Sex on Six Legs: Lessons on Life, Love, and Language from the Insect World - Marlene Zuk (2011)

Chapter 9. Six-Legged Language

The Battle between Impatience and Procrastination

SUDDENLY, a lot of bees seemed to be flying in and out of our garage. There has always been a space of about a foot between the top of the wall and the roof, so it is not an enclosed building, but while I was used to seeing insects, our cats, and the occasional possum or raccoon making use of the opening, for a couple of days a steady stream of humming golden-bodied workers went back and forth at one corner. Needless to say, no flowers grow in our garage, so I wasn't sure why I was seeing half a dozen or so bees buzzing overhead every time I went to get my bike.

I told my husband. They're just bees, he said. Don't worry about it. I wasn't worried, exactly. I just was a little leery of what the increased traffic might portend. And on the third day I noticed a baseball-sized clump of bees surrounding a beam inside the garage near the opening they had entered. Uh-oh, I thought. They're swarming.

After a suitably pointed "I told you so" to my husband, I knew just what to do. I called Kirk Visscher, who is a professor of entomology at my university and an expert on bees and beekeeping. "Help," I said. "We've got bees." Kirk drove over to our house with a portable hive constructed from boards, which he set out at what we hoped was a tempting yet suitably lengthy distance from the beam, and our garage. With a little luck, he assured us, the bees would move their operations into the hive and he could take the colony to use in his research back on campus.

Luck, however, was not with us. A day later, the clump had grown to the size of a small football, and honeycomb was visible when the layer of bees shifted. Kirk returned, this time with the age-old beekeeper's equipment of a funnel and smoker. He gently pumped the smoke over the cluster, which had no discernable effect on the bees other than to make them hum in what, at least to my ears, was a rather agitated way. I backed up into the driveway and asked Kirk exactly what we were trying to accomplish, since having a garage full of annoyed and active bees did not seem like an improvement over having one full of reasonably quiescent ones.

"We're just trying to convince them that this wasn't the great place they first thought it was," he said. Like moving to a neighborhood you later discover has bad air quality or a lousy school system, I guess, only without the complication of already having filed the paperwork and commencing escrow. Whatever the rationale, in another day the entire swarm had suddenly decamped, as if they had never been, except for the telltale irregularly shaped sheets of fragrant honeycomb attached to the beam. Presumably, the bees had left for a more permanent home, whether in a tree cavity or some other fortunate beekeeper's hive, but at any rate sufficiently far from our garage.

Honeybee swarms are the colony's way of reducing overpopulation. When a colony grows large, the worker bees nurture new queens, and the old queen, along with perhaps half of the workers, goes off to establish a new hive somewhere else. Initially, the pioneering bees and their queen settle in a mass like the one inside our garage, while scout worker bees go out and look for a new place to live. For centuries, enterprising humans have taken advantage of these temporary swarms to capture a new colony and place it into a manufactured hive, as Kirk had attempted. While handy for the beekeepers, this abrupt human-induced end to the house-hunting process had meant that no one paid attention to, or understood, the extraordinary process the bees undertake in making a decision about where to go.

Remember, the bees are in a swarm of up to ten thousand individuals, surrounding a plump, fecund queen, who must be protected at all costs. Only a few bees are able to survey their surroundings and choose a site where they and subsequent generations will spend the rest of their lives. What makes for exclusive bee real estate? How do the scouts convey the news about where they have been to everyone else in the swarm? And once the information is delivered, how does the group decide which of the prospective new homes is the most suitable? Finally, how can such an enormous group of tiny creatures stay together and get to the same place?

The answers to these questions shed light not just on the behavior of bees, but on how decisions are made by groups of animals, whether these are insects, migrating birds, or humans. At the same time, only bees and their close relatives show the kind of complex communication system that challenges our definition of what it means to be human. How do insects decide where to go? Further, and more provocative, is the means by which they indicate their destination a real language?

The Spirit of the Hive

ALL KINDS of animals, and even some microorganisms, make decisions: go left instead of right, eat this food and not that, sing now or rest for the afternoon. Decisions by female Drosophila about where to lay their eggs have vital implications for the fate of the offspring, and scientists have made great strides in understanding how genes control the fruit flies' choices from among an array of options (too much sugar in the medium and they turn up their little ovipositors, or egg-laying organs, at it). But the flies do not have to consult with their families about their decisions, and no one else offers an opinion.

The bees, however, live in a society, and while it is not democratic, neither is it a dictatorship. The queen may have the last word in reproduction, but not in moving house. Maurice Maeterlinck, the playwright who praised the nobility of ants and their cooperative nature in his 1930 book, had written The Life of the Bee in 1901. He considered the way the colony found its way to its new home, and concluded, "All things go to prove that it is not the queen, but the spirit of the hive, that decides on the swarm." As with house hunting in humans, the decision about where to move in honeybees and other social insects is fraught with complication. The decision must be made fairly quickly, because the swarm is vulnerable as it clings to a branch (or garage ceiling beam). At the same time, its consequences are crucial, since the colony will spend its life in its new home and needs to have ample room to raise its brood, with food sources located nearby. How do the bees keep from spending endless time in filibuster and argumentation, like a miniature all-night congressional attempt to arrive at a budget? What is more, sometimes the old home is destroyed by fire, flood, or the untimely arrival of a hungry bear, necessitating the abrupt evacuation of the old home and a pressing need to find a new one. A group decision is essential; the bees can't simply go back to their constituents and try again next season.

Group decisions are particularly interesting because they imply first that the members of the group are able to convey messages to each other, and second that they have some mechanism for evaluating each individual's contribution. Groups have a rather dubious reputation when it comes to collective activity; none other than Friedrich Nietzsche disparaged humans by suggesting, "Madness is the exception in individuals but the rule in groups." Maeterlinck, however, was more charmed by the process of group decisions in the bees and felt that "there can be no doubting that they understand each other," although "certain as it may seem that the bees communicate with each other, we know not whether this be done in human fashion." The bees exhibit what is called a consensus decision, which means that they choose between several mutually exclusive alternatives and then all abide by the selected one. This process is similar to what goes on in a democratic election, or in international treaties signed by a number of nations with a common goal. Everyone doesn't necessarily contribute to the decision, but they all agree to do the same thing in the end.

Consensus decisions are distinguished from what are called combined decisions because they require everyone to concur, which means the group has to possess a fairly sophisticated means for exchanging information. A combined decision is made when the individuals in a group simply assign themselves different tasks, for example, the allocation of hive cleaning versus foraging in bees, but don't all agree beforehand on a list of who will do what. The distinction is important because getting everyone to agree to a single outcome means that they may have to sacrifice their own interests in doing so, a rather advanced capacity for a tiny insect. Many scientists first started thinking about the possibility of a "hive mind," that controversial greater-than-the-sum-of-its-parts superorganism, when pondering the way that social insects choose a new place to live.

Aristotle had noticed that it seemed as if bees received information from scouts that had made advance sallies to find potential nest sites, but the process of deciding on a new nest site was first studied in detail in the 1950s by a German zoologist, Martin Lindauer. He happened upon a swarm near the Zoological Institute at his university in Munich and noticed that a few of the bees on the outside of the swarm were performing the same waggle dance that his mentor, the Nobel laureate Karl von Frisch, had described in the context of signaling the whereabouts of food sources. Since the bees had no pollen or nectar, Lindauer wondered if they might be signaling not the location of a patch of flowers, but the possible place the swarm might settle.

By recording the different locations encoded in the dances of the apparent scouts, Lindauer noticed that although the bees seemed to be dancing "for" many different sites at first, eventually they seemed to settle on just one. Soon after this winnowing of alternatives, the swarm rose in a body and took off for the site that had made it to the finals. In the decades that followed Lindauer's work, scientists established the characteristics that bees would use in their description of a dream house to a bee real estate agent, including a south-facing entrance, a small enough entrance hole to discourage unwanted visitors, and enough room for an average-sized honeybee colony to spread out in comfort. The ability to compare several different possibilities, like enterprising couples scanning the online real estate ads, indicates a rather sophisticated cognitive ability on the part of the insects and has even led to the suggestion that the bees possess some form of consciousness. Why being able to choose a split-level ranch over a refurbished Victorian is peculiarly emblematic of higher intelligence, while other decisions are not, is unclear to me, but it is undoubtedly a complicated decision.

In the 1990s, Kirk and his former advisor, the eminent bee expert Tom Seeley at Cornell University, began to work with other colleagues to determine how the selection of just one site was made. One swarm took about 16 hours of dancing, spread over three days, to reach a decision, with eleven different potential sites taken under consideration before the winner was determined. In a New York Times column, James Gorman noted that the scientists were, like Maeterlinck, convinced that the bees arrived at decisions that were good for the group, and that "Dr. Seeley is a bit more cheery than Nietzsche," a comparison that was probably novel for both the entomologist and the philosopher.

So how do the bees choose the winner? The idea of a bee version of polling the hive constituents to get a sense of everyone's views on the various sites before arriving at an informed decision is appealing, but it turns out that this is not how the bees decide which scout to follow. Instead, they seem to be sensing a quorum of dancers "for" a particular site, and then the entire swarm follows the quorum.

Kirk, Seeley, and Kevin Passino of Ohio State University made this discovery using bee colonies on Appledore Island off the coast of Maine, where Cornell has a research facility. The island was handy because it has almost no trees that could serve as natural nests, which means the scientists could provide all the potential homes for the colonies they brought there.

The scientists gave different swarms of bees on opposite sides of the island either just one nest box into which they could relocate, or five similar boxes set close together. If the bees required a quorum of dancers, the dilemma of five equivalent alternatives should delay the formation of the quorum and, hence, delay the swarm movement itself, but the rest of the decision-making process would be the same in the two cases. As predicted, the bees took an average of 442 minutes to arrive at a decision when they were spoiled for choice, as it were, compared with just 196 minutes when one box was available. "Group intelligence," the researchers concluded, "is a product of disagreement and contest." Whether that constitutes more optimism than Nietzsche is perhaps a matter of debate.

Kirk and Tom Seeley also determined that the bees dance differently depending on the quality of the site they have discovered; scouts spent equal amounts of time inspecting two potential sites that were offered, but performed more circuits of their dance back at the swarm for the better location. The bees also avoid getting drawn into agonizing fruitlessly over a poor candidate by the rapid decrease in sequential visits to a lower-quality site, so that they are able to ruthlessly reject a loser instead of second-guessing themselves, something more humans would probably do well to emulate.

How the bees assess the presence of enough scouts to constitute a quorum is still not well understood. The swarm does not always arrive at a unanimous decision; occasionally one will split at takeoff, and even when dissention is not so drastic, a few divergent dancers will still be rooting for their own selection up until the very last minute. Until very recently, scientists likewise could not understand how the group of bees could all get up and move in synchrony after the winning site was selected. The scouts produce a kind of rallying cry, called piping, that seems to energize the swarm to warm up before they take off in unison.

Some work by Seeley and Clare Rittschof of the University of Florida suggests that the scout bees work the crowd by moving among the more languid members of the group, making a stereotyped set of motions accompanied by sounds, called a buzz-run. The buzz-run seems to encourage any laggards to move their wings as well, which in turn ensures that everyone's wing muscles are sufficiently warmed up for flight. Because they are cold-blooded like other insects, bees need to reach a certain temperature before they can fly, and they do so by revving their muscles like diminutive engines. Rittschof and Seeley then proposed that the scouts act like swarm thermometers to gauge the temperature of the mass of bees and trigger its synchronized takeoff when everyone is ready.

Even after takeoff, the synchronicity of the swarm is amazing. Although the scouts have done their advertisement and the decision has been made, less than 5 percent of the bees in the swarm have actually been to the site themselves and, hence, don't know exactly where to go. Yet all of the ten thousand or more end up in the right place, often miles away. Another publication with Seeley as the bee expert, this time with engineer Kevin Schultz from the Ohio State University as a collaborator, gave the solution to this problem as well. Using high-definition films of the swarms on Appledore Island, the researchers examined more than 3,500 frames of bee movement and determined that the informed few fly through the top half of the swarm at high speed to lead the way. These leaders are called streaker bees, after their cometlike movements in the cloud of insects.

Microscopic Real Estate

PEOPLE have long taken a personal interest in the real estate preferences of honeybees, mainly because the product of a smoothly running hive is relevant to human well-being. They have been less concerned about the decisions made by other social insects, such as ants, so long as they do not decide to relocate in or near human habitation. The house-hunting behavior of ants, however, is both similar to and different from nest site selection in honeybees, and the contrast is instructive.

Much of the research on group decisions by ants on where to live has centered on a couple of species with life histories that sound like they come from a fairy tale, or maybe a Winnie the Pooh story. The insects are even tinier than the ants commonly seen in kitchens, and use either rock crevices, or, more charmingly, acorns, as their place of residence. The entire colony, queen and all, can fit into a space smaller than a person's thumb. Needless to say, this makes replicating their world in the laboratory extremely easy; one of the foremost researchers on these ants, Nigel Franks of the University of Bristol, makes little homes for them by gluing a bit of cardboard between two glass microscope slides to recreate a crevice that is also easily spied upon.

The ants' house-hunting activities have attracted attention mainly because they use the tandem running procedure I described in the chapter on learning to help their nest mates find the new location. As in the bees, ants send out scouts to search for new homes, but unlike the bees, the scouts enlist enthusiasts for the new cavity by the same "follow me" motions used to direct other colony members to food sources. The ants don't perform waggle dances like the bees, but they will recruit for good sites more quickly than for poorer ones. The new recruits, if they concur with the desirability of the chosen location, then get others to join them. If you are an ant living in a small dark hollow, the best home has a narrow entrance with dim light, presumably to discourage predators, and just the right amount of floor space. The ants can even evaluate the potential for nasty neighbors, in the form of a foreign ant colony, and eschew such potentially troublesome locations.

At this point the process diverges from that of the bees, because once a site is selected by enough ants, the process becomes one of shanghai rather than persuasion, as the remainder of the colony is simply picked up bodily and carried, head ignominiously pointing backward, to the chosen location. Carrying is three times faster than tandem running, and once the carrying starts, the ants are committed to their new location and do not switch preferences in midstream. Regret, it would seem, is not part of the ant repertoire. As a paper by Robert Planqué and his collaborators, including Franks, puts it, "Ant colonies have found a good compromise between impatience and procrastination." Would that we were all so prudent, at least when it comes to moving house.

In human groups it's often the case that the larger the crowd, the harder it is to reach a decision, whether about going to war or choosing a restaurant. In contrast, the ants seem equally good at determining the best nest site from among an array of options presented in the laboratory regardless of the size of their colony. The larger colonies do use more of the tandem runs to exhort others to follow them, and seem to need a larger quorum of assenting individuals before they decamp. Interestingly, both small and large colonies select sites that will comfortably contain a colony that has grown to full size, suggesting that the ants can anticipate their future needs, a remarkable feat.

Franks and his colleagues demonstrated this ability of ants to plan by showing that they can distinguish between various qualities of nests and perform reconnaissance when they evaluate the possibilities. The official definition of reconnaissance, according to the Oxford English Dictionary, is "an examination of a region to ascertain strategic features through a preliminary survey," and the ants manage this by retaining information about the different potential nests and using it later to recruit for different sites. Like a person who sees an ice cream store while jogging in the morning and files away the information for dessert, the ants can remember the landmarks near a potential nest site or the odors left there, even if they are not actively house hunting at the time. If these cues are removed by an investigator, and the ants are then required to find a new home by virtue of the scientist destroying the old one, the ants can no longer distinguish among the sites.

Ants can also arrive at the best group decision almost as a by-product of individual behavior, without the need for extensive communication. Say that a tasty bit of food can be found at the other side of a deep crack in the ground from the colony. A leafy branch lies across the crevice, and the ants can either take a shorter, direct path to the food or a longer, more convoluted one, depending on which twig they use to cross. The shorter path would be more efficient, and it turns out that this is the one favored by the ants. But how did they arrive at the decision? Even for a devoted myrmecophile, it defies reason to imagine the ants testing out one path and then the other, timing both, and then sending the message to the rest of the colony that they can save their exoskeleton some wear by taking the shorter journey.

It turns out they don't have to. Franks and several other scientists determined that a much simpler process is at work. As an ant returns from a food source, she lays down an odor trail that attracts her nest mates. The more ants that have been back and forth from the colony, the stronger the attraction of a particular pathway. Thus, the shorter trip over the twig gets more use and builds up more odor, simply because it takes less time to go to and from the food, and the ants themselves reinforce the easier path as the best choice. Others follow and, voilà, the colony as a whole has made the right decision. Similar behavior allows the ants to select the easiest sites to excavate when the possible nest entrances are blocked with sand.

At least one other species of ant, the delightfully named gypsy ant, can make collective decisions about which kinds of food can be harvested singly and which require enlisting reinforcements. A group of French and Spanish researchers presented the gypsy ants with dead crickets, which could be moved by a cooperating group of ants but not by a single individual; dead shrimps, which are five hundred times heavier than a worker and must be butchered into individually transportable pieces; or sesame seeds, which as any picnicker knows can be easily borne aloft by an ant acting alone. Making off with food in a timely and efficient manner is important, because other ant species are potentially lurking nearby, ready to snatch any food left unattended. The ants were able to gauge the number of workers necessary to lift and carry the crickets depending on the size of the prey, with small crickets requiring about a dozen workers but large ones fifteen or more, and they quickly recruited an even greater number of ants to carry out the dismemberment of the shrimp before it could be detected by competitors.

Not all group decisions by insects have such a happy outcome. Although the social ants and bees get most of the attention, scientists have also examined collective behavior in forest tent caterpillars, which live in groups until they spin their cocoons and become adult moths. The caterpillars move in munching hordes through the treetops and may either linger on a particularly succulent tree or move quickly through it in search of a more nutritious set of leaves. Because of the caterpillars' discerning tastes, forests that have been attacked by the caterpillars are often a patchwork of ravaged and intact trees. In nature, experiments have shown that they prefer carbohydrate-enriched or untreated aspen leaves, rather than leaves with a high protein content, a kind of anti-Atkins diet. Offered a choice between diets concocted in the laboratory that differ in their nutrient composition, an individual caterpillar will make the "right" selection and eschew an unbalanced low-carbohydrate food in favor of one with the natural blend of proteins, carbohydrates, and fiber.

In groups, however, the caterpillars, like schoolchildren egging each other on to eat Doritos and Twinkies instead of carrot sticks, will often end up choosing the less nourishing offering. The problem seems to occur because, like ants, the caterpillars follow odor trails left by their companions. The initial decision to taste one or another of the foods is made at random, but once a caterpillar has started eating, its odor trail encourages others to follow, and then the entire gang gets trapped by heeding the message that went before it. The caterpillars thus follow each other to their collective nutritional doom. Unlike the bees or ants, the caterpillars lack any capability of communicating their state to each other, so they cannot indicate that they have arrived at a less tasty branch and warn others of their folly. Nietzsche's pessimism about groups seems to be better illustrated by the caterpillars than the bees in this regard, which makes you wonder whether we are so close to the social insects after all. Luckily, the caterpillars differ in their tendency to move around, and if a large proportion of the group was of a more active predilection, the group itself was less cohesive and managed to escape the poor decision.

Flying versus Walking, and the Lead-up to Language

DECISIONS about food or nest sites are closely tied to the success or failure of any given insect colony, and the way that different species get help when an individual finds a food item that is too big for it, or needs to get everyone else on board with a decision has important implications for social behavior. The way that an insect recruits is, in turn, constrained by its own biology. Ants, as I've discussed, lay down an odor trail that becomes stronger and stronger as more workers use it, but to each ant that traverses the trail, its end point is a mystery—she simply follows her nose, so to speak, until she reaches the goal. In the case of establishing a new nest, ants can be carried by their nest mates to the new site, and again those being unceremoniously tucked under a leg need have no idea of where they are being taken.

Bees are different. Flying instead of walking means that you can't easily haul your sister workers around, which means that the bees need some other way to convey information to the rest of the colony. And although some species of bees do place dabs of odor on plants and other objects as signposts on the way to a food source, pheromones are not nearly as satisfactory a method for indicating directions for flying insects as they are for crawling ones; the bees have to continually dart down to the vegetation, and the odors fade without continual reinforcement by a stream of workers.

What's more, at least some kinds of bees have to worry about eavesdroppers on their odor cues. James Nieh at the University of California at San Diego has been studying tropical stingless bees in Brazil, Panama, and other parts of Latin America for many years. The stingless bees are social, like honeybees, and Nieh noticed that the species he was studying left scent marks near good food sources. The problem was that the scent marks were easily detected by a larger and more aggressive species of stingless bee, and when the bullies found the food, they dispatched their victims with what Nieh describes as "a range of forms of aggression from threats to intense grappling followed by decapitation." The victim species avoids the odor marks left by the aggressor species and sticks to its own signals, but the aggressor does the opposite, preferring the odor marks of the victim species to its own.

What's a bee to do? One possibility is to encrypt your directions. Instead of setting out an odor that broadcasts "Tasty morsel here!," whisper your findings only to those for whom the message is intended: your nest mates. In other words, evolve a symbolic language with which you can convey what you know to others in the privacy of the hive, without fear of being overheard. Nieh suggests that the famous dance language of the honeybee, and its counterparts in a few other species, evolved under pressure to hide indications of the location of rich food sources from any competitor bees in the area. Ideally, of course, one would have a code able to be read only by the members of one's own colony, but that degree of encryption seems to be beyond the bees, and so they have had to settle with having species-specific, or at least population-specific, signals. Combined with the other advantages of such communication to a flying rather than walking insect, for example, the inability to carry other workers and the inconvenience of odor trails over long distances, the dance doesn't seem like an anomaly, but like an obvious solution to a problem.

Ants and bees differ in a few other respects: ants are much slower than bees at redirecting their efforts to a newly introduced rich food source, and the members of an ant colony act almost like neurons in the brain when responding to stimulation. Ants also exhibit something called stigmergy, which sounds like either an eighties band or what happens when the recipients of social stigma gather in groups, for example, smokers outside a building, but is the way that the ants coordinate each other's movements by changing the odor trails that convey activity patterns. This too means that the ants can make decisions without resorting to the direct exchange of information among individuals.

Bee Spoke

REGARDLESS of the waggle dance's evolutionary origin, the idea that bees could possess a symbolic language has never been simply relegated to an incidental by-product of their flying existence, a serendipity of evolution. Anthropologists endlessly debate whether it is possible to have thinking without language, whether one has to be able to formulate thoughts into something resembling words to be truly sentient. And they take enormous pains to define what makes our language special, and how it can be the one holdout in making humans different from all other animals. But the bees make us ask instead whether it is possible to have language without thinking, since even the most ardent admirers of the waggle dance do not maintain that the bees' cognitive capacities mirror our own. So do the bees speak? And if so, does it mean we have to admit them into a special club, unlike any other animal?

Although many beekeepers had noticed that single foraging bees seem to advertise the location of nectar-rich patches of flowers to the rest of the hive, the first detailed description of the forager's performance was made in 1919 by the Austrian scientist Karl von Frisch, who shared the 1973 Nobel Prize in physiology and medicine with the ethologists Konrad Lorenz and Niko Tinbergen for his accomplishment. He was able to carefully track the movements of individual bees by placing his colonies in glass-walled observation hives and marking the bees with either dabs of paint or tiny numbered circles that he glued to their backs.

Von Frisch noted that when a worker bee returned to the hive after visiting a rich food source, she performed a stereotyped series of movements on the surface of the honeycomb. If the food source is close by, less than 50 yards or so, she did a rather simple "round dance," in which the forager runs in narrow circles. More distant food patches warranted a "waggle dance," which contains information about both the distance of the food from the hive and the direction in which it lies. The waggle dance consists of a straight run followed by a semicircle first to one side and then another, in a rough figure eight, with the bee waggling her abdomen energetically during the straight run.

The length of the run is correlated with the distance of the food from the hive, while the angle of the bee's body relative to vertical indicates the angle between the sun and the food source. The vibrating wings of the dancing bee also convey auditory information to the rest of the hive; silenced bees do not recruit others to the food source, and it makes sense that sound would be needed, since the inside of the hive is dark and the other workers cannot simply watch what the dancer is doing. Once the dancer has completed her performance, other bees venture out of the hive and go, more or less directly, to the location she indicated.

In other words, the bees seem to have symbolic representations for the distance and direction of the food, which fits many if not all of the criteria for an actual language. This was big news. Historian of science Tania Munz points out that during the 1960s, bee language was "the most widely studied form of animal communication and some deemed it the most complex second only to human speech." Even Carl Jung took note, musing that we would interpret the bees' behavior, if it occurred in humans, "as a conscious and intentional act and can hardly imagine how anyone could prove in a court of law that it had taken place unconsciously.... Nor is there any proof that bees are unconscious." Those with a yearning to see the waggle dance for themselves need look no further than YouTube, of course; one video of a dancing bee had nearly eighty thousand hits, and enthusiastic if sometimes inadvertently ironic comments such as, "I couldn't do that. Bees are smarter than me," "Why would you shake your butt as communication, weird," or, even better, "Wow. Their [sic] smart."

Although von Frisch's discovery was mainly greeted with amazement and rather uncritical acceptance by both the general public and other scientists, a few remained skeptical that the bees were truly capable of using the sophisticated information encoded in the dances. Foremost among these was Adrian Wenner, a professor at the University of California, Santa Barbara—and, in the spirit of full disclosure, my former teacher and mentor as an undergraduate. A soft-spoken but determined man, Wenner did not dispute the information contained in the waggle dance; he could observe a returning forager and calculate the distance and direction of the food patch perfectly well himself. He just didn't think the bees were using the information.

Wenner claimed that a much simpler explanation for how the bees found the food existed: the other workers simply smelled the odor that lingered on the recruiter's body, left the hive and flew, sniffing the air, until they perceived the same scent emanating from a patch of flowers. The experiments that von Frisch and other scientists performed demonstrated merely that the bees found the food, he said, not how they did so. His hypothesis was much more parsimonious, and hence, Wenner concluded, scientists were obliged to use it rather than the more elaborate explanation that required talking bees. Why, then, did the bees dance, and why did the dance contain information that was interpretable by humans, if the bees didn't use it? Wenner would always smile an impish smile when asked that question, and point out that nature did not evolve for a purpose—to suggest that it did was teleological and unscientific. The dance didn't have to be used by the bees in the way we could use it; a cricket's call can be used to calculate the temperature because he sings more quickly when it is warmer, but no one has ever suggested that the crickets evolved their chirps so that they could act as thermometers.

Wenner's iconoclastic views were not particularly popular, which he also attributed to an unscientific bias toward wanting to believe the more dramatic and exciting story of an insect language. Eventually, however, scientists began to pit the two ideas against each other. To some extent, it is unfair to claim that von Frisch dismissed the use of odor cues by the bees, since he did acknowledge its role in some of his papers, and indeed most researchers acknowledge that the bees in the hive do not ignore the information contained in the scent of a returning worker.

Many biologists were convinced that the bees do indeed use the information in the dance by some experiments published in 1975 by James L. Gould, in which he manipulated the dancer to "lie" about where the food was located using a flashlight to mimic the sun and, hence, alter the angle at which the dance was produced relative to the sun's actual position. Wenner was unconvinced, suggesting that the experiment was never replicated, and he and a few other scientists also claimed that Gould did not fully control for the bees' use of odors as an alternative explanation.

Several scientists have tried to manufacture artificial bees that could be made to dance inside the hive to further test the hypotheses, and one of these was able to recruit at least some bees to the food source it was programmed to dance about to the rest of the colony. Wenner once again dismissed these findings as inconclusive, and it is certainly the case that the mechanical bees didn't do the job nearly as well as a real one.

The conclusive set of experiments, at least in the majority of scientists' view, came from H. Esch and colleagues, who were able to manipulate something called the optic flow perceived by the bees. Bees measure distance by gauging the way images in the environment move across their eyes as they fly, rather like clocking the trees that tick by the windows of a moving train. The scientists trained the bees to fly through a tunnel lined with a black and white pattern that presented an optical illusion to the insects, making it appear that they had flown a longer distance than they actually had. When the fooled bees got back to the hive, they produced a dance that indicated the food was farther away than it was. The recruits promptly flew to the wrong site, indicating that they had indeed been misled by the dance itself.

Yet other studies used harmonic radar to track individual bees and the flight paths they took to the feeder or flower patch; these showed that most of the bees recruited by a dancer took a straight path to the food, rather than zigzagging back and forth the way they would be expected to if they were simply using the odors in the air to find the patch that smelled like the dancer inside the hive.

Finally, my friend Kirk Visscher and a former student of his, Gavin Sherman, demonstrated that the waggle dances help the bees survive in nature. In a clever experiment, they used lighting to mimic the sun and misdirect the bees, so that the dances didn't help the members of the hive to find a food source. They allowed a control set of colonies to dance appropriately. At the end of the season, the deceived colonies had accumulated significantly less honey than those in the control group, an important consideration in the well-being of the hive.

No one, including Kirk, disputes that the bees also use the odor information from the initial dancer to find food, and that under some circumstances the dances are not needed for the colony members to find out where they can forage. At some times of year, the bees can find plenty of nectar by relying simply on the flower odors in their environment that are carried on the bodies of the workers that find each patch of blossoms. But when the going gets tough, the bees seem to need dancing. Some theoretical work by Madeleine Beekman and Jie Bin Lew of the University of Sydney in Australia formalized this mathematically, demonstrating that dancing helps a colony concentrate on the best food sources in the area and not waste time sending workers to a low-quality patch. It is most helpful when the probability of finding a patch on one's own as an independent forager is relatively low, because the dance allows the colony to exploit only the richest nectar sources.

Bilingual Bees?

WHERE did the bee dance language come from? I suggested earlier that scientists believe it may have evolved from the need to hide signals of food sources from competitors, but that problem is common to many group-living animals, not just honeybees. Which species have dance language, and how it is used, sheds light on the origin of this behavior.

Beekman and her colleagues study dance language in the red dwarf bee of southeast Asia, which is closely related to the honeybee but nests in the open, making a single comb that is suspended from a shaded branch, rather like a wasp nest. This nesting habit is thought to be more like the ancestral state, with the elaborate cavity nests of the honeybees and several other species being more recently evolved. Dwarf bees still dance, and like honeybees, they do so both when they are selecting a new nest site and when they are feeding. But giving directions to a new nest site on a branch out in the open poses a much different problem than telling the rest of the colony how to find a small entrance hole to a cavity, such as the honeybees use. It's like the difference between telling someone to head north on State Street until he sees a big pink building—"you can't miss it"—versus giving explicit directions to a door on the third floor, east wing, of that building. On the other hand, a flower patch is a flower patch, and directions don't need to be all that precise when a worker is dancing to indicate where her nest mates can find food.

By videotaping dances of the dwarf bees, Beekman and her colleagues found that the dances used for both food and nest site directions were equally imprecise. Honeybees, in contrast, are far sloppier when they dance to show the other workers where food is than when they are directing them to a new home. The scientists believe that the dance evolved as a way to convey information about the new nest site, and that its use to indicate food sources came later.

If more than one species of bee uses symbolic language, can they understand each other? In a paper titled "East Learns from West," Songkun Su from Zheijiang University in China and co-workers showed that Asian honeybees, which are a different species than the European honeybees commonly found in Europe and the species that has been introduced to North America, can follow directions given by their European counterparts. Su and colleagues painstakingly constructed colonies containing a queen of one species and workers of the other, a daunting task because the specific odors of each colony usually mean the different species detect and kill any outsiders. Ordinarily the dances from the two bee species differ in what might be called dialect, with variations in the duration of the waggle portion of the dance. Su demonstrated that the two species could follow each other's directions, which means that the bees must learn some elements of the dance language.

Bees, Chimps, and Symbols

DESPITE the great interest in bee communication and the ever-greater elucidation of the dance, as Wenner points out, no one has ever been able to use the information to direct bees to particular crops that need pollinating or to sources of nectar that would be preferred by humans for honey production. So what is the significance of the bee dance language?

As I have mentioned before, we seem almost obsessed with setting out criteria for membership in a club that only we can enter; humans are the only species to use tools, for example, or to routinely kill members of our own species without using them for food. Both of these turn out to be unwarranted—chimpanzees, crows, and several other animals use tools, and fig wasps, among other species, routinely slaughter their own. One can detect a certain desperation in resorting to homicidal violence as a badge of distinction, but the effort continues. And language, with its slang and poetry, has always remained a prime candidate.

The problem is that many if not most other animals communicate, too, and they communicate in often complex and sophisticated ways. As Alison Wray put it in a book titled Language Origins, "Pinning down precisely what it is that makes human language special has never been so difficult. It's not that we no longer regard it as special, but almost every time you think you have a feature that helps define the real essence of language, or that provides a necessary context for its emergence, you seem to find some other animal that does it as well."

When that other animal is an insect, the comparison seems particularly troubling. Eileen Crist, in an analysis of the bee language controversy, says, "This almost-serious idea of an insect with language has had an unsettling effect in behavioral science." She notes that the waggle dance satisfies the criteria of having a set of rules, with a necessary order and complexity of the symbols that are used. Psychologists Mark Hauser, Noam Chomsky, and Tecumseh Fitch declare that human language is qualitatively different from other forms of animal communication, whether birdsong or bee dances, at least if one distinguishes between what they call the faculty of language in the broad sense and the narrow sense; it isn't clear whether bees get to join at least one of those circles. Other language scholars struggle with the distinction, sometimes mentioning the auditory sensitivity that enables the nearly endless discrimination among different sounds. The idea that Washoe the chimp or Alex the African grey parrot could be taught elements of our own language makes us reexamine our uniqueness yet again.

Just as an aside, amid all the hand-wringing and contention about whether what the bees do is really "language," no one seems to question whether it's really "dance." Maybe the dance scholars are just more easygoing than the linguists, or maybe we are already comfortable sharing that capacity with other species, though one could argue that the struts and tail shimmies of a peacock are hardly analogous to a waltz. But this points to the futility of the discussion; if we always narrow our definition of language, sooner or later we will end up with a capacity only we can possess. The breathtaking displays of a bird of paradise, or the comical movements of a lizard extending its dewlap, do not detract from the achievements of a ballerina.

It seems to me that the bees are not much like Alex or Washoe, because we can't teach them to say "cup," or to comment on the day's activities, or ask for another piece of fruit. Bees only talk about what they need to, mainly involving food or a place to live, and I think we have gotten way too interested in the accident of their using representational movements in communicating those objectives. Bee language didn't arise from a common ancestor with humans, which means we can't see it as a primitive version of our own language. This forces us to be less anthropomorphic than we are with the primates. And the less anthropomorphic we are, the more incredible the bees' accomplishment becomes, because they evolved this system of communication with entirely different selection pressures than the ones that led to human language. How did evolution take such different paths to get to superficially similar outcomes?

If it's true that bees needed a way to hide their communication from rivals, and that the ants' method of hauling colony members off to the new nest was unworkable for a flying insect, two other questions remain that in my mind are much more interesting than endless fussing over who does and doesn't qualify to enter the human club. The first is why all other social flying insects did not evolve some version of dance language. The second is why, when we are much more like the ants than the air-bound bees, we humans evolved language ourselves, rather than just dragging each other around when we wanted to convey a decision. Maybe human language isn't unique. But it beats at least one of the obvious alternatives.

Bee language, and the complicated decisions that accompany it, exemplifies why we keep coming back to insects, why, despite their encroachment on our kitchens and sometimes our health, we can't shake our simultaneous sense of connection and distance. We all want to be able to talk to animals. With bees, as with other insects, we can be pretty sure that we will never be able to communicate with them, even to the limited extent we can communicate with our pets. Fanciful interpretations such as T. H. White's and Maeterlinck's aside, no one really believes we could get a sense of what a bee is feeling, if it has feelings at all. And yet although we can't talk to them, they seem to be able to talk to each other, in a way that can be said to be more sophisticated than the chirps and buzzes common throughout the rest of the animal kingdom. It is precisely this sense of them being more like us than anything else, with their elaborate houses, facial recognition, use of others' labor, and complicated symbols, and yet so impossibly different from the inside out, that keeps us hooked.

Nearly a century ago, as the Jazz Age gathered steam, Don Marquis was a writer for the Evening Sun in New York. His work encompassed many topics, but he is best remembered for creating—or at least transcribing—archy, a cockroach that wrote free verse on Marquis's typewriter by laboriously crashing his head into the keys. Archy's inability to hold down the shift key led to all of his poems being written in lower case, which added a certain insouciance to his observations. The poems were first collected in 1927 and were followed by several additional volumes, with a new trove of Marquis's work discovered in 1986. The poems proved remarkably popular, coming to include commentary by the insect's friend mehitabel, "an alley cat of questionable character," as she is described on DonMarquis.com.

Archy was generally blunt about the human condition, but he reserved some of his most trenchant observations for the role of the six-legged in the lives of the bipedal. As I have throughout this book, archy questioned the careless hubris of our assumption of superiority:

men talk of money and industry
of hard times and recoveries
of finance and economics
but the ants wait and the scorpions wait
for while men talk they are making deserts all the time
getting the world ready for the conquering ant
drought and erosion and desert
because men cannot learn

The descendents of archy and his kind no longer seem to be leaving us missives, which seems rather a shame. Perhaps our modern keyboards seem daunting, with their need to be connected to vast processors that are inaccessible to a mere cockroach lacking both strength to turn the switch as well as a password. I would give a great deal to come into my office one day and find something like this, one of archy's best, on my monitor:

i do not see why men
should be so proud
insects have the more
ancient lineage
according to the scientists
insects were insects
when man was only
a burbling whatisit

One can only hope that perhaps one day soon our modern cockroaches will learn to manipulate a touchpad.