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

Chapter 8. Pirates at the Picnic

Today it is accepted as proven that the ant is incontestably one of the noblest, most courageous, most charitable, most devoted, most generous and most altruistic creatures on earth.

—MAURICE MAETERLINCK, 1930

If ants had nuclear weapons, they would probably end the world in a week.

—BERT HöLLDOBLER AND E. O. WILSON, 1994

ANTS may inspire more emotional reactions than any other insect, reactions that go far beyond the revulsion of finding a cockroach scurrying across the kitchen counter or pleasure at seeing a butterfly light on a flower. As the two quotations above attest, ants can be paragons of harmony and virtue, or symbols of bloodthirsty violence. Honeybees come close to ants in serving as reflections of our own society, but we see bees singly, flying from blossom to blossom, rather than en masse, and the workings of the hive are not visible to most of us. Ants, however, stream across our driveways in glistening black ribbons. They seethe through our cereal boxes and bear crumbs triumphantly along edge of the shelf and out the door. With a few moments of casual observation, it's possible to see ants carrying their young from place to place, whereas no one other than beekeepers (and entomologists) ever sees much in the way of bee family life. And they walk, rather than fly, making them a little easier, perhaps, to identify with.

Like many of the other social insects, ants seem to share food unhesitatingly, and they work tirelessly for their colony, as Maeterlinck notes above. Maeterlinck, a Belgian playwright and poet who won the 1911 Nobel Prize for literature, was particularly taken by the ants' practice of passing droplets of food from one individual to another, called trophyllaxis, a behavior not seen in most nonsocial insects. For reasons that are not altogether clear, at least to me, he seemed to think that this behavior was intensely pleasurable for the ants, somehow compensating the workers for their lack of sexual activity by a near-orgasmic sensation when the food was transferred.

Solomon, of course, enjoined us to "Go to the ant, thou sluggard; consider her ways, and be wise." As historian Charlotte Sleigh writes in her entertaining book Ant, "The ant's supposed virtues of industry, prudence and mutual aid were extolled by a great number of people." The diligent ants that labor and save for the winter provide a smug contrast to the grasshopper that fritters the time away in a host of moralistic fables. A fair share of people probably sympathize with the indolent pleasure-seeking half of the story more than with the ants themselves, but the object lesson is clear: hard work is virtuous and will be rewarded. The Victorians seemed especially partial to the idealization of the ants' nobility and stressed the idyllic domestic activity supposedly taking place in the ant nest.

But ants also have a dark side that is obvious to even a casual observer. Naturalists since ancient times noted the apparent wars that raged between ants of different colors, with battles that went on for hours. Army ants are so named for their rampaging behavior. And as Sleigh points out, "The commonly known fact that ants engage in warfare has given them a particular edginess in times of human conflict." And a handful of species of ants exhibit a behavior that is strikingly similar to slavery in humans: one kind of ant will make raids on a colony of another species and steal its young workers, to be reared in the nest of the invaders and put to work for the rest of their lives. Charles Darwin described part of such a raid in The Origin of Species, musing on "the wonderful instincts of making slaves." According to Bertrand Russell, "Ants and savages put strangers to death," although plenty of familial slaughter takes place as well. So-called killer bees are a close second, with plenty of media hype about enraged swarms pursuing hapless passersby. The pursuit is obvious (though the actual numbers of people attacked and injured is often exaggerated), and people stand at the ready to attribute rage and bloodlust to the pursuers.

Hostility has also been linked with insects in novel ways. A now-defunct band from Houston, Texas, was called "Insect Warfare." Its album World Extermination is being re-released by the deliciously named Earache Records, with apocalyptic cover art showing giant cockroaches, or possibly crickets (I am personally offended by this), fleeing a skeleton looming over a decaying cityscape. Humans are nowhere in sight.

So which is it? Do ant wars and slave-taking raids mean that these, and perhaps the other social insects, are particularly aggressive, and hence that warmongering is natural in animals? Does the devotion and self-sacrifice so approvingly cited by Maeterlinck prevail? A closer look reveals that the real villainy takes place much more surreptitiously, and while less full of carnage, it is far more deadly.

An Army of Savage Lace

WHEN I was a child I went through a phase in which I told people I wanted to be a myrmecologist when I grew up. Although I did indeed spend time watching the ants in our backyard, along with the other insects, I was probably driven more by smug delight at knowing that the word means someone who studies ants than by any actual career motivation. Be that as it may, when we had an assignment in third or fourth grade to read a book and report on it to the rest of the class, I chose a book on ants, and happily launched into a litany of their amazing behaviors. Ants, I proclaimed, made gardens of fungus that they harvested for food. They stored honeydew in their own massively swollen abdomens and fed it to the other workers, droplet by droplet. Not only that, I cheerfully told my classmates, who were by that point probably unnerved if they were not simply bored, but army ants could swarm through entire jungle villages, consuming every living thing they encountered by tearing it to pieces. Cows, pigs, chickens, and people, all were subject to the advancing hordes with their bladed jaws. If one were caught unawares by the oncoming troops, the only recourse was to set one's bedposts in saucers of kerosene, get under the covers, and pray the ants didn't find a way to drop down onto the bed from the ceiling. I was slightly hampered in my explanation of this dire state of affairs by my uncertainty of exactly what kerosene was, but I was sure that if I lived in an area frequented by army ants, I would be able to procure some.

Here my teacher intervened. Surely, she said gently, you are exaggerating. Ants couldn't possibly be that destructive. Perhaps they attacked the animals near the area, or got into a hut or two, but this scale of devastation and carnage seemed a bit much for such tiny creatures.

I dug in my heels. No, I insisted, the book had said (and hence I unswervingly believed) that the ants could tear apart a person in minutes. It wasn't just the odd hen or two, it was An Entire Village. I honestly don't remember exactly how or if this disagreement was resolved, or if my grade on the book report was reduced due to my teacher's suspicion of hyperbole, but I remain convinced that people don't fully appreciate the wonders of ants, perhaps because they refuse to believe the extraordinary things ants can do.

Army ants in particular inspire superlatives. They were described in detail in the late nineteenth and early twentieth centuries by legendary scientists such as William Morton Wheeler and Theodore Schneirla; the latter published a paper in 1934 titled "Raiding and Other Outstanding Phenomena in the Behavior of Army Ants," in the prestigious Proceedings of the National Academy of Sciences, which was, interestingly, placed into the "Psychology" section of the journal, as if it had more relevance to the workings of the mind than to zoology. Wheeler referred to army ants as "filled with an insatiable carnivorous appetite and a longing for perennial migrations, accompanied by a motley host of weird myrmecophilous camp-followers," and Hölldobler and Wilson call them "the unstoppable, superorganismic grim reapers of the tropical forest."

Army ants occur in several parts of the world, including the southern and western United States, but have been best studied in the New World tropics. They lack a fixed nest site, instead creating bivouacs, football-shaped masses that can be nearly a yard wide with anywhere from ten thousand to seventy thousand workers surrounding the queen and larvae, depending on the species. Hölldobler and Wilson estimate that the bivouac contains "a kilogram of ant flesh." The ants link their limbs and jaws to form their shelter, making a kind of savage yet delicate lacework of individuals that supports layers upon layers of brownish bodies. Just after dawn breaks, the bivouac seethes and breaks apart, sending out lines of ants in many directions.

The lines include army ant workers of several shapes and sizes, all female, of course, despite my students' disbelief. The small and medium-sized individuals lay down an odor trail as they walk down the middle of the track, while the larger soldier caste ants, with their scimitar-shaped jaws, lumber alongside. Workers are about the size of many North American ants, perhaps as long as a grain of rice, but the soldiers are three times their size, about as long as a kidney bean. The streams of advancing ants have no leader; individuals hustle back and forth at the edges of the swarm, altering direction as they encounter prey.

As my childhood reading experience suggested, army ants and their relatives the African driver ants are merciless when they encounter an animal in their path. People and other vertebrates such as birds or squirrels, however, are usually able to evade the advancing columns unless they are injured or otherwise prevented from moving out of the way, which vindicates at least some of my teacher's skepticism, though the ants certainly could overpower an immobile human being. Insects, spiders, and other invertebrates usually cannot escape so easily and are surrounded by the eager jaws of the horde. Hundreds of ants sink their mandibles into the prey, their grip so strong that if the ant is torn away, its jaws remain imbedded in the flesh of its victim. Anecdotally, at least, this powerful grasp has led to their use as sutures by the Masai of Africa, who induce the ants to latch onto either side of a wound with their jaws, holding it shut even after the body of the ant is discarded. (I was once asked how the ant jaws are removed once they have served their purpose, and I don't know the answer, save that the process might put that "ouch" at the tug of a Band-Aid to shame.) Small animals are borne away intact, while larger victims such as tarantulas or grasshoppers, or the occasional unlucky mouse or even deer, are efficiently butchered and carried off in chunks that can be managed by one of the medium-sized workers.

The intimidating-looking jaws of the soldiers, like many weapons, are not actually useful for practical tasks, and so all of the work of hauling food back and forth is done by the more modestly equipped smaller workers. Sometimes a group of such ants collaborates to transport a larger prey item, balancing it expertly among themselves so that the load can be carried by the minimum number of individuals needed. Schneirla reported that the entire operation is accompanied by the sound of thousands of tiny exoskeletons tapping against the dry leaves of the forest floor, a sound that according to Hölldobler and Wilson "beats on the ears of an observer until it acquires a distinctive meaning almost as the collective death rattle of the countless victims."

The naturalist and author William Beebe once observed a bivouac of army ants that had taken temporary residence in the outhouse near his laboratory in Guyana. Transfixed by the sight, he determined to observe the insects as they set up their encampment. He first noted the odor of the group, which was "sometimes subtle, again wafted in strong successive waves. It was musty, like something sweet which had begun to mold; not unpleasant, but very difficult to describe." He was deterred from further rumination by "a dozen ants [that] had lost no time in ascending my shoes, and, as if at a preconcerted signal, all simultaneously sank their jaws into my person." Beebe proceeded to take a chair into the outhouse and use the traditional technique of placing each of its legs into a can of disinfectant; he then rushed over to the chair, hung a bag of equipment over the back, and pulled his legs onto the seat. "Close to my face were the lines ascending and descending, while just above me were hundreds of thousands, a bushel-basket of army ants, with only the strength of their thread-like legs as suspension cables. It took some time to get used to my environment, and from first to last I was never wholly relaxed, or quite unconscious of what would happen if a chair-leg broke, or a bamboo fell across the outhouse."

This rhythm of activity, with the ants alternating between going out on raids and forming bivouacs, continues for months. In the Central American army ants that Schneirla studied, the ants sometimes will form a new bivouac every evening and sometimes settle in their self-manufactured housing for a few weeks at a time. Because army ants have no permanent nest site, they do not reproduce as many other ants do, with the release of winged males and females that mate in flying swarms before the newly inseminated queens found new colonies. Instead, at least in the species of army ants that have been the best studied, although both fertile males and females are produced at a certain time of year, only the males can fly. They attempt to join the bivouacs of another colony. At the next raiding period, a group of workers stays with the old queen and moves to a new bivouac, while one of the virgin queens is surrounded by another set of workers and travels to a different site, where she mates with one of the males that had flown into the colony. In some species of army ants the young queen mates with several males in succession, in others with only one. The male ants, like the drones of honeybees and many other social insects, die soon after mating, assuming they get a chance to mate at all. The rest of the handful of reproductive females are abandoned to the company of a small group of workers, but they do not hunt for food, and eventually all die, leaving their mother and sister to carry on in their place.

Army ant queens themselves have dramatically episodic reproductive lives; instead of monotonously laying egg after egg, day after day, for their entire adult life span, the queen's ovaries will develop only while the colony is in their more long-term bivouac. At that point, rapidly making up for lost time, her abdomen distends and she lays up to three hundred thousand eggs in one fell swoop. When the workers that are the product of her labor appear, they seem to perk up the energy levels in the group, and after a while the entire colony starts the migratory phase again, as the queen's labor subsides and she is shielded from harm as the columns of scissor-jawed daughters resume their activity.

The term army ant is not a truly scientific designation; it is used to describe those species of ants that exhibit both incessant migration of the entire colony and coordinated group hunting, including the raids by large numbers of individuals and the carrying of prey back to the nest. Sometimes terms such as legionary or driver ants are used, but virtually everyone who has written about them describes the ants' behavior in the most aggressive terms. While Hölldobler and Wilson, in their monumental tome The Ants, concede, "Yet driver ants are not really the terror of the jungle as popularly conceived," they devote much of their chapter on army ants to the same bloodthirsty details relished by Beebe and other naturalists. Even Maeterlinck, with his enthusiasm for the social virtues exhibited by ants in general and for their food-sharing proclivities in particular, sorrowfully notes, "Even in the ants this universal charity, this perpetual communion, does not prevent wars: though the wars of the ants are less frequent and less cruel than is generally believed." He also saw—or thought he did—a perfect mirror of human foibles: "Every kind of warfare known to ourselves will be found in the world of the ants; open warfare, overwhelming assaults, levies en masse, wars of ambush and surprise and surreptitious infiltration, implacable wars of extermination, incoherent and nerveless campaigns, sieges and investments as wisely ordered as our own, magnificent defenses, furious assaults, desperate sorties, bewildered retreats, strategic withdrawals, and sometimes, though very rarely, brawls between allies, and so forth."

In the midst of this veritable battalion of military metaphors, it might be worth stepping back and considering the actual goal of the army ants themselves. Those forms of warfare Maeterlinck exhaustively details might be better replaced by a far humbler list: going to the grocery store, harvesting vegetables in the garden, or hooking fish in a river. The ants are an army without an enemy. They are predators, and predation is not waging war, it is acquiring food. We seem to like linking hunting live prey with being aggressive, and we seem to especially like linking it to manliness. Predatory animals such as hawks or lions are often depicted as being exceptionally fierce, and so we transfer that to the ants, struggling with the grasshoppers that are elephant sized to them. But the truth is that hunting is a more widespread and less glamorous profession than it is sometimes made out to be. We tend to think of predators as animals that subdue large, warm-blooded prey, usually after a heroic struggle, but there is no a priori reason for us to dismiss animals that catch and kill more modest fare, for example, the ladybug gleaning aphids from a rosebush, or a chickadee nipping an inchworm off of a leaf. Some biologists refer to any food item that comes in a discrete chunk, as opposed to the unending sea of grass in a field, as "prey," and talk about animals such as the seed-eating kangaroo rats as "seed predators." Even if that is going a bit too far for some, is it any less savage to bite a worm than a weasel? Why does a hawk swooping down on a mouse seem more aggressive than a songbird snapping its bill against the hard shell of a beetle?

It's true that hunting, for both humans and other animals, can be risky, and facing up to prey that is bigger than you are and that has sharp teeth or claws can take courage. And in some cultures hunting, because it requires that bravery, is used as a test of manhood. But none of this applies to the ants, not least because, of course, all of the workers—even the ones with the big, bladed jaws—are female and won't get any more kudos from the colony no matter how many tarantulas or pythons they bring down. That they all eat meat doesn't make them any more vicious than the more peaceably named harvester ants that lug heavy seeds back to their nests.

Maybe the emphasis on warfare and aggression in army ants is an effort to counter that idealization of the ants' social harmony that used to be so prevalent. After all, Solomon wanted us as sluggards to look to the ant for inspiration to hard work; he didn't ask us as wimps to look to her for inspiration to violence. Sleigh discusses a book on "natural history and animal morals" published in 1851 by the Society for the Promotion of Christian Knowledge, which is still active. In it, ants are held up as models of prudence and industry from which humans are exhorted to learn. Ant and bee societies were embraced by the natural theologians of the nineteenth century, and their cooperative altruism was used as a model for social organizations that supported the poor. Later, socialists claimed that ants were exemplars of comradely sharing, though they must not have looked too closely at that turgid-bellied queen.

As my childhood flirtation with a career in myrmecology suggests, I am hardly immune to the drama of the ants' activities. But all of this symbolism, and the focus on aggression, runs the risk of seeing the ants as miniature soldiers instead of the skillful predators they are. What's really interesting about army ants isn't whether they show "incoherent and nerveless campaigns" as opposed to "sieges and investments as wisely ordered as our own." It's how and why that one virgin queen is singled out and sequestered from the rest in the colony. (Is she older? Younger? Or does one live and the others die at random? We still don't know.) It's how the colony's internal clock tells it when to migrate and when to make camp, given that research has shown the ants are not simply driven by hunger. Day length may give a proximate cue, while colony size also plays a role. It's how those massive colonies in Africa and South America differ from their less conspicuous counterparts in Texas or Alabama.

Army ants could even serve a more prosaic function, and one potentially useful to humans. Adrian Smith and Kevin Haight from Arizona State University pointed out that because other ant colonies tend to flee with their brood, evacuating the entire colony, queen and all, when army ants approach, researchers attempting to collect the prey species could exploit this behavior and save themselves time and trouble. They cheerfully—and in my opinion, just a tad cold-bloodedly—suggest that fellow scientists use a small batch of army ants to rout a desired species from their subterranean chambers, rather like tiny terriers sent after rabbits in a burrow, saving hours of often back-breaking labor excavating the nest. Their paper even includes links to videos that demonstrate, in eerily infomercial fashion, exactly how nifty and efficient this technique can be. It sounds like a great idea. But somehow "terrier ants" doesn't have much zing.

Adopting the Enemy

IF THE army ants are more hunters stocking their family larder than noble soldiers proving their mettle, what about the slave-making ants with their "wonderful" instinct, as noted by Darwin? The wars, or raids, that these ants undertake are not about getting food, at least not directly. A slave-maker colony is started when an inseminated queen of one species enters the nest of another, kills or expels the resident queen or queens, and begins to lay eggs of her own kind. Her children are then reared by the host species, which accepts them as if they were nest mates. To replenish the host workers, the slave-maker species sets out on periodic expeditions to snatch the larvae and pupae from another host colony, bearing them back to the slave-maker nest to mature and act as normal workers for their hosts. About fifty of the eleven thousand known ant species behave in this manner, with some capable of living on their own and others so specialized that they cannot even feed themselves without the help of their captives.

Despite their rarity, the slave-making ants have attracted a great deal of human attention. Charlotte Sleigh documents the fascination of nineteenth-century observers with the slave-making ants, many of whom were quite overt in their analogy with the human slave trade of the time. Perhaps surprisingly, many naturalists and authors decried, not the practice of exploiting the labor of others, but the "degeneracy" of the slave makers themselves. In characteristically opinionated prose, Maeterlinck disapprovingly notes that the slave makers "cannot eat without assistance, for they cannot take any nourishment save from the mouths of their servants. They are as little capable of rearing their young as of building or repairing their nest. In the depths of their lair they pass their time in besotted idleness, rousing themselves only in order to polish their armor, or to pester their slaves for a mouthful of honey. Without their servants these magnificent warriors, with their bronze armor, these superb shock-battalions, these irresistible veterans of great campaigns, are as impotent, as utterly helpless as so many suckling infants." In his 1954 book Ways of the Ant, John Crompton was similarly censorious: "Even if their slaves do not desert them, mental and physical decay will in itself and in its own time exterminate them. There must be many species of slave-making ants that have died out for this reason."

Although his language is rather histrionic, Maeterlinck was scientifically accurate, at least with regard to the obligate slave-making ants; in the early 1800s the great entomologist Pierre Huber had placed a group of ants of one of the slave-maker species in a kind of ant farm, along with honey to eat and some of their own pupae and larvae. Within a few days half had already died and the remainder were on the brink of starvation.

The raids themselves can be quite dramatic to witness. The species whose brood is being taken generally attempt to drag the pale, helpless larvae and pupae away from the nest, only to be pursued by the workers of the host ant species. Raids seem to be confined to certain times of the year, and at least some of the ants studied in this regard use cues from within the nest to decide when to begin raiding behavior. Slave making in ants is confined to temperate regions of the world, and scientists have suggested that the absence of seasons in the tropics explains the lack of raiding and, hence, slave-making behavior, since there is no internal signal that indicates when pupae can reliably be abducted from their nests. Some species also raid at certain times of day. Joan Herbers, a scientist at Ohio State University and an authority on such ants, says that when she was at Colorado State University her students knew exactly when to go looking for raids: "Jeremy [her student] could head to the hills of Colorado around 10 in the morning, knowing he would be done with fieldwork by 3 or 4." Others are not so reliable: "We have set up many experiments in the lab; some days they raid and other days they don't. Some days they raid fiercely and other days the raids fade away. Sometimes it takes an hour and other times 6–8. It's a pain, and has frustrated several journalists who have visited my lab."

In addition to studying the ants as a scientist, Herbers has questioned the wisdom and accuracy of the name slave-maker ants. She is not alone in this regard; Hölldobler and Wilson point out, "It is traditional to use the expression slavery for the exploitation of one species by another. In the human sense this is not slavery but more akin to the forcible domestication of dogs and cattle by humans." They go on to detail situations in which ants use the labor of others from the same species, but the term slavery is clearly limited in its applicability. Some entomologists use the more technical jargon term dulosis to refer to the process, whether within or across species, but most scientific journals still call it slave making.

Herbers is not just concerned about the use of the word slavery by scientists. She questions its suitability given its obvious connotations of human activity. At public lectures, she often is asked about the parallel between ant and human slavery, a parallel she always decries. She has come to the conclusion that we would all be better off abandoning the metaphor and terminology entirely, because of its emotionally loaded overtones. As an alternative, Herbers proposes the term pirate ant, since human pirates also make raids and steal cargo, often killing some of the victim ship's crew. Scientists could continue to discuss raiding parties, captives, and booty, without recourse to the loaded terms that certainly bring the public up short. I am in agreement with the distaste for the word slavery in nonhumans, and use it here only when the original authors use the term, so as not to rewrite their usage.

Regardless of its social baggage, however, another problem with calling the ants slave makers is that, as with the army ants, it gives an entirely incorrect view of what the ants themselves are doing. Hölldobler and Wilson's point about domesticated animals versus forced labor from members of the same species aside, most biologists, including them, classify the behavior as a kind of parasitism. In other words, the so-called slave makers are acting like exceptionally free-roaming tapeworms. Like the tapeworm, the slave makers, at least the obligate species, make their living entirely off of another organism, the host. But instead of traveling passively from one host's intestinal tract to another via, say, a contaminated bite of meat, the ants take matters into their own six legs. The slave raids, with the excited workers rushing to and fro with their cargo of pale cocoons, are just a more visible and dramatic version of the worm in the gut ensuring it will have someone to provide it with a steady supply of meals for the foreseeable future. Even Crompton notes that "a slave-raiding expedition is not really a battle, it is a routine commercial undertaking."

Admittedly, this analogy is not perfect, and the ants are what scientists call social parasites, rather than internal ones. Cuckoos and cowbirds are the most familiar examples of such animals: the cuckoo female lays her eggs in the nest of another bird species, exploiting the parental behavior of the host, who rears a genetically unrelated chick. The hosts have, in a sense, adopted the enemy to their own advantage, gaining the labor of others at little expense. And Maeterlinck points out that the captive ants do exactly the same thing that they would be doing in their own nest, namely, feeding the workers and caring for the queen. Their lives are no harsher than they would be in their own nest, and the everyday life of any ant is pretty grim by anthropomorphic human standards at least. But those pejorative declarations about degeneracy from Crompton and Maeterlinck fit right in with this point of view. Tapeworms and many other parasitic organisms have reduced limbs, eyes, and other organs, a state of affairs that probably evolved because the appendages are unnecessary, maybe even an impediment, in the dark cozy confines of the host's gut. Crompton's prediction about the extinction of the slave makers may be off the mark, since of course parasites show no signs of going out of business. Seeing slave making as a form of parasitism gives rise to the unsettling thought that, by the same token, we are a kind of slave to our own pathogens.

Viewing the interaction as parasitic not only sidesteps the terminology melodrama, it clears the way for asking other interesting questions. Herbers and her colleagues have examined variation across the range of several species of pirate ants regarding which species they exploit, and, as with a disease-causing organism, talk about the "virulence" of different raiding species. Just as anthrax is more virulent than athlete's foot, by doing more damage to its host, a more virulent social ant parasite kills a larger proportion of the adult ants at the nest it raids.

With postdoctoral scholar Christine Johnson, Herbers introduced two different slave-making species that parasitize the same host species into outdoor enclosures in a field in Ohio. The enclosures had one or the other slave-making species or both at the same time, along with the host species. The researchers then waited to see how the host species did, predicting that the presence of both slave-maker species would be the biggest burden on the host ants. Much to their surprise, the host colonies did better when both parasite species were present together. Johnson and Herbers speculated that the two types of slave makers might have competed with each other, to the detriment of both, leaving the host ants to prosper unmolested. This kind of complicated interaction among several species is becoming increasingly interesting to scientists, since it suggests that we need to look at more than just one species at a time to understand an animal's ecology. The researchers concluded that variation in the abundance of slave makers could affect "hot and cold spots" of ant abundance in the forests where the ants occur.

Just such geographic variability in ants was the subject of a study by Susanne Foitzik, now at Regensburg University in Germany but formerly another postdoctoral scholar working in Herbers's laboratory. Foitzik and others have recognized that the ants are a good way to study ways that a host and parasite can influence the evolution of each other, in what's called a coevolutionary arms race. After all, one wouldn't expect the host, or exploited species, to just sit back and take it—for example, we evolved an entire immune system to resist the attacks of viruses and bacteria. Other kinds of hosts of social parasites show varying degrees of defenses against the parasite; some cuckoo and cowbird hosts recognize and reject the interloper's eggs, while others seem to be oblivious to the gigantic size of the parasite chick relative to their own offspring and valiantly stuff food into the cuckoo chick's gaping maw at the expense of their own reproduction.

Foitzik and her coworkers looked at the ways that the slave, or host, species varied in its ability to defend itself against the slave makers. They were interested in whether the defense mechanisms were the same in different places, regardless of the intensity of the raids by the slave makers, or whether each pair of host and parasite populations evolves a unique way of interacting, with a new arms race in each locale. They compared colonies of a raiding species and its victims in the Huyck Preserve in New York state with those in West Virginia. More and larger colonies of the slave-making species occur in New York, which should make the pressure on the host species more severe, since they are being raided more frequently. The slave-making ants in turn can kill the queens of their hosts without too many repercussions, since many colonies of potential victims are also present.

The scientists found that the coevolution between host and parasite was in fact different in the different places; in New York, a guard ant was more likely to be found protecting the host nest entrance, and in turn the New York slave-making ants took more of the brood from the nests they raided. The host defenses were also more aggressive to the initial scouts sent out by the raiding parties. "Ironically," write the researchers, "these host ants are probably killed by enslaved conspecifics [members of the same species] that accompany ... workers on raids, rather than by the slave-makers themselves." The defenses, however, weren't unique to a particular set of nests, supporting the idea that universal defense mechanisms evolve throughout the population.

The idea that the hosts could defend themselves against the raiders wasn't given much credence until recently, and it's tempting to speculate that the lack of exploration of the idea came from people clinging a little too tightly to that slavery analogy. Slave rebellions are risky and scarce. But it's commonplace to imagine a host and parasite, for example, the worm inside the gut of a mouse, continually evolving ways to attack or defend against each other.

Whether you think of it as piracy, parasitism, or slavery, capturing live individuals of another species and benefiting from their labor requires a complicated set of behaviors. How did such a practice evolve? Charles Darwin offered the first potential explanation in The Origin of Species, proposing that the ancestral slave makers first took the pupae as prey. When some of the pupae accidentally escaped detection back in the host nest and became adult workers, they were not perceived to be foreigners and, hence, began doing their normal ant activities, which made the colony as a whole prosper.

Another possible route to the evolution of piracy is via the territorial battles that commonly take place between colonies of the same species. Ants and other social insects usually have very strong loyalties to their own colony and will attack intruders that smell like they come from a foreign nest. If a new colony is established too near an existing colony, fights between the workers of the two groups can result, and several scientists have suggested that this generally pugnacious behavior could have evolved to be directed at ants of other species as well. If the two species were closely related, and hence shared a more recent common ancestor, the likelihood of them also becoming tolerant of a captured pupa or larva is increased, because the captive would smell more familiar.

Jeannette Beibl, a researcher at Regensburg along with Foitzik, examined the DNA of numerous slave-making species. They and colleagues R. J. Stuart and J. Heinze determined that the practice evolved independently several times in different groups of ants, some relatively recently, at least by evolutionary standards. This variation suggests that different selection pressures might have caused slave making to evolve in the different species.

Six-Legged Constables

IF THE army ants aren't a real fighting force and the slave makers are just parasites with an uncanny resemblance to their hosts, do treachery and aggression exist at all for the social insects? The answer is a resounding yes. The carnage is subtle, but far more devastating in its after effects than even the most formidable slave-taking raid. In evolutionary terms, loss of life is not nearly as injurious as loss of reproduction. The social insects, with their suicidal colony defense and sterile workers, have perplexed evolutionary biologists since Darwin. While biologists have mostly explained the benefits of such extreme cooperation for the individual colony members, those busy little virgin bees and ants still turn out to show some enterprising forms of rebellion.

Although worker ants, bees, and wasps cannot mate, they often possess functional ovaries and can produce their own eggs. These unfertilized eggs develop into males, because throughout this group of insects and a few others, daughters have two copies of each chromosome, like humans and other vertebrates, and develop from fertilized eggs, but sons have only the mother's genes and, in effect, have no father. (I often give my animal behavior students an exam question that asks whether it is true that a honeybee male has a grandfather but no father. The ones who get it are triumphant, often hammering the point home in far more text than necessary, while the ones who don't flounder in ever-widening circles of confusion; one ended up declaring in apparent despair, "No, every animal has a father, if they didn't have a father they wouldn't have a mother and then what would happen?")

This genetic oddity means that workers are often more closely related to each other than they are to their own offspring, although the exact proportion of shared genes varies depending on how many males have mated with the queen. The real genetic payoff comes, as I pointed out in an earlier chapter, not from the workers helping to rear their sterile sisters, but from production of the future reproductives, the queens and drones that will leave the colony and found a nest of their own.

Under some circumstances, therefore, it is beneficial to an individual worker to lay some eggs that will become male reproductives. But the other workers would pass on more of their genes by investing in their brothers, the sons of the queen, rather than their nephews, the sons of their sisters. So you might expect that workers would sabotage each others' efforts to slip a few of their own eggs into the hive. Indeed, Francis Ratnieks and Kirk Visscher documented exactly such behavior, termed worker policing, in honeybees. The bees are able to tell which eggs are laid by the queen and which by their sister workers and will remove the latter and prevent them from developing. Visscher and Reuven Dukas discovered that the workers can even detect the degree of ovarian development in their sisters and act more aggressively to the ones that are on the verge of producing their own eggs.

Ratnieks, along with Tom Wenseleers, took the idea of worker policing further. They pointed out that the better the workers are at stopping each other's attempts at reproduction, the more likely it is for workers to give up, in effect, and simply put all their efforts into the queen's offspring rather than try to produce their own. To test this idea, the scientists compared the proportion of egg-laying workers in ten species of wasps and the honeybee; the insects vary in the effectiveness of worker policing in the nest. As they predicted, workers from species in which the policing is stringent are much less likely to try to lay their own eggs in the first place. The scientists conclude that the insects "provide evidence for something that has proved notoriously hard to demonstrate in human society: that better law enforcement can lead to fewer individuals behaving antisocially."

Ratnieks and Wenseleers also noted that the workers can control each others' reproduction in a different way, by regulating which female eggs end up as queens and which as workers. In many, though not all, social insects, this caste difference is determined during development, with future honeybee queens, for example, placed in larger cells than the plebian workers and fed more of a special substance called royal jelly that jump-starts their growth. Reproducing oneself, rather than caring for the young of others, is an attractive evolutionary prospect, but developing into a queen is only part of the process. It's rather like becoming a movie star: being stunningly beautiful, while essential, is no guarantee of red carpet status. Only a tiny fraction of the queens produced will actually make it to the Oscar-winning equivalent of starting their own hive. But it's not good for the colony if too many individuals become queens, because queens don't do any of the foraging, cleaning, or other mundane tasks of daily life. And yet, as with eager celebrity wannabes, the starlets rush to audition. As Ratnieks and Wenseleers put it, "The lottery to reproduce is so attractive that many more enter than could possibly win the prize of heading a new colony." Policing by the other workers prevents too many queens from being reared, because the larger cells in the comb for rearing queens are strictly limited.

A tropical stingless bee called Melipona provides an elegant illustration of the scope and limitation of policing. Unlike honeybees, which are reared in wax cells that are open at the top so that the workers can feed the larvae a bit at a time over their development, the stingless bee queens are about the same size as workers and are reared in sealed cells, each of which contains its own ration of food. The female Melipona thus develops into an adult without interference from other bees and can become either a queen or a worker. As a result, up to 20 percent of females are aspiring queens. But grim reality sets in once they emerge from their virginal chambers: lack of policing beforehand means that many of the new queens are set upon by the workers and torn limb from limb. The policing ameliorates this carnage by preventing too many queens from being produced in the first place.

Punishment of cheaters who try to reproduce on their own in a social insect colony is not confined to bees. Ordinarily, only queen ants produce a particular chemical on their body's surface to indicate their reproductive status. But if a worker's ovaries develop and she begins to lay eggs, the other workers detect the same odor on her body and attack their sister. Adrian Smith, Bert Hölldobler, and Jurgen Liebig painted workers with the telltale compound and induced the aggression, showing that the odor is indeed the trigger for detection of cheaters. In a colony with its queen removed, however, the newly reproductive workers are left alone.

Ratnieks and Wenseleers ask, "Can humans learn anything from insect policing? The principal lesson seems to be that policing is a common feature of social life and helps to resolve the conflicts caused by the transition from individuals to societies.... Po-licing in human societies has been used by repressive regimes to sustain inequalities, as demonstrated by the negative connotation of the phrase 'Police State.' But a human society in which policing is used to promote greater equality and justice may not be an unattractive prospect." Of course, the conflict between the good of society and individual freedom is an old one, and not likely to be settled by observations from the beehive. My take on the sinister world of Big Sister is that such behavior is far more deadly than the army ants swarming over every living thing in their path. Who needs nuclear weapons?