery, it became clear that we had to start thinking like an ant. Suppose, we reasoned, a newly mated Polyergus queen entered a new nest and killed a Formica queen that was raising her first brood of eggs or larvae. The invading queen would be unable to feed herself or the brood and would soon starve. The earliest time that killing the Formica queen would be effective is when her brood had developed into workers eager to assist in foraging and nest maintenance. Johnson discovered that it took almost two months from the time a Formica queen was inseminated to the stage when her first brood completed development. As soon as these first eight workers were functional, Johnson introduced a Polyergus queen that had been ruling her own nest of Formica workers. Surprisingly, the Polyergus queen remained passive. In-

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aving determined that invading an established Formica nest is the key to successful colony takeover, we were faced with one final thorny issue. Linda Goodloe, a graduate student working with the eastern species Polyergus lucidus, had discovered that new queens go after only the Formica species that they grew up with—in other words, the ones that had been enslaved by their parent queen’s colony. But social parasitism requires intricate behavioral interactions between two species: parasite and host. Clearly, the evolution from a free-living to a parasitic way of life required that a newly mated queen occasionally invade the nest of an unfamiliar species. Although a risky business at best, a successful adoption by the foreign workers would enable the invading queen to lay many more eggs than she could possibly raise on her own. Rapid colony development, in turn, would set the stage for the debut of slave raids and the chemical imprinting necessary for the slave ants to care for their captors. So we decided to set up a situation in which this chance happening could occur. To do so, we traveled to a habitat higher in elevation, one where Polyergus conducts slave raids on Formica occulta instead of F. gnava. We captured colonies of F. occulta, installed them in our laboratory nests and introduced a newly mated Polyergus queen from a colony found at the lower elevation—a colony that therefore contained F. gnava slaves. As expected, attempts by Polyergus queens to take over colonies of Formica containing unfamiliar workers and queens were only partially successful. Five Polyergus queens showed no interest in attacking the F. occulta queens; three of these nonaggressive Polyergus queens were killed by F. occulta workers, and two others evaded attack by abandoning the nest. But the most significant outcome was that two of the seven Polyergus queens did seize and kill the foreign Formica queen. And when they had finished licking the dead ruler, both Polyergus queens were promptly adopted by the F. occulta workers. What’s in a Name?

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n Origin of Species, Charles Darwin’s description of Polyergus shows that he was keenly aware of the numerous conundrums raised by the evolution of social parasitism— one of those being the issue of what is in it for the slaves. After all, a colony of Formica can forfeit more than 14,000 pupae during a single raiding season. Their only evolutionary “defense” seems to be brood replacement, thanks to the Formica queen’s enor-

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COURTESY OF HOWARD TOPOFF

The Polyergus queen is out for blood—or other body fluids.

BATTLE ROYAL between the Formica queen (left) and the Polyergus queen (right) can take 30 minutes or more. Roughly the same size and often evenly matched, the queens repeatedly bite

each other with their strong jaws. If the Polyergus queen wins, she licks the wounds of the Formica queen, thereby gathering the chemicals that make the Formica workers view her as their leader.

mous reproductive ability. Although defenseless Formica pupae are unable to thwart their capture, it is unclear why adult slaves don’t abandon the Polyergus colony and rejoin their free-living nestmates. The answer lies in imprinting. Newly hatched slaves view the Polyergus workers, brood and queen as their family. Even though they do not participate in raids on other Formica nests, the slaves respond aggressively to any Formica they meet while foraging. The imprinting process is similar to that occurring between a duckling and its mother—except that in ants the stimuli are chemical rather than visual and auditory. The fact that parasitism develops from olfactory bonds between Formica and Polyergus suggests that “slavery” is an inappropriate term for these insects. A more accurate human analogy would be adoption, because the Polyergus nest is the only “home” ever known by Formica workers. Early experience can promote social bonds between different species of ants, but the process is not open-ended. The ability to form such interspecific attachments declines as the evolutionary relatedness of the creatures decreases. This fact explains why parasite-host relations invariably conform to the rule identified by Italian entomologist Carlo Emery: social parasites are taxonomically close to their hosts. Not surprisingly, this genetic relatedness is connected to ecological similarity—the quintessence of a successful parasite-host relationship. The Polyergus-Formica association works well precisely because Formica workers in a Polyergus nest need only conduct the same foraging and nest maintenance activities that they do in their own colonies. Having been reared in a Polyergus nest does not change Formica’s species-specific be-

haviors of foraging, feeding or fighting. (Fortunately, workers don’t mate.) Since the publication of Origin of Species, scientists have recognized social parasitism in insects and birds as a classic example of convergent evolution. My field and laboratory research on the most salient adaptations for parasitism by Polyergus reveal the depth of this convergence. In England, cuckoos parasitize four species of host, but any given individual female cuckoo specializes in one particular host species. And how does this female cuckoo select the appropriate host species? Simple: she uses the “Polyergus principle” of imprinting. Just as a Polyergus queen selects the same species of Formica present in her nest when she emerged, a female cuckoo opts for the host species in whose nest she hatched. When I first heard the term “social parasitism” as a college student, it sounded like an oxymoron. After all, the term “social” denotes communication, cooperation and even altruism— all diametrically opposed to the patently selfish habits of parasites. As I learned, however, the term is appropriate because a social parasite’s infiltration into the host’s life is based on the same developmental and communicative processes that both parasite and host use for interacting with members of their own species. Nevertheless, 15 years of research have reinforced my empathy with Darwin as he struggled to incorporate social parasitism into his theory of natural selection. As usual, Darwin put it best: “I tried to approach the subject in a skeptical frame of mind, as any one may well be excused for doubting the existence of so extraordinary an instinct as that of making slaves.” SA

Further Reading

The Author HOWARD TOPOFF became interested in social insects as an undergraduate, when he studied army ants in the department of animal behavior at the American Museum of Natural History in New York City. After receiving his Ph.D. in 1968 from a joint program of the museum and the City University of New York, he joined the museum as a curator and continued his field research on the social behavior of army ants. Though a professor in the department of psychology at Hunter College of C.U.N.Y., his research is field-oriented and based primarily at the museum’s Southwestern Research Station, located in the Chiricahua Mountains of Arizona. His interest in the evolution of behavior in social insects led to his more recent studies of slave-making ants. When not teaching or “slaving” away in the field, he develops multimedia science presentations for schoolchildren, college students and the adult public. He invites questions and can most easily be reached by e-mail: [email protected].

Colony Takeover by a Socially Parasitic Ant, POLYERGUS BREVICEPS: The Role of Chemicals Obtained during Host-Queen Killing. Howard Topoff and Ellen Zimmerli in Animal Behaviour, Vol. 46, Part 3, pages 479– 486; September 1993. Queens of the Socially Parasitic Ant POLYERGUS Do Not Kill Queens of FORMICA That Have Not Formed Colonies. Howard Topoff and Ellen Zimmerli in Journal of Insect Behavior, Vol. 7, No. 1, pages 119–121; January 1994. Adaptations for Social Parasitism in the Slave-Making Ant Genus POLYERGUS. Howard Topoff in Comparative Psychology of Invertebrates. Edited by Gary Greenberg and Ethel Tobach. Garland Publishing, 1997.

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Divided We Fall: Cooperation among Lions Although they are the most social of all cats, lions cooperate only when it is in their own best interest by Craig Packer and Anne E. Pusey

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n the popular imagination, lions hunting for food present a marvel of group choreography: in the dying light of sunset, a band of stealthy cats springs forth from the shadows like trained assassins and surrounds its unsuspecting prey. The lions seem to be archetypal social animals, rising above petty dissension to work together toward a common goal—in this case, their next meal. But after spending many years observing these creatures in the wild, we have acquired a less exalted view. Our investigations began in 1978, when we inherited the study of the lion population in Serengeti National Park in Tanzania, which George B. Schaller of Wildlife Conservation International of the New York Zoological Society

Originally published in May 1997

YOUNG FEMALE LIONS, shown here, band together in groups of six to 10, called prides. Such togetherness does not always make them more successful hunters, as scientists once presumed; loners frequently eat more than individuals in a pride do. Instead communal living makes lions better mothers: pridemates share the responsibilities of nursing and protecting the group’s young. As a result, more cubs survive into adulthood. COPYRIGHT 2004 SCIENTIFIC AMERICAN, INC.

PHOTOGRAPHS BY CRAIG PACKER


SISTERHOOD makes it possible for pridemates to protect their cubs against invading males (top). Angry groups can ward off lone males, which are on average nearly 50 percent larger than females (middle). And they will frequently attack and kill less powerful trespassing females (bottom).

began in 1966. We hoped to discover why lions teamed up to hunt, rear cubs and, among other things, scare off rivals with chorused roars. All this togetherness did not make much evolutionary sense. If the ultimate success of an animal’s behavior is measured by its lifetime production of surviving offspring, then cooperation does not necessarily pay: if an animal is too generous, its companions benefit at its expense. Why, then, did not the evolutionary rules of genetic self-interest seem to apply to lions? We confidently assumed that we would be able to resolve that issue in two to three years. But lions are supremely adept at doing nothing. To the list of inert noble gases, including krypton, argon and neon, we would add lion. Thus, it has taken a variety of research measures to uncover clues about the cats’ behavior. Indeed, we have analyzed their milk, blood and DNA; we have entertained them with tape recorders and stuffed decoys; and we have tagged individuals with radio-tracking collars. Because wild lions can live up to 18 years, the answers to our questions are only now becoming clear. But, as we are finding out, the evolutionary basis of sociality among lions is far more complex than we ever could have guessed. Claiming Territory

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ale lions form lifelong alliances with anywhere from one to eight others—not out of any fraternal goodwill but rather to maximize their own

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MALES are quick to challenge lions they do not know—real or not. When the authors played tape recordings of strange males roaring within a coalition’s turf, representatives from that coalition immediately homed in on the sound. Moreover, they often took the offensive, pouncing on decoys placed nearby.

chances for reproducing. Most companions are brothers and cousins that have been reared in the same nursery group, or crèche. Others consist of nonrelatives that teamed up after a solitary nomadic phase. Once matured, these coalitions take charge of female lion groups, called prides, and father all offspring born in the pride during the next two to three years. After that, a rival coalition typically moves in and evicts them. Thus, a male lion’s reproductive success depends directly on how well his coalition can withstand challenges from outside groups of other males. Male lions display their greatest capacity for teamwork while ousting invaders—the situation that presents the greatest threat to their common self-interest. At night the males patrol their territory, claiming their turf with a series of loud roars. Whenever we broadcast tape recordings of a strange male roaring within a coalition’s territory, the response was immediate. They searched out the speaker and would even attack a stuffed lion that we occasionally set beside it. By conducting dozens of these experiments, our graduate student Jon Grinnell found that unrelated companions were as cooperative as brothers and that partners would approach the speaker even when their companions could not monitor their actions. Indeed, the males’ responses sometimes bordered on suicidal, approaching the speaker even when they were outnumbered by three recorded lions to one. In general, large groups dominate smaller ones. In larger coalitions, the males are typically younger when they first gain entry into the pride, their subsequent tenure lasts longer and they have more females in their domain. Indeed, the reproductive advantages of cooperation are so great that most solitary males will join forces with other loners. These partnerships of nonrelatives, how-

SERENGETI NATIONAL PARK in Tanzania houses a population of lions that has been studied by scientists since 1966. 29 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE COPYRIGHT 2004 SCIENTIFIC AMERICAN, INC.

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PREY CAPTURE is usually done by a single lion, when the group is hunting warthog and wildebeest (photographs). Because she will very likely succeed in capturing such easy prey, her sisters will probably eat even if they refrain from the chase. Thus, the pride will often stand back at a safe distance, awaiting a free meal. But when a single lion is less likely to make a kill—say, if she is stalking zebra or buffalo—her pridemates will join in to pursue the prey together (charts).

HOW INDIVIDUAL LIONS ACT WHEN HUNTING PURSUE ALONE

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FOR BUFFALO

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KILLS are shared by the entire pride. If kills are made close to home, mothers bring their cubs to the feast. But they deliver nourishment from more distant kills in the form of milk.

ever, never grow larger than three. Coalitions of four to nine males are always composed of close relatives. Why do not solitary males recruit more partners until their groups also reach an insuperable size? The reasons again come down to genetic self-preservation and, in particular, weighing the odds of gaining access to a pride against those of actually fathering offspring. Although large coalitions produce the most offspring on a per capita basis, this averaging assumes fair division among companions—a form of cooperation that does not happen in the Serengeti. In fact, the first male to find a female in estrus will jealously guard her, mating repeatedly over the next four days and attacking any other male that might venture too close. Dennis A. Gilbert, in Stephen J. O’Brien’s laboratory at the National Cancer Institute, performed DNA fingerprinting on hundreds of our lion samples and found that one male usually fathered an entire litter. Moreover, reproduction was shared equally only in coalitions of two males. In the larger coalitions, a few males fathered most of the offspring. Being left childless is not too bad from a genetic standpoint if your more successful partner is your brother or cousin. You can still reproduce by proxy, littering the world with nephews and nieces that carry your genes. But if you are a lone lion, joining forces with more than one or two nonrelatives does not pay off. Hunting

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raditionally, female lions were thought to live in groups because they benefited from cooperative hunting. (The females hunt more often than the resident males.) But on closer examination, we have found that groups of hunting lions do not feed any better than solitary females. In fact, large groups end up at a disadvantage because the companions often refuse to cooperate in capturing prey. Once one female has started to hunt, her companions may or may not join her. If the prey is large enough to feed the entire pride, as is the usual case, the companions face a dilemma: although

a joint hunt may be more likely to succeed, the additional hunters must exert themselves and risk injury. But if a lone hunter can succeed on her own, her pridemates might gain a free meal. Thus, the advantages of cooperative hunting depend on the extent to which a second hunter can improve her companion’s chances for success, and this in turn depends on the companion’s hunting ability. If a lone animal is certain to succeed, the benefits of helping could never exceed the costs. But if she is incompetent, the advantages of a latecomer’s assistance may well exceed the costs. Evidence from a wide variety of bird, insect and mammalian species suggests that, as expected, cooperation is most wholehearted when lone hunters do need help. The flip side of this trend is that species are least cooperative when hunters can most easily succeed on their own. Consistent with this observation, our graduate student David Scheel found that the Serengeti lions most often work


together when tackling such difficult prey as buffalo or zebra. But in taking down easy prey—say, a wildebeest or warthog—a lioness often hunts alone; her companions watch from the sidelines. Conditions are not the same throughout the world. In the Etosha Pan of Namibia, lions specialize in catching one of the fastest of all antelopes, the springbok, in flat, open terrain. A single lion could never capture a springbok, and so the Etosha lions are persistently cooperative. Philip Stander of the Ministry of Environment and Tourism in Namibia has drawn an analogy between their hunting tactics and a rugby team’s strategy, in which wings and centers move in at once to circle the ball, or prey. This highly developed teamwork stands in sharp contrast to the disorganized hunting style of the Serengeti lions. All female lions, whether living in the Serengeti or elsewhere, are highly cooperative when it comes to rearing young. The females give birth in secrecy and AUGUST 2004


NURSING is a job shared by all mothers in a pride, not out of generosity but, rather, fatigue. Cubs feed when their mothers return from hunting (top). If the mothers stay awake, they will not let cubs other than their own, such as the large adolescent shown, take milk from them (bottom). Although cubs try to nurse most often from their own mothers, they can be quite cunning in their attempts to nurse from other females (charts). NURSING ATTEMPTS BY CUBS ON MOTHERS ON OTHER FEMALES 0

0.1 0.2 0.3 0.4 0.5 NUMBER OF ATTEMPTS (PER FEMALE PER HOUR)

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WHEN OTHER CUBS ARE ALREADY NURSING ON MOTHERS ON OTHER FEMALES WHEN CUB GREETS THE FEMALE ON MOTHERS ON OTHER FEMALES 0

keep their litters hidden in a dry riverbed or rocky outcrop for at least a month, during which time the cubs are immobile and most vulnerable to predators. Once the cubs can move, though, the mothers bring them out into the open to join the rest of the pride. If any of the other females have cubs, they form a crèche and remain in near-constant association for the next year and a half before breeding again. The mothers lead their cubs to kills nearby but deliver nourishment from more distant meals in the form of milk. When they return from faraway sites, the mothers collapse, leaving their youngsters to nurse while they sleep. We have studied over a dozen crèches, and in virtually every case, each cub is allowed to nurse from each mother in the group. Communal nursing is a major component of the lion’s cooperative mystique. And yet, as with most other forms of cooperation among lions, this behavior

is not as noble as it seems. The members of a crèche feed from the same kills and return to their cubs in a group. Some are sisters; others are mother and daughter; still others are only cousins. Some have only a single cub, whereas a few have litters of four. Most mothers have two or three cubs. We milked nearly a dozen females and were surprised to discover that the amount of milk from each teat depended on the female’s food intake and not on the actual size of her brood. Because some females in a pride have more mouths to feed, yet all produce roughly the same amount of milk, mothers of small litters can afford to be more generous. And in fact, mothers of single cubs do allow a greater proportion of their milk to go to offspring that are not their own. These females are most generous when their crèchemates are their closest relatives. Thus, milk distribution depends in large part on a pattern of surplus production and on kinship. These


0.1 0.2 0.3 0.4 0.5 0.6 PROPORTION OF ATTEMPTS

factors also influence female behavior across species: communal nursing is most common in those mammals—including rodents, pigs and carnivores— that typically give birth to a wide range of litter sizes and live in small kin groups. Although female lions do nurse the offspring of other females, they try to give milk primarily to their own cubs and reject the advances of other hungry cubs. But they also need sleep. When they doze for hours at a time, they present the cubs with an enormous temptation. A cub attempting to nurse from a lioness who is not its mother will generally wait until the female is asleep or otherwise distracted. The females must therefore balance the effort needed to resist the attentions of these pests against their own exhaustion. Generosity among female lions, then, is largely a matter of indifference. Females that have the least to lose sleep best—owing either to the small size of AUGUST 2004

AFFECTION is common among pridemates, which rely on one another to help protect their young. Male lions present one of the greatest threats: if one coalition takes over a new pride, the newcomers—eager to produce their own offspring—will murder all the pride’s small cubs and drive the older cubs away.

their own litter or to the company of close relatives. Female spotted hyenas have resolved this conflict by keeping their cubs in a well-protected den. Mothers return to their cubs for short periods, feed their brood and then sleep somewhere else in peace. By watching hyenas at the den, we found that mother hyenas received as many nursing attempts from the cubs of other females as did mother lions, but the hyenas were more alert and so prevented any other than their own offspring from nursing. Surviving in the Serengeti

A

s we have seen, female lions are most gregarious when they have dependent young; the crèche is the social core of the pride. Childless females occasionally visit their maternal companions but generally keep to themselves, feeding well and avoiding the social complexities of the dining room or nursery. Mothers do not form a crèche to improve their cubs’ nutrition. And gregarious mothers may actually eat less than solitary mothers; they have no system of baby-sitting to ensure a more continuous food supply. Instead mother lions form a crèche only to defend themselves and their cubs. A female needs two years to rear her cubs to independence, but should her cubs die at any point, she starts mating within a few days, and her interval between births is shortened by as much as a year. Male lions are rarely affectionate to their offspring, but their territorial excursions provide effective protection. Should the father’s coalition be

ousted, however, the successors will be in a hurry to raise a new set of offspring. Any cubs left over from the previous regime are an impediment to the new coalition’s immediate desire to mate and so must be eliminated. More than a quarter of all cubs are killed by invading males. The mothers are the ultimate victims of this never-ending conflict, and they vigorously defend their cubs against incoming males. But the males are almost 50 percent larger than the females, and so mothers usually lose in one-on-one combat. Sisterhood, on the other hand, affords them a fighting chance; in many instances, crèchemates succeed in protecting their offspring. Male lions are not their only problem. Females, too, are territorial. They defend their favorite hunting grounds, denning sites and water holes against other females. Large prides dominate smaller ones, and females will attack and kill their neighbors. Whereas most males compress their breeding into a few short years, females may enjoy a reproductive life span as long as 11 years. For this reason, boundary disputes between prides last longer than do challenges between male coalitions, and so the females follow a more cautious strategy when confronted by strangers. Karen E. Mc-

Comb, now at the University of Sussex, found that females would attempt to repel groups of tape-recorded females only when the real group outnumbered the taped invaders by at least two. Females can count, and they prefer a margin of safety. Numbers are a matter of life and death, and a pride of only one or two females is doomed to a futile existence, avoiding other prides and never rearing any cubs. The lions’ pride is a refuge in which individuals united by common reproductive interests can prepare for the enemy’s next move. The enemy is other lions—other males, other females—and they will never be defeated. Over the years, we have seen hundreds of males come and go, each coalition tracing the same broad pattern of invasion, murder and fatherhood, followed by an inevitable decline and fall. Dozens of prides have set out to rule their own patch of the Serengeti, but for every new pride that has successfully established itself, another has disappeared. Lions can seem grand in their common cause, battling their neighbors for land and deflecting the unwanted advances of males. But the king of beasts above all exemplifies the evolutionary crucible in which a cooperative society is forged.

The Authors

Further Reading

CRAIG PACKER and ANNE E. PUSEY are professors in the department of ecology, evolution and behavior at the University of Minnesota. They conducted their studies at the Serengeti Wildlife Research Institute, the University of Chicago and the University of Sussex. Packer completed his Ph.D. in 1977 at Sussex. That same year, Pusey received her Ph.D. from Stanford University.

A Molecular Genetic Analysis of Kinship and Cooperation in African Lions. C. Packer, D. A. Gilbert, A. E. Pusey and S. J. O’Brien in Nature, Vol. 351, No. 6327, pages 562–565; June 13, 1991. Into Africa. Craig Packer. University of Chicago Press, 1994. Non-offspring Nursing in Social Carnivores: Minimizing the Costs. A. E. Pusey and C. Packer in Behavioral Ecology, Vol. 5, No. 4, pages 362–374; Winter 1994. Complex Cooperative Strategies in Group-Territorial African Lions. R. Heinsohn and C. Packer in Science, Vol. 269, No. 5228, pages 1260–1262; September 1, 1995.


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Parrots were once thought to be no more than excellent mimics, but research is showing that they understand what they say. Intellectually, they rival great apes and marine mammals

Originally published in Scientific American Presents: Exploring Intelligence 1998

Talking with Alex: Logic by Irene M. Pepperberg


TIMOTHY ARCHIBALD

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ye. I’m gonna go eat dinner. I’ll see you tomorrow,” I hear Alex say as I leave the laboratory each night. What makes these comments remarkable is that Alex is not a graduate student but a 22-year-old Grey parrot. Parrots are famous for their uncanny ability to mimic human speech. Every schoolchild knows “Polly wanna cracker,” but the general belief is that such vocalizations lack meaning. Alex’s evening good-byes are probably simple mimicry. Still, I wondered whether parrots were capable of more than mindless repetition. By working with Alex over the past two decades, I have discovered that parrots can be taught to use and understand human speech. And if communication skills provide a glimpse into an animal’s intelligence, Alex has proved that parrots are about as smart as apes and dolphins. When I began my research in 1977, the cognitive capacity of these birds was unknown. No parrot had gone beyond the level of simple mimicry in terms of language acquisition. At the time, researchers were training chimps to communicate with humans using sign language, computers and special boards decorated with magnet-backed plastic chips that represent words. I decided to take advantage of parrots’ ability to produce human speech to probe avian intelligence. My rationale was based on some similarities between parrots and primates. While he was at the University of Cambridge, Nicholas Humphrey proposed that primates had acquired advanced communication and cognitive skills because they live and interact in complex social groups. I thought the same might be true of Grey parrots (Psittacus erithacus). Greys inhabit dense forests and forest clearings across equatorial Africa, where vocal communication plays an important role. The birds use whistles and calls that they most likely learn by listening to adult members of the flock. Further, in the laboratory parrots demonstrate an ability to learn symbolic and conceptual tasks often associated with complex cognitive and communication skills. During the 1940s and 1950s, European researchers such as Otto D. W. Koehler and Paul Lögler of the Zoological Institute of the University of Freiburg had found that when parrots are exposed to an array of stimuli, such as eight flashes of light, some of them could subsequently select a set containing the same number of a different type of object, such as eight blobs of clay.

Because the birds could match light flashes with clay blobs on the basis of number alone means that they understood a representation of quantity—a demonstration of intelligence. But other researchers, including Orval H. Mowrer, found that they were unable to teach these birds to engage in referential communication—that is, attaching a word “tag” to a particular object. In Mowrer’s studies at the University of Illinois, a parrot might learn to say “hello” to receive a food reward when its trainer appeared. But the same bird would also say “hello” at inappropriate times in an attempt to receive another treat. Because the parrot was not rewarded for using the word incorrectly, eventually it would stop saying “hello” altogether. Some of Mowrer’s parrots picked up a few mimicked phrases, but most learned nothing at all. Because parrots communicate effectively in the wild, it occurred to me that the failure to teach birds referential speech might stem from inappropriate training techniques rather than from an inherent lack of ability in the psittacine subjects. For whatever reason, parrots were not responding vocally to the standard conditioning techniques used to train other species to perform nonverbal tasks. Interestingly, many of the chimpanzees that were being taught to communicate with humans were not being trained with the standard paradigms; perhaps parrots would also respond to nontraditional training. To test this premise, I designed a new method for teaching parrots to communicate.

Go Ask Alex The technique we use most frequently involves two humans who teach each other about the objects at hand while the bird watches. This so-called model/rival (M/R) protocol is based, in part, on work done by Albert Bandura of Stanford University. In the early 1970s Bandura showed that children learned difficult tasks best when they were allowed to observe and then practice the relevant behavior. At about the same time, Dietmar Todt, then at the University of Freiburg, independently devised a similar technique for teaching parrots to replicate human speech. In a typical training session, Alex watches the trainer pick up an object and ask the human student a question about it:

and Speech in Parrots 35 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE


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for example, “What color?” If the student answers correctly, he or she receives praise and is allowed to play with the object as a reward. If the student answers incorrectly, however, the trainer scolds him or her and temporarily removes the object from sight. The second human thus acts as a model for Alex and a rival for the trainer’s attention. The humans’ interactions also demonstrate the consequences of an error: the model is told to try again or to talk more clearly. We then repeat the training session with the roles of trainer and model reversed. As a result, Alex sees that communication is a two-way street and that each vocalization is not specific to an individual. In Todt’s studies, birds were exposed only to pairs of individuals who maintained their respective roles. As a result, his birds did not respond to anyone other than the human who initially posed the questions. In contrast, Alex will respond to, interact with and learn from just about anyone. The fact that Alex works well with different trainers suggests that his responses are not being cued by any individual—one of the criticisms often raised about our studies. How could a naive trainer possibly cue Alex to call an almond a “cork nut”—his idiosyncratic label for that treat? In addition to the basic M/R system, we also use supplemental procedures to enhance Alex’s learning. For example, once Alex begins to produce a word describing a novel item, we talk to him about the object in full sentences: “Here’s the paper” or “You’re chewing paper.” Framing “paper” within a sentence allows us to repeat the new word frequently and with consistent emphasis, without presenting it as a single, repetitive utterance. Parents and teachers often use such vocal repetition and physical presentation of objects when teaching young children new words. We find that this technique has two benefits. First, Alex hears the new word in the way that it is used in normal speech. Second, he learns to produce the term without associating verbatim imitation of his trainers with a reward. We also use another technique, called referential mapping, to assign meaning to vocalizations that Alex produces spontaneously. For example, after learning the word “gray,” Alex came up with the terms “grape,” “grate,” “grain,” “chain” and “cane.” Although he probably did not produce these specific new words intentionally, trainers took advantage of his wordplay to teach him about these new items using the modeling and sentenceframing procedures described earlier. Finally, all our protocols differ from those used by Mowrer and Todt in that we reward correct responses with intrinsic reinforcers—the objects to which the targeted questions refer. So if Alex correctly identifies a piece of wood, he receives a piece of wood to chew. Such a system ensures that at every interaction, the subject associates the word or concept to be learned with the object or task to which it refers. In contrast, Mowrer’s programs relied on extrinsic reinforcers. Every correct answer would be rewarded with a preferred food item—a nut, for example. We think that such extrinsic rewards may delay learning by causing the animal to confuse the food item with the concept being learned. Of course, not every item is equally appealing to a parrot. To keep Alex from refusing to answer any question that doesn’t involve a nut, we allow him to trade rewards once he has correctly answered a question. If Alex correctly identifies a key, he can receive a nut—a more desirable item—by asking for it directly, with a simple “I wanna nut.” Such a protocol provides some flexibility but maintains referentiality of the reward.

What’s Different, What’s the Same I began working with Alex when he was 13 months old—a baby in a species in which individuals live up to 60 years in captivity. Through his years of training Alex has mastered tasks once thought to be beyond the capacity of all but humans and certain nonhuman primates. Not only can he produce and understand labels describing 50 different objects and foods but he also can categorize objects by color (rose, blue, green, yellow, orange, gray or purple), material (wood, wool, paper, cork, chalk, hide or rock) and shape (objects having from two to six corners, where a two-cornered object is shaped like a football). Combining labels for attributes such as color, material and shape, Alex can identify, request and describe more than 100 different objects with about 80 percent accuracy. In addition to understanding that colors and shapes represent different types of categories and that items can be categorized accordingly, Alex also seems to realize that a single object can possess properties of more than one category— a green triangle, for example, is both green and three-cornered. When presented with such an object Alex can correctly characterize either attribute in response to the vocal queries “What color?” or “What shape?” Because the same object is the subject of both questions, Alex must change his basis for classification to answer each query appropriately. To researchers such as Keith J. Hayes and Catherine H. Nissen, who did related work with a chimpanzee at the Yerkes Regional Primate Research Center at Emory University, the ability to reclassify items indicates “abstract aptitude.” On such tests, Alex’s accuracy averages about 80 percent. Alex has also learned the abstract concepts of “same” and “different.” When shown two identical objects or two items that vary in color, material or shape, Alex can name which attributes are the same and which are different. If nothing about the objects is the same or different, he replies, “None.” He responds accurately even if he has not previously encountered the objects, colors, materials or shapes. Alex is indeed responding to specific questions and not just randomly chattering about the physical attributes of the objects. When presented with a green, wooden triangle and a blue, wooden triangle, his accuracy was above chance on questions such as “What’s same?” If Alex were ignoring the question and responding based on his prior training, he might have responded with the label for the one anomalous attribute—“color”— rather than either of the correct answers—“matter” or “shape.” Alex’s comprehension matches that of chimpanzees and dolphins. He can examine a tray holding seven different objects and respond accurately to questions such as “What color is object-X?” or “What object is color-Y and shape-Z?” A correct response indicates that Alex understood all parts of the question and used this understanding to guide his search for the one object in the collection that would provide the requested information. His accuracy on such tests exceeds 80 percent. We also used a similar test to examine Alex’s numerical skills. He currently uses the terms “two,” “three,” “four,” “five” and “sih” (the final “x” in “six” is a difficult sound for a parrot to make) to describe quantities of objects, including groupings of novel or heterogeneous items. When we show Alex a “confounded number set”—a collection of blue and red keys and toy cars, for example—he can correctly answer questions about the number of items of a particular color and form, such as “How many blue key?” His accuracy in this test, 83.3 percent,


AUGUST 2004

TRANSCRIPTS OF DIALOGUES indicate that Alex can count objects on a tray. Dialogue 1, recorded in 1986, shows that Alex can distinguish five objects of two different types— in this case, plant stakes and keys. Dialogue 2, from 1997, reveals that Alex has become more sophisticated in his ability: presented with a more complex set of objects), Alex can count the number of blue blocks and green wool balls without being distracted by the other items on the tray.

DIALOGUE 1 Alex is shown two plant stakes and three keys on a tray. Trainer: How many key? Alex: Wood Irene (with back to tray, to trainer): Are there any wood? Trainer (to Irene): Yes. Irene: Try that. Trainer: Okay, tell me, how many wood? Alex: Two. Irene: Two? Trainer: Yes. Alex is given one stake, which he chews apart. It is replaced, and the tray is presented again. Trainer: Alex: Trainer: Alex: Trainer: Alex: Trainer:

Now, how many key? Key. That’s right, keys. How many? Two wood. There are two wood, but you tell me, how many key? Five. Okay, Alex, that’s the number of toys; you tell me, how many key? Alex: Three. Irene: Three? Trainer: Good boy! Here’s a key.

DIALOGUE 2 Irene: Okay, Alex, here’s your tray. Will you tell me how many blue block? Alex: Block. Irene: That’s right, block…how many blue block? Alex: Four. Irene: That’s right. Do you want the block? Alex: Wanna nut. Irene: Okay, here’s a nut. (Waits while Alex eats the nut.) Now, can you tell me how many green wool? Alex: Sisss... Irene: Good boy!

equals that of adult humans who are given a very short time to quantify similarly a subset of items on a tray, according to work done by Lana Trick and Zenon Pylyshyn of the University of Western Ontario. Alex also comprehends at least one relative concept: size. He responds accurately to questions asking which of two objects is the bigger or smaller by stating the color or material of the correct item. If the objects are of equal size, he responds, “None.” Next, we will try to get Alex to tackle relative spatial relations, such as over and under. Such a proposition presents an added challenge because an object’s position

relative to a second object can change: what is “over” now could be “under” later. One last bit of evidence reinforces our belief that Alex knows what he is talking about. If a trainer responds incorrectly to the parrot’s requests—by substituting an unrequested item, for example—Alex generally responds like any dissatisfied child: he says, “Nuh” (his word for “no”), and repeats his initial request. Taken together, these results strongly suggest that Alex is not merely mimicking his trainers but has acquired an impressive understanding of some aspects of human speech.

Tricks of the Training

What is it about our technique that allows Alex to master these skills? To address that question, we enlisted a few years ago the help of Alo, Kyaaro and Griffin—three other juvenile Grey parrots. Of the many different variations on our technique we tried with these parrots, none worked as well as the two-trainer interactive system. We attempted to train Alo and Kyaaro using audiotape recordings of Alex’s training sessions. The birds also watched video versions of Alex’s sessions while they were in isolation (with an automated system providing rewards) or in the presence of trainers who were slightly interactive. Griffin viewed the same videos in the presence of a highly interactive human trainer who rephrased material on the video and questioned the bird directly. Although all three parrots occasionally mimicked the targeted labels presented in the interactive video sessions, they failed to learn referential speech in any of these situations. When we then trained these birds using the standard M/R protocol, their test scores improved dramatically. In the past two years Griffin, for example, has acquired labels for seven objects and is beginning to learn his colors. The parrots’ failure to learn from the alternative techniques suggests that modeling and social interactions are important for maintain-



Target items

Keys

Wood

ALEX’S ACCURACY in identifying the number of targeted items in 1986 was 70 percent (seven out of 10 questions); now Alex is correct more than 80 percent of the time.

Correct

Mowrer demonstrated communication skills that were far less flexible and less “languagelike” than those of apes trained using systems that had more in common with our techniques.

Wood

2

Rocks

2

Keys

3

Wood

2

Jacks

4

Yellow wool

4

Corks

2

Rocks

Rock

Wood

Wool

Bird Brains

GEORGE RETSECK

Object set

Alex's response

Alex continues to perform as well as apes and dolphins in tests of intellectual acuity, even though the structure of the parrot brain differs considerably from that of terrestrial and aquatic mammals. Unlike primates, parrots have little gray matter and thus not much of a cerebral cortex, the brain region associated with cognitive processing in higher mammals. Other parts of Alex’s brain must power his cognitive function. The parrot brain also differs somewhat from that of songbirds, which are known for their vocal versatility. Yet Alex has surpassed songbirds in terms of the relative size of their “vocabularies.” In addition, he has learned to communicate with members of a different species: humans. With each new utterance, Alex and his feathered friends strengthen the evidence indicating that parrots are capable of performing complex cognitive tasks. Their skills reflect the innate abilities of parrots and suggest that we should remain open to discovering advanced forms of intelligence in other SA animals.

About the Author ing the birds’ attention during training and for highlighting which components of the environment should be noted, how new terms refer to novel objects and what happens when questions are answered correctly or incorrectly. All these concepts are critical in training birds to acquire some level of human-based communication. The M/R technique and some variants have also proved valuable in teaching other species referential communication. Diane Sherman of New Found Therapies in Monterey, Calif., uses the M/R technique for teaching language skills to developmentally delayed children. Even Kanzi, the bonobo (pygmy chimpanzee) trained by Sue Savage-Rumbaugh and her colleagues at Georgia State University, initially learned to communicate with humans via computer by watching his mother being trained—a variant of our modeling technique. Kanzi’s abilities are probably the most impressive of all primates’ trained to date. Chimpanzees have been taught human-based codes through a variety of techniques; however, apes that were trained using protocols similar to those developed by

IRENE M. PEPPERBERG’s work is for the birds— or so the funding agencies first thought. “My early grants came back with pink sheets basically asking what I was smoking,” she jokes. Pepperberg actually trained as a theoretical chemist: as a Ph.D. student at Harvard University, she generated mathematical models to describe boron compounds. But an episode of Nova featuring “signing” chimps, singing whales and squeaking dolphins drew her to her current work. “I was fascinated to see that people could study animal behavior as a career,” she says. Now Pepperberg is an associate professor at the University of Arizona at Tucson, a city that brings tears to her eyes— literally. “I’m allergic to everything that grows in Tucson,” Pepperberg says of the trees, grasses, molds and weeds. In 1997 she used the funds from a John Simon Guggenheim Memorial Foundation fellowship to write a book on parrot cognition and communication, In Search of King Solomon’s Ring: Studies on the Communicative and Cognitive Abilities of Grey Parrots (currently in press). Alex also has a life in publishing— he is the title character in Alex and Friends, a children’s book about the animals that have learned to communicate with humans. Through the Internet, you can order a special copy— one that Pepperberg has signed and Alex has chewed. It is available at www.azstarnet.com/nonprofit/alexfoundation/ on the World Wide Web.


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the

Originally published in January 2001

Cultures of

Chimpanzees Humankind’s nearest relative is even closer than we thought: chimpanzees display remarkable behaviors that can only be described as social customs passed on from generation to generation by Andrew Whiten and Christophe Boesch

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s researchers quietly approach a clearing in the Taï Forest of Ivory Coast, they hear a complex pattern of soft thuds and cracks. It sounds as though a small band of people are busy in the forest, applying some rudimentary technology to a routine task. On entering the clearing, the scientists observe several individuals working keenly at anvils, skillfully wielding wooden hammers. One or two juveniles have apprenticed themselves to the work and— more clumsily and with less success— are struggling to lift the best hammer they can find. All this activity is directed toward cracking rock-hard but nutritious coula nuts. Intermittently, individuals set aside their tools to gather more handfuls of nuts. An infant sits with her mother, gathering morsels of broken nuts. In many ways, this group could indeed be a family of foraging people. The hammers and anvils they leave behind, some made of stone, would excite the imagination of any anthropologist searching for signs of a primitive civilization. Yet these forest residents are not humans but chimpanzees. The similarities between chimpanzees and humans have been studied for years, but in the past decade researchers have determined that these resemblances run much deeper than anyone first thought. For instance, the nut cracking observed in the Taï Forest is far from a simple chimpanzee behavior; rather it is a singular adaptation found only in that particular part of Africa and a trait that biologists consider to be an expression of chimpanzee culture. Scientists frequently use the term “culture” to describe elementary animal behaviors— such as the regional dialects of different populations of songbirds— but as it turns out, the rich and varied cultural tradi-

tions found among chimpanzees are second in complexity only to human traditions. During the past two years, an unprecedented scientific collaboration, involving every major research group studying chimpanzees, has documented a multitude of distinct cultural patterns extending across Africa, in actions ranging from the animals’ use of tools to their forms of communication and social customs. This emerging picture of chimpanzees not only affects how we think of these amazing creatures but also alters human beings’ conception of our own uniqueness and hints at very ancient foundations for humankind’s extraordinary capacity for culture. Contemplating Culture

H

omo sapiens and Pan troglodytes have coexisted for hundreds of millennia and share more than 98 percent of their genetic material, yet only 40 years ago we still knew next to nothing about chimpanzee behavior in the wild. That began to change in the 1960s, when Toshisada Nishida of Kyoto University in Japan and Jane Goodall began their studies of wild chimpanzees at two field sites in Tanzania. (Goodall’s research station at Gombe— the first of its kind— is more famous, but Nishida’s site at Mahale is the second-oldest chimpanzee research site in the world.) In these initial studies, as the chimpanzees became accustomed to close observation, the remarkable discoveries began. Researchers witnessed a range of unexpected behaviors, including fashioning and using tools, hunting, meat eating, food sharing and lethal fights between members of neighboring com-


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Do Apes Ape? Recent studies show that chimpanzees and other apes can learn by imitation

he notion that the great apes—chimpanzees, gorillas, with three-year-old human children as subjects. Our reorangutans and gibbons—can imitate one another sults demonstrate that six-year-old chimpanzees show immight seem unsurprising to anyone who has watched itative behavior that is markedly like that seen in the chilthese animals playing at the zoo. But in scientific circles, dren, although the fidelity of their copying tends to be the question of whether apes, well, ape, has become con- poorer. In a different kind of experiment, one of us (Boesch), troversial. Consider a young chimpanzee watching his mother along with some co-workers, gave chimpanzees in the crack open a coula nut, as has been observed in the Taï Zurich Zoo in Switzerland hammers and nuts similar to Forest of West Africa. In most cases, the youth will even- those available in the wild. We then monitored the repertually take up the practice himself. Was this because he toire of behaviors displayed by the captive chimpanzees. imitated his mother? Skeptics think perhaps not. They ar- As it turned out, the chimpanzees in the zoo exhibited a gue that the mother’s attention to the nuts encouraged the greater range of activities than the more limited and foyoungster to focus on them as well. Once his attention cused set of actions we had seen in the wild. We interprethad been drawn to the food, the young chimpanzee ed this to mean that a wild chimpanzee’s cultural environlearned how to open the nut by trial and error, not by im- ment channeled the behavior of youngsters, steering them in the direction of the most useful skills. In the zoo, withitating his mother. Such a distinction has important implications for any out benefit of existing traditions, the chimpanzees experidiscussion of chimpanzee cultures. Some scientists define mented with a host of less useful actions. Interestingly, some of the results from the experiments a cultural trait as one that is passed down not by genetic inheritance but instead when the younger generation involving the artificial fruits converge with this idea. In one copies adult behavior. If cracking open a coula is some- study, chimpanzees copied an entire sequence of actions thing that chimpanzees can simply figure out how to do they had witnessed, but did so only after several viewings on their own once they hold a hammer stone, then it can’t and after trying some alternatives. In other words, they be considered part of their culture. Furthermore, if these tended to imitate what they had observed others doing at the expense of their own trialanimals learn exclusively by triand-error discoveries. al and error, then chimpanzees In our view, these findings must, in a sense, reinvent the taken together suggest that apes wheel each time they tackle a do ape and that this ability new skill. No cumulative culforms one strand in cultural ture can ever develop. transmission. Indeed, it is diffiThe clearest way to estabcult to imagine how chimpanlish how chimpanzees learn is zees could develop certain geothrough laboratory experigraphic variations in activities ments. One of us (Whiten), in such as ant-dipping and paracollaboration with Deborah M. site-handling without copying Custance of Goldsmiths Colestablished traditions. They lege, University of London, must be imitating other memconstructed artificial fruits to bers of their group. serve as analogues of those the We should note, however, animals must deal with in the that—just as is the case with huwild (right). In a typical experimans—certain cultural traits are ment, one group of chimpanno doubt passed on by a combizees watched a complex technation of imitation and simpler nique for opening one of the kinds of social learning, such as fruits, while a second group obhaving one’s attention drawn to served a very different method; useful tools. Either way, learnwe then recorded the extent to which the chimpanzees had PRACTICE MAKES PERFECT as a juvenile chimpanzee ing from elders is crucial to experiments with an artificial fruit it has been given to been influenced by the method “peel” after watching others do so. Such studies help growing up as a competent they observed. We also con- scientists determine how chimpanzees learn by imitat- wild chimpanzee. —A.W. and C.B. ducted similar experiments ing others. 40 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE COPYRIGHT 2004 SCIENTIFIC AMERICAN, INC.

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SARAH MARSHALL AND ANDREW WHITEN Ngamba, UWEX, Uganda

T

A Guide to the Cultures of Chimpanzees n an effort to catalogue cultural variations among chimpanzees, we asked researchers working at six sites across central Africa to classify chimpanzee behaviors in terms of occurrence or absence in seven communities. (There are two communities at Mahale.) The key categories were customary behavior, which occurs in most or all members of one age or sex class; habitual, which is less common but

Hammering nuts To crack open nutritious coula nuts, chimpanzees use stones as rudimentary hammers and anvils.

Pounding with pestle With the stalks of palm trees acting as makeshift pestles, chimpanzees can pound and deepen holes in trees.

Fishing for termites Chimpanzees insert thin, flexible strips of bark into termite mounds to extract the insects, which they then eat. Wiping ants off stick manually Once the ants have swarmed almost halfway up sticks dipped into the insects’ nests, chimpanzees pull the sticks through their fists and sweep the ants into their mouths. Eating ants directly off stick After a few ants climb onto sticks inserted into the nests, chimpanzees bring the sticks directly to their mouths and eat the ants.

Removing bone marrow With the help of small sticks, chimpanzees eat the marrow found inside the long bones of monkeys they have killed and eaten. Sitting on leaves A few large leaves apparently serve as protection when chimpanzees sit on wet ground. Fanning flies To keep flies away, chimpanzees utilize leafy twigs as a kind of fan.

Tickling self A large stone or stick can be used to probe especially ticklish areas on a chimpanzee’s own body.

which still occurs repeatedly; present; absent; and unknown. Certain behaviors are absent for ecological reasons (eco): for example, chimpanzees do not use hammers to open coula nuts at Budongo, because the nuts are not available. The survey turned up 39 chimpanzee rituals that are labeled as cultural variations; 18 are illustrated below. —A.W. and C.B.

MAHALE MAHALE TAÏ BOSSOU FOREST GOMBE M-GROUP K-GROUP KIBALE BUDONGO

customary customary

absent

absent

absent

absent (eco?)

absent (eco)

customary

absent

absent

absent (eco?)

absent (eco?)

absent (eco?)

absent (eco?)

absent

absent (eco)

customary

absent

customary

absent (eco)

absent (eco?)

present

absent

customary

absent

absent

absent

absent

customary customary

present

absent

absent

absent

absent

absent

customary

absent

absent

absent

absent

absent

present

habitual

absent

absent

absent

present

absent

absent

habitual

present

absent

absent

absent

habitual

absent

absent

habitual

absent

absent

absent

absent


AUGUST 2004

ILLUSTRATIONS BY PATRICIA J. WYNNE; MAP BY SUE CARLSON

I

Budongo, Uganda

Bossou, Guinea

Kibale, Uganda

Taï Forest, Ivory Coast

Gombe, Tanzania

TAÏ BOSSOU FOREST

MAHALE MAHALE GOMBE M-GROUP K-GROUP KIBALE BUDONGO

customary customary customary customary

absent

present

customary customary

absent

absent

absent

absent

present

absent

absent

absent

customary

habitual

customary

habitual

present

absent

habitual

present

present

absent

habitual

absent

absent

absent

customary customary

unknown

unknown

absent

customary

present

customary

habitual

absent

unknown

unknown

absent

customary customary

absent

absent

customary

absent

customary customary customary customary

present

absent

customary

absent

Mahale, Tanzania

Throwing Chimpanzees can throw objects such as stones and sticks with clear— though often inaccurate— aim.

Inspecting wounds When injured, chimpanzees touch wounds with leaves, then examine the leaves. In some instances, chimpanzees chew the leaves first. Clipping leaves To attract the attention of playmates or fertile females, male chimpanzees noisily tear leaf blades into pieces without eating them.

Squashing parasites on leaves While grooming another chimpanzee, an individual removes a parasite from its partner, places it on a leaf and then squashes it.

customary

Inspecting parasites Parasites removed during grooming are placed on a leaf in the chimpanzee’s palm; the animal inspects the insect, then eats or discards it.

absent

Squashing parasites with fingers Chimpanzees remove parasites from their grooming partners and place the tiny insects on their forearms. They then hit the bugs repeatedly before eating them.

absent

Clasping arms overhead Two chimpanzees clasp hands above their heads while grooming each other with the opposite hand.

absent

Knocking knuckles To attract attention during courtship, chimpanzees rap their knuckles on trees or other hard surfaces.

habitual

Rain dancing At the start of heavy rain, adult males perform charging displays accompanied by dragging branches, slapping the ground,


AUGUST 2004

The Culture Club How an international team of chimpanzee experts conducted the most comprehensive survey of the animals ever attempted

S

cientists have been investigating chimpanzee culture for several decades, but too often their studies contained a crucial flaw. Most attempts to document cultural diversity among chimpanzees have relied solely on officially published accounts of the behaviors recorded at each research site. But this approach probably overlooks a good deal of cultural variation for three reasons. First, scientists typically don’t publish an extensive list of all the activities they do not see at a particular location. Yet this is exactly what we need to know— which behaviors were and were not observed at each site. Second, many reports describe chimpanzee behaviors without saying how common they are; without this information, we can’t determine whether a particular action was a once-in-a-lifetime aberration or a routine event that should be considered part of the animals’ culture. Finally, researchers’ descriptions of potentially significant chimpanzee behaviors frequently lack sufficient detail, making it difficult for scientists working at other spots to record the presence or absence of the activities. To remedy these problems, the two of us decided to take a new approach. We asked field researchers at each site for a list of all the behaviors they suspected were local traditions. With this information in hand, we pulled together a comprehensive list of 65 candidates for cultural behaviors. Then we distributed our list to the team leaders at each site. In consultation with their colleagues, they classified each

behavior in terms of its occurrence or absence in the chimpanzee community studied. The key categories were customary behavior (occurs in most or all of the able-bodied members of at least one age or sex class, such as all adult males), habitual (less common than customary but occurs repeatedly in several individuals), present (seen at the site but not habitual), absent (never seen), and unknown. Our inquiry concentrated on seven sites with chimpanzees habituated to human onlookers; all told, the study compiled a total of more than 150 years of chimpanzee observation. The behavior patterns we were particularly interested in, of course, were those absent in at least one community, yet habitual or customary in at least one other; this was our criterion for denoting any behavior a cultural variant. (Certain behaviors are absent for specific local reasons, however, and we excluded them from consideration. For example, although chimpanzees at Bossou scoop tasty algae from pools of water with a stick, chimpanzees elsewhere don’t do this, simply because algae are not present.) The extensive survey turned up no fewer than 39 chimpanzee patterns of behavior that should be labeled as cultural variations, including numerous forms of tool use, grooming techniques and courtship gambits, several of which are illustrated throughout this article. This cultural richness is far in excess of anything known for any other species of animal. — A.W. and C.B.

eration, not through their genes but by learning. For biologists, this is the fundamental criterion for a cultural trait: it must be something that can be learned by observing the established skills of others and thus passed on to future generations [see box on page 66]. By the 1990s the discovery of new behavioral differences among chimpanzees made it feasible to begin assembling comprehensive charts of cultural variations for these animals. William C. McGrew, in his 1992 book Chimpanzee Material Cultures, was able to list 19 different kinds of tool use in distinct communities. One of us (Boesch), along with colleague Michael Tomasello of the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, identified 25 distinct activities as potential cultural traits in wild chimpanzee populations. The most recent catalogue of cultural variations results from a unique collaboration of nine chimpanzee experts (including the two of us) who pooled extensive field observations that, taken together, amounted to a total of 151 years of chimp watching [see box on opposite page]. The list cites 39 patterns of chimpanzee behavior that we

munities. In the years that followed, other primatologists set up camp elsewhere, and, despite all the financial, political and logistical problems that can beset African fieldwork, several of these outposts became truly long-term projects. As a result, we live in an unprecedented time, when an intimate and comprehensive scientific record of chimpanzees’ lives at last exists not just for one but for several communities spread across Africa. As early as 1973, Goodall recorded 13 forms of tool use as well as eight social activities that appeared to differ between the Gombe chimpanzees and chimpanzee populations elsewhere. She ventured that some variations had what she termed a cultural origin. But what exactly did Goodall mean by “culture”? According to the Oxford Encyclopedic English Dictionary, culture is defined as “the customs ... and achievements of a particular time or people.” The diversity of human cultures extends from technological variations to marriage rituals, from culinary habits to myths and legends. Animals do not have myths and legends, of course. But they do have the capacity to pass on behavioral traits from generation to gen43 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE


believe to have a cultural origin, including such activities as using sticks to “fish” for ants, making dry seats from leaves, and a range of social grooming habits. At present, these 39 variants put chimpanzees in a class of their own, with far more elaborate customs than any other animal studied to date. Of course, chimpanzees also remain distinct from humans, for whom cultural variations are simply beyond count. (We must point out, however, that scientists are only beginning to uncover the behavioral complexity that exists among chimpanzees— and so the number 39 no doubt represents a minimum of cultural traits.) Multicultural Chimpanzees

W

hen describing human customs, anthropologists and sociologists often refer to “American culture” or “Chinese culture”; these terms encompass a wide spectrum of activities— language, forms of dress, eating habits, marriage rituals and so on. Among animals, however, culture has typically been established for a single behavior, such as song dialects among birds. Ornithologists haven’t identified variation AUGUST 2004

in courtship patterns or feeding practices, for example, to go alongside the differences in dialect. Chimpanzees, though, do more than display singular cultural traits: each community exhibits an entire set of behaviors that differentiates it from other groups [see illustrations on pages 64 and 65]. As a result, we can talk about “Gombe culture” or “Taï culture.” Indeed, once we observe how a chimpanzee behaves, we can identify where the animal lives. For instance, an individual that cracks nuts, leaf-clips during drumming displays, fishes for ants with one hand using short sticks, and knuckle-knocks to attract females clearly comes from the Taï Forest. A chimp that leaf-grooms and hand-clasps during grooming can come from the Kibale Forest or the Mahale Mountains, but if you notice that he also ant-fishes, there is no doubt anymore— he comes from Mahale. In addition, chimpanzee cultures go beyond the mere presence or absence of a particular behavior. For example, all chimpanzees dispatch parasites found during grooming a companion. But at Taï they will mash the parasites against their forearms with a finger, at Gombe they squash them onto leaves, and at Budongo they put them on a leaf to inspect before eating or discarding them. Each community has developed a unique approach for accomplishing the same goal. Alternatively, behaviors may look similar yet be used in different contexts: at Mahale, males “clip” leaves noisily with their teeth as a courtship gesture, whereas at Taï, chimpanzees incorporate leaf-clipping into drumming displays. The implications of this new picture of chimpanzee culture are many. The information offers insight into our distinctiveness as a species. When we first published this work in the journal Na-

ture, we found some people quite disturbed to realize that the characteristic that had appeared to separate us so starkly from the animal world— our capacity for cultural development— is not such an absolute difference after all. But this seems a rather misdirected response. The differences between human customs and traditions, enriched and mediated by language as they are, are vast in contrast with what we see in the chimpanzee. The story of chimpanzee cultures sharpens our understanding of our uniqueness, rather than threatening it in any way that need worry us. Human achievements have made enormous cumulative progress over the generations, a phenomenon Boesch and Tomasello have dubbed the “ratchet effect.” The idea of a hammer— once simply a crude stone cobble—has been modified and improved on countless times until now we have electronically controlled robot hammers in our factories. Chimpanzees may show the beginnings of the ratchet effect— some that use stone anvils, for example, have gone a step further, as at Bossou, where they wedge a stone beneath their anvil when it needs leveling on bumpy ground— but such behavior has not become customary and is rudimentary indeed beside human advancements. The cultural capacity we share with chimpanzees also suggests an ancient ancestry for the mentality that must underlie it. Our cultural nature did not emerge out of the blue but evolved from simpler beginnings. Social learning similar to that of chimpanzees would appear capable of sustaining the earliest stone-tool cultures of human ancestors living two million years ago. Whether chimpanzees are the sole species on the planet that shares humankind’s capacity for culture is too early to judge: nobody has undertaken

the comprehensive research necessary to test the idea. Early evidence hints that other creatures should be included in these discussions, however. Carel P. van Schaik and his colleagues at Duke University have found orangutans in Sumatra that habitually use at least two different kinds of tools. Orangutans monitored for years elsewhere have never been seen to do this. And Hal Whitehead of Dalhousie University and his colleagues have begun to document the ways in which populations of whales that sing in different dialects also hunt in different ways. We hope that our comprehensive approach to documenting chimpanzee cultures may provide a template for the study of these other promising species. What of the implications for chimpanzees themselves? We must highlight the tragic loss of chimpanzees, whose populations are being decimated just when we are at last coming to appreciate these astonishing animals more completely. Populations have plummeted in the past century and continue to fall as a result of illegal trapping, logging and, most recently, the bushmeat trade. The latter is particularly alarming: logging has driven roadways into the forest that are now used to ship wild-animal meat— including chimpanzee meat— to consumers as far afield as Europe. Such destruction threatens not only the animals themselves but also a host of fascinatingly different ape cultures. Perhaps the cultural richness of the ape may yet help in its salvation, however. Some conservation efforts have already altered the attitudes of some local people. A few organizations have begun to show videotapes illustrating the cognitive prowess of chimpanzees. One Zairian viewer was heard to exclaim, “Ah, this ape is so like me, I can no longer eat him.”

The Authors

Further Information

ANDREW WHITEN and CHRISTOPHE BOESCH have collaborated since 1998 on the cross-cultural study of chimpanzees. Whiten, a fellow of the British Academy, is professor of evolutionary and developmental psychology at the University of St. Andrews in Scotland. Boesch is co-director of the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, and a professor at the University of Leipzig. The chimpanzee field-study directors participating in the research described here are Jane Goodall, Jane Goodall Institute, Washington, D.C.; William C. McGrew, Miami University; Toshisada Nishida, Kyoto University, Japan; Vernon Reynolds, University of Oxford; Yukimaru Sugiyama, Tokaigakuen University, Japan; Caroline E. G. Tutin, University of Stirling, Scotland; and Richard W. Wrangham, Harvard University.

Chimpanzee Material Culture. William C. McGrew. Cambridge University Press, 1992. Cultures in Chimpanzees. A. Whiten, J. Goodall, W. C. McGrew, T. Nishida, V. Reynolds, Y. Sugiyama, C.E.G. Tutin, R. W. Wrangham and C. Boesch in Nature, Vol. 399, pages 682–685; 1999. Chimpanzees of the Taï Forest: Behavioral Ecology and Evolution. Christophe Boesch and Hedwige Boesch-Aschermann. Oxford University Press, 2000. Primate Culture and Social Learning. Andrew Whiten in Cognitive Science. Special issue on primate cognition, Vol. 24, pages 477–508; 2000. Chimpanzee Cultures Web site: http://chimp.st-and.ac.uk/cultures/ Wild Chimpanzee Foundation Web site: http://www.wildchimps.org


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