فصل 08کتاب: آیا ما به اندازه ی کافی باهوش هستیم که بدانیم حیوانات چقدر باهوش هستند؟ / فصل 8
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8OF MIRRORS AND JARS
Pepsi was the star of a recent study on Asian elephants. The adolescent bull passed a mirror test conducted by Joshua Plotnik by carefully touching a large white X that had been painted on the left-hand side of his forehead. He never paid attention to the X that had been put with invisible paint on the right-hand side; nor did he touch the white one until he walked up to the mirror in the middle of a meadow. The next day we reversed the sides of the visible and invisible markings, and Pepsi again specifically felt the white X. He rubbed off some of the paint with the tip of his trunk and brought it to his mouth, tasting it. Since he could know its location only via his reflection, he must have connected his mirror image with himself. As if to make the point that the mark test isn’t the only way to do so, Pepsi took one step back at the end of testing to open his mouth wide. With the mirror’s help, he peered deeply inside. This move, also common in apes, makes perfect sense given that one never gets to see one’s own tongue and teeth without a mirror.1
Years later Pepsi towered over me as a nearly adult male. He was very gentle, though, lifting me up and putting me down on the orders of his mahout. Revisiting Thailand to see the camp in the Golden Triangle, where the Think Elephants International Foundation conducts its research, I met Josh’s team of enthusiastic young assistants. Every day they invite a couple of elephants to their experiments. With a mahout sitting high up on their neck, the colossal animals lumber to the testing site on the jungle’s edge. After the mahout gets off to squat in the background, the elephant performs a few simple tasks. She feels an object with her trunk, after which she is asked to pick a matching one from among several; or she stretches her trunk to smell the difference between two buckets depending on what the students put into them.2
A marked Asian elephant in front of a mirror. The mark test requires an individual to connect her reflection with her own body, resulting in inspection of the mark. Only a handful of species pass this test spontaneously.
Everyone knows that elephants are smart, but there is an enormous scarcity of data similar to those for primates, corvids, dogs, rats, dolphins, and so on. All we have for the elephant is spontaneous behavior, which doesn’t allow for the precision and controls that science desires. Discrimination tasks like the ones I witnessed are an excellent starting point. But even if the pachyderm mind may be the next frontier in evolutionary cognition, it is a most challenging one given that the elephant is probably the only land animal never to be seen alive on a university campus or in a conventional lab. While science’s preference for easy-to-keep species is understandable, it has its limits. It has given us a small-brain perspective on animal cognition, one that we have had trouble shedding.
Southeast Asians have a long-standing cultural relation with elephants. For thousands of years, these animals have carried out heavy forest work, transported royalty, and served in hunting and warfare. They have always remained wild, though. The species is not domesticated in the genetic sense, and free-ranging elephants still often sire the offspring of captive ones. Not surprisingly, elephants are less predictable than many domesticated animals. They can be hostile to people, occasionally killing a mahout or tourist, but many of them also form lifelong bonds with their caretakers. In one story, an elephant at the age of ten pulled her drowning mahout out of a lake after hearing his cries for help a kilometer away; in another, a fully grown bull would charge anyone who came close except the wife of the village elder, whom he would caress with his trunk. Young elephants grow so used to people that they learn how to fool them by stuffing a trunkful of grass into the wooden bells around their necks so as to muffle their sound. This way they can move about unnoticed.
African elephants, in contrast, are rarely brought under human control. They live their own parallel lives, even though the massive ivory trade is now putting them in danger to the point that we face the dismaying prospect of permanently losing one of the world’s most beloved and charismatic animals. The elephant’s Umwelt being largely acoustic and olfactory, the protection of wild populations against poaching and conflict with humans requires methods that are not immediately obvious to our visual species. Studies focus on the extraordinary senses of these animals. One study, in arid Namibia, followed free-ranging elephants equipped with GPS collars. It discovered that these animals are aware of thunderstorms at enormous distances and adjust their travel routes to precipitation days before it actually arrives. How do they do this? Elephants can hear infrasound, which are sound waves far below the human hearing range. Also used in communication, these sounds travel over much longer distances than the ones we are able to discern.3 Is it possible that elephants can hear thunder and rainfall hundreds of miles away? It seems the only way to explain their behavior.
But isn’t this just a matter of perception? Cognition and perception cannot be separated, though. They go hand in hand. As the father of cognitive psychology, Ulric Neisser, put it: “the world of experience is produced by the man who experiences it.”4 Since the late Neisser was a colleague of mine, I know that nonhuman minds were not his foremost interest, yet he refused to view animals as mere learning machines. The behaviorist program was ill suited to all species, he felt, not just ours. Instead, he emphasized perception and how it is turned into experience by picking and choosing what sensory input to pay attention to and how to process and organize it. Reality is a mental construct. This is what makes the elephant, the bat, the dolphin, the octopus, and the star-nosed mole so intriguing. They have senses that we either don’t have, or that we have in a much less developed form, making the way they relate to their environment impossible for us to fathom. They construct their own realities. We may attach less significance to these, simply because they are so alien, but they are obviously all-important to these animals. Even when they process information familiar to us, they may do so quite differently, such as when elephants tell human languages apart. This ability was first demonstrated in African elephants.
In Amboseli National Park, in Kenya, the British ethologist Karen McComb studied elephant reactions to different human ethnic groups. The cattle-herding Maasai sometimes spear elephants in order to show their virility or to gain access to grazing grounds and water holes. Understandably, elephants flee the Maasai, who approach them in their characteristic red ochre robes, but they don’t avoid other people on foot.5 How do they recognize the Maasai? Instead of focusing on their color vision, McComb explored what is perhaps the elephant’s keenest sense: sound. She contrasted the Maasai with the Kamba people, who live in the same area but rarely interfere with elephants. From a concealed loudspeaker, McComb played human voices saying a single phrase in the language of either the Maasai or the Kamba: “Look, look over there, a group of elephants is coming.” It is hard to imagine that the precise words mattered, but the investigators compared the elephants’ reaction to the voices of adult men, adult women, and boys.
Herds retreated and “bunched” together (forming a tight circle with calves in the middle) more often after playbacks of Maasai than of Kamba voices. Maasai male voices triggered more defensive reactions than those of Maasai women and boys. Even after the natural voices were acoustically transformed so as to make male voices sound more female, and vice versa, the outcome remained the same. The elephants were especially vigilant upon hearing the resynthesized voices of Maasai men. This was surprising because the pitch of these voices had now the opposite gender’s qualities. Possibly the elephants identified gender by other characteristics, such as the fact that female voices tend to be more melodious and “breathy” than those of males.6
Experience played a role, because herds led by older matriarchs were more discriminating. The same difference was found in another study in which lion roaring was played from a speaker. Older matriarchs would charge the speaker, which is quite different from their hasty retreat from Maasai voices.7 Aggressive mobbing of men carrying spears is unlikely to pay off, yet driving off lions is something elephants are good at. Despite their size, these animals face other dangers, including very small ones, such as stinging bees. Elephants are vulnerable to stings around the eyes and up their trunks, and young elephants lack a thick enough skin to protect themselves against a mass attack. Elephants give deep rumbles as an alarm to both humans and bees, but the two sounds must differ because playbacks induce quite different responses. Upon hearing the bee-rumble from a speaker, for example, elephants flee with head-shaking movements that would knock insects away, a reaction not shown to the human-rumble.8
In short, elephants make sophisticated distinctions regarding potential enemies to the point that they classify our own species based on language, age, and gender. How they do so is not entirely clear, but studies like these are beginning to scratch the surface of one of the most enigmatic minds on the planet.
The Magpie in the Mirror
The ability to recognize oneself in the mirror is often viewed in absolute terms. According to Gallup, the pioneer of this field, a species either passes the mirror mark test and is self-aware, or it doesn’t and isn’t.9 Very few species do. For the longest time, only humans and the great apes passed, and not even all those. Gorillas used to flunk the mark test, leading to theories about why the poor things might have lost their self-awareness.10
Evolutionary science, however, is uncomfortable with black-and-white distinctions. It is hard to imagine that among any set of related species, some are self-aware whereas others, for lack of a better term, remain unaware. Every animal needs to set its body apart from its surroundings and to have a sense of agency (awareness that it controls its own actions).11 You wouldn’t want to be a monkey up in a tree without awareness of how your own body will impact a lower branch on which you intend to land. And you wouldn’t want to engage in rough-and-tumble play with a fellow monkey, with all your combined arms, legs, and tails intertwined, while stupidly gnawing on your own foot or tail! Monkeys never make this mistake and gnaw exclusively on their partner’s foot or tail in such a tangle. They have a well-developed body ownership and self-other distinction.
In fact, experiments on the sense of agency show that species without mirror self-recognition are very well capable of distinguishing their own actions from those produced by others. Tested in front of a computer screen, they have no trouble telling the difference between a cursor that they themselves control with a joystick and a cursor that moves by itself.12 Self-agency is part of every action that an animal—any animal—undertakes. In addition, some species may possess their own unusual kind of self-recognition, such as bats and dolphins that pick out the echoes of their own vocalizations from among the sounds made by others.
Cognitive psychology doesn’t like absolute differences either, but for a different reason. The problem with the mirror test was that it introduced the wrong absolute difference. Instead of sharply dividing humans from all other animals—which, as we have seen, is a staple of the field—Gallup’s mirror test moved the Rubicon slightly to annex a few more species. Lumping humans in with the apes so as to elevate the Hominoids, as a group, to a different mental level than the rest of the animal kingdom, didn’t go over well. It diluted humanity’s special status. Still today, claims about self-awareness outside our own species cause consternation, and debates about mirror responses turn acrimonious. Moreover, many specialists have felt the need to conduct mirror tests on the animals in their care, usually with disappointing results. These debates have led me to the sarcastic conclusion that mirror self-recognition is considered a big deal only by scientists working on the handful of species capable of it, whereas all others poo-poo the phenomenon.
Since I study animals that both do and don’t recognize themselves in the mirror, and have a high opinion of them all, I feel torn. I do think that spontaneous self-recognition means something. It may signal a stronger self-identity, such as is also reflected in perspective taking and targeted helping. These capacities are most marked in animals that pass the mirror test as well as in children who have reached the age, around two, when they do. This is also the age when they can’t stop referring to themselves, as in “Mama, look at me!” Their sharpened self-other distinction is said to help them adopt another’s viewpoint.13 Still, I can’t believe that a sense of self is absent either in other species or in younger children. Rather obviously, animals that fail to link their mirror image to their own body vary greatly in what they understand. Small songbirds and fighting fish, for example, never get over their mirror image and keep courting or attacking it. During the spring, when they are most territorial, tits and bluebirds will respond this way to the sideview mirror of a car and stop their hostilities only when the car drives off. This is absolutely not what monkeys do, nor many other animals. We would not be able to have mirrors in our homes if cats and dogs reacted the same way. These animals may not recognize themselves, but they are also not totally baffled by the mirror, at least not for long. They learn to ignore their reflection.
Some species go further in that they understand mirror basics. Monkeys, for example, may not recognize themselves but are able to use the mirror as a tool. If you hide food that can be found only by using a mirror to look around a corner, the monkey will have no trouble reaching for it. Many a dog can do the same: holding up a cookie behind them while they watch you in a mirror makes them turn around. Curiously, it is specifically the relation with their own body, their own self in the mirror, that they fail to grasp. But even then, rhesus monkeys can be taught to do so. It requires adding a physical sensation. They need a mark that they can both see in the mirror and feel on their body, such as a laser light that irritates the skin or a cap fastened to their head. Instead of a traditional mark test, this is better described as a felt mark test. Only under these circumstances can monkeys learn to connect their reflection with their own body.14 This is obviously not the same as what apes do spontaneously relying on vision alone, but it does suggest that some of the underlying cognition is shared.
Even though capuchin monkeys fail the visual mark test, we decided to study them in a way that, surprisingly, no one had ever tried before. Our goal was to see if these monkeys truly mistake their reflection for a “stranger,” as is commonly implied. Capuchins were placed in front of a Plexiglas panel, behind which they faced either a member of their own group, a stranger of their species, or a mirror. It quickly became evident that the mirror was special. They treated their reflection quite differently from a real monkey. They didn’t need any time to decide what they saw, and reacted within seconds. They turned their backs to strangers, barely glancing at them, yet made prolonged eye contact with their own reflections as if thrilled to see themselves. They showed absolutely none of the timidity toward the mirror image that one would expect if they mistook it for a stranger. Mothers, for example, let their infants freely play in front of the mirror yet held them close in case of a stranger. But the monkeys also never inspected themselves in the mirror, the way apes do all the time, or the way Pepsi the elephant had done. They never opened their mouth to peek inside. Thus, while capuchins fail to recognize themselves, they also don’t mix up their reflection with someone else.
As a result, I have become a gradualist.15 There are many stages of mirror understanding, running all the way from utter confusion to a full appreciation of the specular image. These stages are also recognizable in human infants, which are curious about their mirror image well before passing the mark test. Self-awareness develops like an onion, building layer upon layer, rather than appearing out of the blue at a given age.16 For this reason, we should stop looking at the mark test as the litmus test of self-awareness. It is only one of many ways to find out about the conscious self.
Nevertheless, it remains fascinating how few species pass this test without a helping hand. After the Hominoids, spontaneous self-recognition was observed only in elephants and dolphins. When bottlenose dolphins at the New York Aquarium were marked by Diana Reiss and Lori Marino with painted dots, they would race from the spot where the marking took place to a mirror in another pool, at quite a distance, only to spin around seemingly to get a good look at themselves. The dolphins spent more time near the mirror checking out their bodies when they had been marked than without a visible mark.17
It was unavoidable that the mirror test would be tried on birds. While most species have thus far failed, we have one exception: the Eurasian magpie. It is an interesting species to put in front of a reflective surface. As a child, I learned never to leave small shiny objects, such as teaspoons, unattended outdoors as these raucous birds will steal anything they can put their beaks on. This folklore inspired a Rossini opera, La gazza ladra (The Thieving Magpie). Nowadays, this view has been replaced with a more ecologically sensitive one that depicts magpies as murderous robbers of the nests of innocent songbirds. Either way, they are considered black-and-white gangsters.
But no one has ever accused a magpie of being stupid. The bird belongs to the corvid family that has begun to challenge the cognitive supremacy of primates. The German psychologist Helmut Prior subjected magpies to a mirror test that was at least as well controlled as any conducted on apes and children. Placed on their black bib (throat feathers), the mark—a tiny yellow sticker—stood out but was visible only with help of the mirror. The birds were untrained, which is a critical difference with the highly coached pigeons employed long ago to discredit mirror research. Put in front of a mirror, the magpies kept scratching with their foot until the mark was gone. They never did the same amount of frantic scratching if there was no mirror to see themselves in, and they ignored a “sham” mark—a black sticker on their black bib. As a result, the self-recognition elite has now been expanded with its first feathered member. Others may follow.18
The next frontier will be to see if animals care about their mirror image to the point of embellishing themselves, the way we do with makeup, hair care, earrings, and the like. Does the mirror induce vanity? Would any species other than ours be prone to take selfies, if they could? This possibility was first hinted at by observations in the 1970s of a female orangutan at the Osnabrück Zoo, in Germany. Jürgen Lethmate and Gerti Dücker described Suma’s narcissistic ways:
Suma, an orangutan at a German zoo, loved to decorate herself in front of the mirror. Here she puts a leaf of lettuce onto her head like a hat.
She gathered salad and cabbage leaves, shook each leaf and piled them up. Eventually, she placed one leaf on her head and walked straight to the mirror with it. She sat down directly in front of it, contemplated her headcover in the mirror, straightened it a bit with her hand, squashed it with a fist, then put the leaf on her forehead and began to bob up and down. Later, Suma arrived holding a salad leaf in her hand at the bars [where the mirror stood] to lay it on her head once she could see herself in the mirror.19
The Mollusk Mind
As a biology student, my favorite textbook was Animals Without Backbones. It may seem an odd choice given my current interests, but I was awestruck by all the exotic life-forms that I had never heard about or could scarcely imagine, some of them so tiny that you needed a microscope to see them. The book went into great detail of all invertebrates—from protozoans and sponges to worms, mollusks, and insects—which together make up 97 percent of the animal kingdom.20 Whereas cognition research focuses almost entirely on the tiny vertebrate minority, it is not as if the rest doesn’t move, eat, mate, fight, and cooperate. Obviously, some invertebrates show more complex behavior than others, but they all need to pay attention to their surroundings and solve problems that present themselves. In the same way that almost all these animals have reproductive organs and digestive tracts, they can’t survive without a degree of cognition.
The brainiest of the bunch is the octopus, which is a soft-bodied cephalopod, or “head-footed” animal. This is an apt name, since their squishy bodies consist of a head that directly joins eight limbs, while the body (the mantle) is positioned behind the head. The cephalopods are an ancient class that arose well before there were land vertebrates around, but the group to which the octopus belongs is a fairly modern offshoot. We seem to have almost nothing in common with them, both anatomically and mentally. Yet they have been reported to open a pill bottle protected by a childproof cap. Since this requires the cap to be pushed down and twisted at the same time, it takes skill, intelligence, and persistence. Some public aquariums show off octopus intelligence by locking the animal in a glass jar that they close with a screw top. Like a true Houdini, the octopus takes less than a minute to grab the cover from within with its suckers and unscrew it so as to escape.
The octopus has a most remarkable nervous system that allows it to solve challenging problems, such as how to escape from a glass jar closed with a screw top.
However, when octopuses were given a transparent jar that contained a live crayfish, they failed to do anything. This greatly puzzled the scientists, because the delicacy was clearly visible and moving about. Do octopuses perhaps have trouble unscrewing a lid from the outside? It turned out to be one of those human misjudgments. Despite having excellent eyes, octopuses rarely rely on vision to catch prey. They use mainly touch and chemical information and fail to recognize prey without those cues. As soon as the jar was smeared on the outside with herring “slime,” making it taste like fish, the octopus swung into action and started manipulating it until the top came off. It quickly removed the crayfish and ate it. With further skill development, the process became routine.21
In captivity, octopuses react to us in ways that we find hard not to anthropomorphize. One octopus was fond of raw chicken eggs—each day it would accept an egg and break it to suck out its contents. One day, however, this octopus accidentally received a rotten egg. Upon noticing, it shot the egg’s smelly remains over the edge of its tank back at the surprised human from whom it had received it.22 Given how well they distinguish people, octopuses probably remember encounters like these. In a recognition test, an octopus was exposed to two different persons, one of whom consistently fed it, whereas the other mildly poked it with a bristle on a stick. Initially, the animal made no distinction, but after several days it began doing so despite the fact that both humans wore identical blue overalls. Seeing the loathsome person, the octopus would withdraw, emit jets of water with its funnel, and show a dark bar through its eyes—a color change associated with threat and irritation. It would approach the nice person, on the other hand, without making any attempt at drenching her.23
The octopus brain is the largest and most complex of all invertebrates, but the explanation of its extraordinary skills may lie elsewhere. These animals literally think outside the box. Each octopus has nearly two thousand suckers, every single one equipped with its own ganglion with half a million neurons. That amounts to a lot of neurons on top of a 65-million-neuron brain. In addition, it has a chain of ganglia along its arms. The brain connects with all these “mini brains,” which are also joined among themselves. Instead of a single central command, as in our species, the cephalopod nervous system is more like the Internet: there is extensive local control. A severed arm may crawl on its own and even pick up food. Similarly, a shrimp or small crab can be handed from one sucker to the next, as if on a conveyer belt, in the direction of the octopus’s mouth. When these animals change skin color in self-defense, the decision may come from central command, but perhaps the skin is involved as well, since cephalopod skin may detect light. It sounds rather unbelievable: an organism with seeing skin and eight independently thinking arms!24
This realization has led to a bit of hype: that the octopus is the most intelligent organism in the ocean, a sentient being that we should stop eating. We shouldn’t overlook dolphins and orcas, though, which have vastly larger brains. Even if the octopus stands out among invertebrates, its tool use is rather limited, and its reaction to a mirror is as perplexed as that of a small songbird. It remains unclear whether an octopus is smarter than most fish, but let me hasten to add that such comparisons barely make any sense. Instead of turning the study of cognition into a contest, we should avoid putting apples next to oranges. The octopus’s senses and anatomy, including its decentralized nervous system, make it unparalleled.
If superlatives of uniqueness were allowed, the octopus might be the most unique species of them all. They defy comparison with any other group, unlike our own species, which derives from a long line of land vertebrates with structurally similar body plans and brains.
Octopuses have an odd life cycle. Most live only one or two years, which is unusual for an animal with their brainpower. They grow fast while trying to stay away from predators until they have a chance to mate and reproduce, after which they die. They stop eating, lose weight, and go into senescence.25 This is the stage about which Aristotle observed: “after giving birth … [they] become stupid, and are not aware of being tossed about in the water, but it is easy to dive and catch them by hand.”26
These short-lived loners have no social organization to speak of. Given their biology, they have no reason to pay attention to one another, except as rivals, mates, predators, and prey. They are certainly not friends or partners. There is no evidence that they learn from others or spread behavioral traditions, the way many vertebrates, including fish, do. The absence of social bonds and cooperation, and their cannibalistic ways, make cephalopods quite alien to us.
Their main worry is predation, because apart from their own kind, they are eaten by almost everything around, from marine mammals, diving birds, sharks, and other fish to humans. When they get larger, they become formidable predators themselves, as the Seattle Aquarium accidentally found out. Worried about their giant Pacific octopus in a tank full of sharks, staff were hoping that the animal would know how to hide. But then they noticed one dogfish (a small shark) after another disappearing from the tank—and found to their astonishment that the octopus had turned the tables. The octopus may be the only playful invertebrate. I say may since play behavior is almost impossible to define, but the octopus appears to go beyond mere manipulation and checking out of novel objects. The Canadian biologist Jennifer Mather found that given a new toy, the animal will move from exploration (“What is this?”) to repeated lively movements and tossing around (“What can I do with it?”). With their funnel, they blow jets of water at a floating plastic bottle, for example, to move it from one side of their tank to another, or to have it tossed back at them by the water flow of the filter, which makes them look as if they were bouncing a ball. Such manipulations, which serve no obvious purpose and are repeated over and over, have been taken as indications of play.27
Tied to the immense predation pressure under which these animals live is their ability for camouflage. Perhaps their most astonishing specialization, it provides an inexhaustible “magic well” for those who study them. The octopus changes color so rapidly that it out-chameleons the chameleon. Roger Hanlon, a scientist at the Marine Biological Laboratory in Woods Hole, Massachusetts, has collected rare underwater footage of octopuses in action. All we see at first is a clump of algae on a rock, but hidden among it is a large octopus indistinguishable from its surroundings. When the approaching human diver scares the animal, it turns almost white, revealing that it represented almost half the clump of algae. It speeds away while shooting a dark cloud of ink, which is its secondary defense. The animal then lands on the sea floor and makes itself look huge by spreading all its arms and stretching the skin between them into a tent. This frightening expansion is its tertiary defense.
When this video clip is slowed down and played backward, it is easy to see how superb the original camouflage was. Both structurally and color-wise, the large octopus had made itself look exactly like an algae-covered rock. It did so by making its chromatophores (millions of neurally controlled pigment sacs in its skin) match their surroundings. But instead of exactly mimicking its background, which is impossible, it did so just well enough to fool our visual system. And it probably did more than that, since the octopus also takes other visual systems into account. Humans see no polarized or ultraviolet light and don’t have great night vision, whereas the octopus’s camouflage needs to trick all these visual capacities. In doing so, it draws on a limited set of patterns that it has in stand-by mode. Turning on one of these “blueprint” patterns allows it to blend in in a fraction of a second. The result is an optical illusion, but one realistic enough to save its life hundreds of times.28
Sometimes an octopus mimics an inanimate object, such as a rock or plant, while moving so slowly that one would swear it is not moving at all. It does so when it needs to cross an open space, an activity that exposes it to detection. Imitating a plant, the octopus waves some of its arms above itself, making them look like branches, while tiptoeing on three or four of its remaining arms. It takes tiny little steps in line with the water movements. If the ocean is wild, plants sway back and forth, which helps the octopus disguise its steps by swaying in the same rhythm. On a waveless day, on the other hand, nothing else moves, so the octopus needs to be extremely careful. It may take twenty minutes to cross a stretch of sea floor that it otherwise might have crossed in twenty seconds. The animal acts as if rooted to the spot, counting on the fact that no predator will take the time to notice that it is actually inching forward.29
The champion of camouflage, finally, is the mimic octopus, a species found off the coast of Indonesia that impersonates other species. It acts like a flounder by adopting this fish’s body shape and color as well as its typical undulating swimming pattern close to the sea floor. The repertoire of this octopus includes adopting the likeness of a dozen local marine organisms, such as lionfish, sea snakes, and jellyfish.
We don’t know exactly how octopuses achieve this astonishing range of mimicry. Some of it may be automated, but there is probably also learning involved based on observations of other creatures and adoption of their habits. As primates, we find it impossible to relate to these remarkable capacities, and we may hesitate to call them cognitive. We tend to view invertebrates as instinct machines, arriving at solutions through inborn behavior. But this position has become untenable. There are too many remarkable observations—including the deceptive tactics of cuttlefish, close relatives of the octopus.
Male cuttlefish courting a female may trick rival males into thinking there is nothing to worry about. The courting male adopts the coloring of a female on the side of his body that faces his rival, so that the latter believes he is looking at a female. But the same male keeps his original coloring on the female’s side of his body in order to keep her interested. He thus courts her surreptitiously. This two-faced tactic, called dual-gender signaling, suggests tactical skills of an order that we might expect in primates but not mollusks.30 Hanlon rightly claims that cephalopod truth is stranger than fiction.
Invertebrates will probably continue to challenge students of evolutionary cognition. Being anatomically quite different yet facing many of the same survival problems as the vertebrates, they offer fertile grounds for convergent cognitive evolution. Among the arthropods, for example, we find jumping spiders known to trick other spiders into thinking that their web contains a struggling insect. When the web-owner hurries over for the kill, she herself becomes the prey. Instead of knowing at birth how to enact a trapped insect, jumping spiders seem to learn how to do so by trial and error. They try out a kaleidoscope of random pluckings and vibrations on the silk of another spider, using their palps and legs, while taking note which signals best lure the owner toward them. The most effective signals will be repeated on future occasions. This tactic allows them to fine-tune their mimicry to any victim species, which is why arachnologists have begun to speak of spider cognition.31
And why not?
When in Rome
To our surprise, chimps turn out to be conformists. Copying others for one’s own benefit is one thing, but wanting to act like everybody else is quite another. It is the foundation of human culture. We discovered this tendency when Vicky Horner presented two separate groups of chimpanzees with an apparatus from which food could be extracted in two different ways. The apes could either poke a stick into a hole to release a grape or use the same stick to lift up a little trap and a grape would roll out. They learned the technique from a model: a pretrained group member. One group saw a lifting model, the other a poking model. Even though we used the same apparatus for both groups, moving it back and forth between them, the first learned to lift, and the second to poke. Vicky had created two distinct cultures, dubbed the “lifters” and the “pokers.”32
There were exceptions, though. A few individuals discovered both techniques or used a different one than their model had demonstrated. When we retested the chimps two months later, though, most of the exceptions had vanished. It was as if all the apes had settled on a group norm, following the rule “Do what everyone else is doing regardless of what you found out by yourself.” Since we never noticed any peer pressure nor any advantage of one technique over the other, we attributed this uniformity to a conformist bias. Such a bias obviously fits my ideas about imitation guided by a sense of belonging as well as what we know about human behavior. Members of our own species are the ultimate conformists, going so far as abandoning their personal beliefs if they collide with the majority view. Our openness to suggestion goes well beyond what we found in the chimps, yet it seems related. This is why the conformist label stuck.33
It is increasingly applied to primate culture, such as by Susan Perry in her fieldwork on capuchin monkeys. Perry’s monkeys have two equally efficient ways of shaking the seeds out of the Luehea fruits that they encounter in the Costa Rican jungle. They can either pound the fruits or rub them on a tree branch. Capuchins are the most vigorous and enthusiastic foragers I know, and most adults develop one technique or the other but not both. Perry found conformism in daughters, who adopted the preferred method of their mothers, but not in sons.34 This sex difference, also known of juvenile chimpanzees learning to fish for termites with twigs, makes sense if social learning is driven by identification with the model. Mothers act as role models for daughters but not necessarily for sons.35
Conformism is hard to substantiate in the field. There are too many alternative explanations for why one individual might act like another, including genetic and ecological ones. How these issues can be resolved was shown by a large-scale project on humpback whales in the Gulf of Maine in the northeastern United States. In addition to their regular bubble-feeding, in which whales drive fish together with air bubbles, one male invented a new technique. First seen in 1980, this whale would whack the ocean surface with his fluke to produce a loud noise that clumped the prey even more. Over time this lobtail technique became increasingly common in the population. In the course of a quarter-century, investigators carefully plotted how it spread across six hundred individually recognized whales. They found that whales who had associated with those employing the technique were more likely to use it themselves. Kinship could be ruled out as a factor, because whether a whale had a lobtail-feeding mother hardly mattered. It all boiled down to whom they had encountered while feeding on fish. Since large cetaceans are unsuitable for experiments, this may be as close as we will ever get to proving that a habit spread socially as opposed to genetically.36
On wild primates, experimental work is rare for different reasons. First of all, these animals are neophobic, and rightly so, because imagine the danger of freely approaching human contraptions, including those set by poachers. Second, fieldworkers generally hate to expose their animals to artificial situations, since their goal is to study them with as little disturbance as possible. Third, they have no control over who participates in an experiment and for how long, thus precluding the kind of tests typically applied to animals in captivity.
So one has to admire one of the most elegant experiments on conformism on wild monkeys, carried out by the Dutch primatologist Erica van de Waal (no relation).37 Teaming up with Andy Whiten, who has been an engine of cultural studies, van de Waal gave vervet monkeys in a South African game reserve open plastic boxes filled with maize corn. These small grayish monkeys with black faces love corn, but there was a catch: the scientists had manipulated the supply. There were always two boxes with two colors of corn, blue and pink. One color was good to eat whereas the other was laced with aloe, making it disgusting. Depending on which color corn was palatable, and which not, some groups learned to eat blue, and others pink.
This preference is easily explained by associative learning. But then the investigators removed the distasteful treatment and waited for infants to be born and new males to immigrate from neighboring areas. They watched several groups of monkeys that were supplied with perfectly fine corn of both colors. All adults stubbornly stuck to their acquired preference, however, and never discovered the improved taste of the alternative color. Twenty-six of twenty-seven newborn infants learned to eat only the locally preferred food. Like their mothers, they didn’t touch the other color, even though it was freely available and just as good as the other. Individual exploration was obviously suppressed. The youngsters might even sit on top of the box with the rejected corn while happily feeding on the other type. The single exception was an infant whose mother was so low in rank, and so hungry, that she occasionally tasted the forbidden fruits. Thus, all newborns copied their mothers’ feeding habits. Male immigrants, too, ended up adopting the local color even if they arrived from groups with the opposite preference. That they switched their preference strongly suggests conformism, since these males knew from experience that the other color was perfectly edible. They simply followed the adage “When in Rome …”
These studies prove the immense power of imitation and conformism. It is not a mere extravagance that animals occasionally engage in for trivial reasons—which, I hate to say, is how animal traditions have sometimes been derided—but a widespread practice with great survival value. Infants who follow their mother’s example of what to eat and what to avoid obviously stand a better chance in life than infants who try to figure out everything on their own. The idea of conformism among animals is increasingly supported for social behavior as well. One study tested both children and chimpanzees on generosity. The goal was to see if they were prepared to do a member of their own species a favor at no cost to themselves. They indeed did so, and their willingness increased if they themselves had received generosity from others—any others, not just their testing partner. Is kind behavior contagious? Love begets love, we say, or as the investigators put it more dryly, primates tend to adopt the most commonly perceived responses in the population.38
The same can be concluded from an experiment in which we mixed two different macaques: rhesus and stumptail monkeys. Juveniles of both species were placed together, day and night, for five months. These macaques have strikingly different temperaments: rhesus are a quarrelsome, nonconciliatory bunch, whereas stumptails are laid-back and pacific. I sometimes jokingly call them the New Yorkers and Californians of the macaque world. After a long period of exposure, the rhesus monkeys developed peacemaking skills on a par with those of their more tolerant counterparts. Even after separation from the stumptails, the rhesus showed nearly four times more friendly reunions following fights than is typical of their species. These new and improved rhesus monkeys confirmed the power of conformism.39
One of the most intriguing sides of social learning—defined as learning from others—is the secondary role of reward. While individual learning is driven by immediate incentives, such as a rat learning to press a lever to obtain food pellets, social learning doesn’t work this way. Sometimes conformism even reduces rewards—after all, the vervet monkeys missed out on half of the available food. We once conducted an experiment in which capuchin monkeys watched a monkey model open one of three differently colored boxes. Sometimes the boxes contained food, but at other times they were empty. It didn’t matter: the monkeys copied the model’s choices regardless of whether there was any reward.40
There are even examples of social learning in which the benefits, instead of going to the performer, go to someone else. At the Mahale Mountains in Tanzania, I regularly saw a chimpanzee walk up to another, vigorously scratch the other’s back with his or her fingernails, then settle down to groom the other. In between the grooming, more scratching might follow. This behavior has been known for a long time and has thus far been reported for only one other field site. It is a locally learned tradition, but here’s the rub: when one scratches oneself, it is usually due to itching, and the act brings instant relief. In the case of the social scratch, however, the performer does not feel relief—the recipient does.41
Primates occasionally learn habits from others that do pay off, such as when chimpanzee youngsters learn to crack nuts with stones. But even then things are not as simple as they appear. Sitting next to their nut-cracking moms, infant chimps are total klutzes. They put nuts on top of stones, stones on top of nuts, and push them all together in a heap only to rearrange them over and over. They gain nothing from this playful activity. They also hit nuts with a hand, or stamp them hard with a foot, which fails to crack anything. Palm and panda nuts are far too tough for them. Only after three years of futile efforts do young chimps have enough coordination and strength to break open their first nut with a pair of stones, but they still have to wait until they are six or seven to reach adult skill levels.42 Since they utterly fail at this task for so many years in a row, it is unlikely that food is the incentive. They may even experience negative consequences, such as smashed fingers. Yet young chimps happily persist, inspired by the example of their elders.
How little rewards matter is also evident from habits that lack benefits. In our own species, we have fads such as wearing a baseball cap backward or pants that hang low enough to impede locomotion. But in other primates, too, we find seemingly useless fashions and habits. A nice example is the N-family in a group of rhesus monkeys that I observed long ago at the Wisconsin Primate Center. This matriline was headed by an aging matriarch, Nose, all of whose offspring had names starting with the same letter, such as Nuts, Noodle, Napkin, Nina, and so on. Nose had developed the odd routine of drinking from a water basin by dipping her entire underarm into it, then licking her hand and the hair on her arm. Amusingly, all her offspring, and later her grandchildren adopted the exact same technique. No other monkeys in the troop, or any other that I knew, drank like this, yet there was absolutely no advantage to it. It did not allow the N-family to access anything that other monkeys had no access to.
Or take the way chimpanzees sometimes develop local dialects, such as the excited grunts uttered while snacking on tasty food. These grunts differ not only from group to group but also per food type, such as a particular grunt heard only while they eat apples. When the Edinburgh Zoo introduced chimpanzees from a Dutch zoo to its residents, it took those others three years to get socially integrated. Initially, the newcomers uttered different grunts while eating apples, but by the end they converged on the same grunts as the locals. They had adjusted their calls so that they sounded more like those of the residents. While the media hyped this finding by saying that Dutch chimps had learned to speak Scottish, it was more like picking up an accent. The bonding between individuals of different backgrounds had resulted in conformism, even though chimps are not particularly known for vocal flexibility.43
Clearly, social learning is more about fitting in and acting like others than about rewards. This is why my book on animal culture was entitled The Ape and the Sushi Master. I chose this title partly to honor Imanishi and the Japanese scientists who gave us the animal culture concept, but also because of a story I had heard about how apprentice sushi masters learn their trade. The apprentice slaves in the shadow of the master of an art requiring rice of the right stickiness, precisely cut ingredients, and the eye-catching arrangements for which Japanese cuisine is famous. Anyone who has ever tried to cook rice, mix it with vinegar, and cool it off with a handheld fan so as to mold fresh rice balls in one’s hands knows how complex a skill it is, and it is only a small part of the job. The apprentice learns mostly through passive observation. He washes the dishes, mops the floor, bows to the clients, fetches ingredients, and in the meantime follows from the corners of his eyes, without ever asking a question, everything the sushi master does. For three years he watches without being allowed to make actual sushi for the patrons of the restaurant: an extreme case of exposure without practice. He is waiting for the day when he will be invited to make his first sushi, which he will do with remarkable dexterity.
Whatever the truth about the sushi master’s education, the point is that repeated observation of a skilled model firmly plants action sequences in one’s head that come in handy, sometimes much later, when one needs to carry out the same task. Tetsuro Matsuzawa, who studied nut-cracking in West African chimpanzees, views social learning as based on a devoted master-apprentice relationship, in the same way that I developed my Bonding- and Identification-based Observational Learning model (BIOL).44 Both views reject the traditional focus on incentives and replace it with one on social connections. Animals strive to act like others, especially others whom they trust and feel close to. Conformist biases shape society by promoting the absorption of habits and knowledge accumulated by previous generations. This by itself is obviously advantageous—and not just in the primates—so even though conformism is not driven by immediate benefits, it likely assists survival.
What’s in a Name?
Konrad Lorenz was a big corvid fan. He always kept jackdaws, crows, and ravens around his house in Altenberg, near Vienna, and considered them the birds with the highest mental development. In the same way that I, as a student, took walks with my tame jackdaws flying above me, he traveled with Roah, his old raven and “close friend.” And like my jackdaws, the raven would come down from the sky and try to make Lorenz follow by moving his tail sideways before him. It is a quick gesture that is not easily noticed from a distance yet hard to miss if done right in front of your face. Curiously, Roah used his own name to call Lorenz, whereas ravens normally call one another with a sonorous, deep-throated call-note described by Lorenz as a metallic “krackkrackkrack.” Here is what he said about Roah’s invitations:
Roah bore down on me from behind, and, flying close over my head, he wobbled with his tail and then swept upwards again, at the same time looking backwards over his shoulder to see if I was following. In accompaniment of this sequence of movements Roah, instead of uttering the above described call-note, said his own name, with human intonation. The most peculiar thing about this was that Roah used the human word for me only. When addressing one of his own species, he employed the normal innate call-note.45
Lorenz denied that he had taught his raven to call like this—after all, he had never rewarded him for it. He suspected that Roah must have inferred that since “Roah!” was the call-note Lorenz used for him, it might also work in reverse. This sort of behavior may appear in animals that contact one another vocally and are moreover great imitators. As we shall see, this also holds for dolphins. In the primates, on the other hand, individual identity is usually visually determined. The face is the most characteristic part of the body; hence face recognition is highly developed and has been demonstrated in multiple ways in both monkeys and apes.
It is not just faces that they pay attention to, however. During our studies, we discovered how intimate chimps are with one another’s derrières. In one experiment, they first saw a picture of the behind of one of their group mates followed by two facial pictures. Only one of both faces belonged to the behind, however. Which one would they select on the touchscreen? It was a typical matching-to-sample task of the type invented by Nadia Kohts before the computer age. We found that our apes selected the correct portrait, the one that went with the butt they had seen. They were only successful, though, with chimps that they knew personally. That they failed with pictures of strangers suggests that it was not based on something in the pictures themselves, such as color or size. They must possess a whole-body image of familiar individuals, knowing them so well that they can connect any part of their body with any other part.
In the same way, we are able to locate friends and relatives in a crowd even if we only see their backs. Having published our findings under the suggestive title “Faces and Behinds,” everyone thought it was funny that apes could do this, and we received an IgNobel prize for the study. This parody of the Nobel Prize honors research that “first makes people laugh, and then think.”46
I do hope it makes people think, because individual recognition is the cornerstone of any complex society.47 That animals have this capacity is often underestimated by humans, for whom all members of a given species look alike. Among themselves, however, animals generally have no trouble telling one another apart. Take dolphins, which for us are hard to identify because they all seem to have the same smiley face. Without equipment, we aren’t privy to their main channel of communication, which is underwater sound. Investigators typically follow them around on the surface in a boat, as I did with my former student Ann Weaver, who recognizes about three hundred bottlenose dolphins in the Boca Ciega Bay Intracoastal Waterway estuary, in Florida. Ann carries an enormous photo album with close-ups of every dorsal fin in the area, which she has patrolled for over fifteen years. She visits the bay nearly every day in a small motorboat while on the lookout for surfacing dolphins. The dorsal fin is the body part we see most easily, and each one is shaped slightly differently. Some are tall and sturdy, while others hang to one side or miss a chunk due to fights or shark attacks.
From these identifications, Ann knew that some males form alliances and travel together all the time. They swim synchronously and surface together. The few times that they are not near each other, they get into trouble with rivals, who sense an opportunity. Females and calves, up to the age of five or six, move together, too. Otherwise dolphin society is fission-fusion, meaning that individuals gather in temporary combinations that vary from hour to hour and from day to day. Knowing who is around by looking at a small body part that regularly sticks out of the water is a rather cumbersome technique, however, compared to how dolphins themselves recognize one another.
Dolphins know one another’s calls. This by itself is not so special, since we too recognize each other’s voices, as do many other animals. The morphology of the vocal apparatus (mouth, tongue, vocal cords, lung capacity) varies greatly, which allows us to recognize voices by their pitch, loudness, and timbre. We have no trouble hearing the gender and age of a speaker or singer, but we also recognize individual voices. When I sit in my office and hear colleagues talking around the corner, I don’t need to see them to know who they are.
Dolphins go much further, however. They produce signature whistles, which are high-pitched sounds with a modulation that is unique for each individual. Their structure varies the way ring-tone melodies vary. It is not so much the voice but the melody that marks them. Young dolphins develop personalized whistles in their first year. Females keep the same melody for the rest of their lives, whereas males adjust theirs to those of their closest buddies, so that the calls within a male alliance sound alike.48 Dolphins utter signature whistles especially when they are isolated (lonely ones in captivity do so all the time) but also before aggregating in large groups in the ocean. At such moments, identities are broadcast frequently and widely, which makes sense in a fission-fusion species that dwells in murky water. That whistles are used for individual identification was shown by playing them back through underwater speakers. Dolphins pay more attention to sounds associated with close kin than to those of others. That this is based not on mere voice recognition but on the call’s specific melody was demonstrated by playing back computer-generated sounds that mimicked the melodies: the voice was left out while the melody was preserved. These synthesized calls triggered the same responses as the originals.49
Dolphins have an incredible memory for their friends. The American animal behaviorist Jason Bruck took advantage of the fact that captive dolphins are regularly moved from one place to another for breeding purposes. He played back signature whistles of tank mates that had left long ago. In response to familiar calls, dolphins would become active, approach the speaker, and call in return. Bruck found that dolphins have no trouble recognizing former tank mates regardless of how much or little time they had spent together in the past or how long it had been since they had last seen them. The longest time interval in the study was when a female named Bailey recognized the whistles of Allie, a female she had lived with elsewhere twenty years before.50
Increasingly, experts view signature whistles as names. They are not just identifiers that individuals produce themselves but are sometimes mimicked. For dolphins, addressing specific companions by their own whistles is like calling them by name. While Roah used his own name to call Lorenz, dolphins sometimes mimic the characteristic call of someone else to draw his or her attention. That they do so is obviously hard to prove by observation alone; hence this issue was, again, addressed with playbacks. Working with bottlenose dolphins off the coast of Scotland, near the University of St. Andrews, Stephanie King and Vincent Janik recorded the signature whistles of free-ranging dolphins. They then played the calls back through a submerged speaker while the dolphins who had produced them still swam in the vicinity. The dolphins replied by calling back, sometimes multiple times, to their own characteristic whistles, as if confirming that they’d heard themselves being called.51
The deep irony of animals calling one another by name is, of course, that it was once taboo for scientists to name their animals. When Imanishi and his followers started doing so, they were ridiculed, as was Goodall when she gave her chimps names like David Greybeard and Flo. The complaint was that by using names we were humanizing our subjects. We were supposed to keep our distance and stay objective, and to never forget that only humans have names.
As it turns out, on this issue some animals may have been ahead of us.
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