According to Thor Hanson’s Buzz, the relationship between bees and the human lineage goes back three million years, to a time when our ancestors shared the African savannah with a small, brownish, robin-sized bird—the first honeyguide. Honeyguides are very good at locating beehives, but they are unable to break into them to feed on the bee larvae and beeswax they eat. So they recruit humans to help, attracting them with a call and leading them to the hive. In return for the service, Africans leave a small gift of honey and wax: not enough that the bird is uninterested in locating another hive, but sufficient to make it feel that its efforts have been worthwhile. Honeyguides may have been critical to our evolution: today, honey contributes about 15 percent of the calories consumed by the Hadza people—Africa’s last hunter-gatherers—and because brains run on glucose, honey located by honeyguides may have helped increase our brain size, and thus intelligence.
Bees evolved from wasp ancestors around 100 million years ago. Most wasps are sleek carnivores, but bees are flower-loving, long-haired, and often social vegetarians (the branched hairs that cover their bodies trap pollen, which, along with nectar, is their principal source of food). Their shift to a vegetarian diet had a profound effect on the evolution of flowering plants. If we want to know what a world without bees looks like, Hanson writes, we should visit the bee-less island of Juan Fernández off the coast of Chile, where, despite varied vegetation, almost all flowers are small, white, and inconspicuous. But it is not just gloriously colored flowers that we owe to bees, for many of our crops rely on them for pollination. Both our world and our brains, it seems, have been profoundly shaped by bees.
There are around 20,000 bee species, classified into seven families. The most familiar are the apids, including bumblebees, carpenter bees, and honeybees. The most primitive bees, largely restricted to Australia, are classified into two families that only experts would recognize. Mining bees, which dig nest tunnels nearly ten feet deep and inhabit arid regions, represent another family; oil-collecting bees and a family including leafcutter bees and mason bees make up two more. Sweat bees comprise the final group. In addition to collecting pollen and nectar from flowers, they drink mammals’ sweat for its moisture and salts: as thousands of tiny bee tongues lick deep inside a person’s ears, nose, and other sensitive parts, they can inflict maddening torture; if brushed away they deliver a sting like an electric shock.
Around one fifth of all bee species are parasites on other bees, prompting some bee researchers to recognize parasitism as one of the major evolutionary adaptations of the lineage. The parasites survive either by stealing honey or wax from other bees, or by tricking them into raising their young, much like cuckoos do with birds. And not all bees are social: many are solitary or are flexible in their degree of sociality, depending on temperature or resource availability.
For all their evolutionary diversity and behavioral flexibility, bees are in trouble. In the fall of 2006, honeybee hives across the US “started winking out en masse,” Hanson writes. Apparently healthy bees that set out on foraging trips never returned, leaving behind neglected combs full of honey and broods that became infected with bacteria and other pathogens. Named Colony Collapse Disorder (and colloquially “the Beepocalypse”), the phenomenon triggered the biggest bee research project in history. To date, no single cause has been identified, but several factors, parsed by researchers as “the four Ps”—parasites, poor nutrition, pesticides, and pathogens—have combined to make bees vulnerable.
Franklin’s bumblebee was once found in southwestern Oregon and California, but it hasn’t been seen since 2006. Robbin Thorp, who observed the species before its disappearance, is employed by the US Forest Service to search for survivors. He acknowledges that his work may be futile and the species extinct, theorizing that it fell victim to a pathogen known as Nosema bombi, which reached the US when bumblebees raised in Belgium were imported to pollinate tomatoes in greenhouses. Nosema prevents male bumblebees from having sex. As their bodies fill with Nosema spores they become so heavy that they can’t fly, and their abdomens swell so much that they can’t touch a female in the right spot to copulate. “When that happens, you’re done,” says research entomologist Jamie Strange. “In a couple of generations, it all falls apart.”
Among the most damaging of parasites to honeybees is the Varroa mite, a vampire that debilitates them by sucking their blood. Originally from Southeast Asia, it has infected bees everywhere except Australia, leaving colonies vulnerable to adverse weather and poor nutrition. Incidentally, we often misunderstand what’s needed to keep a bee well fed. “People look across a park or a golf course and think it’s green and lush, but to a bee it’s like a desert or a petrified forest,” says one researcher. As agriculture intensifies, even flowering weeds—an essential part of a bee’s diet—are becoming scarce.
It is well known that bees pollinate many of our crops, yet somehow that knowledge coexists with a willingness to spend over $65 billion per year on insecticides. These chemicals are having a catastrophic impact on them. Unlike insect pests, which quickly become immune to pesticides, bees remain vulnerable. This may be because most pests have had to cope with plant defenses for millions of years. But the plants want bees to visit their flowers, so they don’t chemically defend their nectar or pollen, leaving bees with no experience of chemical defenses. As Hanson puts it, “For the crop eaters, pesticides amount to a familiar—and usually temporary—chemical setback. For bees they’re just a poison.”
Research has revealed the astonishing persistence of chemicals, including pesticides, in the environment. Chemical analyses of pollen, honey, wax, and bees themselves reveal traces of 118 different pesticides, some of which haven’t been used for decades. And the chemicals synergize: some fungicides, for example, can make some insecticides 1,100 times more potent. China’s Maoxian Valley, which has long been renowned for its apple orchards, offers a sober warning of what happens when bees disappear. Beginning in the 1990s, excessive and reckless pesticide use, combined with poor bee nutrition and a lack of nesting spaces, caused both honeybees and wild bees to vanish. Faced with crop failure, orchardists employed thousands of seasonal workers armed with long sticks topped with chicken feathers to pollinate the apple blossoms. But even the most skilled worker could pollinate no more than ten trees per day. Faced with excessive costs, the industry collapsed, and today the only orchards remaining in the valley are a few adjacent to forests, from which wild bees can visit and pollinate the blossoms.
In the spring of 1868, when John Muir made his first visit to California’s Central Valley, he was filled with wonder, describing it as “the best of all the bee-lands of the world”: “One smooth, continuous bed of honey-bloom, so marvellously rich that, in walking from one end of it to the other, a distance of more than four hundred miles, your feet would press more than a hundred flowers at every step.” Today the great bee pasture is gone, and in its place is a vast plantation where almond trees grow, supplying 81 percent of the world’s crop. For three weeks of the year, almond blossoms offer bees plenty to eat, but because almond trees must grow on bare ground if the crop is to be mechanically harvested, for forty-nine weeks of the year the plantations are bee deserts.
Like the apple growers in the Maoxian Valley, California’s almond growers faced a crisis as bees declined. Colony Collapse Disorder was making it prohibitively expensive for them to bring domestic bees to their crops, and the wild bees were mostly gone. But the growers are now being helped by the Xerces Society, the only major nonprofit in North America devoted to saving invertebrates. Ditches, roadsides, and other areas not used for almond production are being restored to wildflower meadows, in which not only bees but other wildlife is thriving. So popular is the project with growers that even a farm owned by an international agribusiness conglomerate based in Singapore has joined in. Yet such is the extent of the Beepocalypse that the work of the Xerces Society in California’s Central Valley is nought but a tiny ray of hope in a world facing a full-blown bee crisis. Only a major reorganization of agriculture, so that biodiversity conservation on croplands becomes a reality, can turn that around.
The social insects—bees, ants, and termites—have inspired us since at least biblical times: in them we see a zeal for work, a wisdom in providing for the future, and a sense of order that is often lamentably lacking in our societies. But as Lisa Margonelli so elegantly demonstrates in Underbug, when we look at social insects, all too often we see only what we want to see. William Wheeler, an American entomologist who coined the term “superorganism,” offers a cautionary tale in this regard. In 1919 he penned a comic speech from the perspective of a termite king called Wee-Wee, in which the monarch describes a termite utopia inhabited by a “physically and mentally perfect race.” This perfect society, however, has been created by eliminating old, unproductive, or unfit individuals by gassing them with hydrocyanic acid. By the 1930s hydrocyanic acid was known as Zyklon B, and it was used during World War II by the Nazis to murder millions of individuals whom they had decided were “unworthy of life.”
A very different view of termite society was produced by the South African journalist, poet, and lawyer Eugène Marais. After his wife died in 1905, he wandered into the veldt, where he took morphine and studied termites. His Soul of the White Ant, which Margonelli describes as “part close observation, part poetic riddle, and part thumbnail guide to the universe,” is one of the greatest nature books ever written.
Termites are very different from other social insects like ants and bees. They are specialized cockroaches that have become social and miniaturized, and they share a complex ecosystem of gut microbes that enable them to break down cellulose. These microbes are constantly shared between individual termites through a practice known as “trophallaxis,” which involves sharing food mouth-to-mouth and licking each other’s anuses. With an eye to the human love of sharing food, Wheeler described trophallaxis as, in Margonelli’s words, “the superglue of societies both insect and human.” For termites, however, trophallaxis leads to the creation of a colony-wide biodigester that constitutes a shared stomach, just as the structural elements of the termite mound constitute a shared integument for the individuals inside.
Margonelli’s quest revolves around understanding two important aspects of termite biology: their social organization and their astonishing gut flora. Her tale begins in the Arizona desert, where she accompanies researchers as they collect termites for classification and analysis, but it soon focuses on two laboratories where termite behavior and digestion are being studied. Both of the projects she documents, incidentally, are heavily funded by the US military.
When Margonelli first meets the researchers at the Joint BioEnergy Institute (JBEI) in Emeryville, California, they are working to produce fuel from plant matter by digesting cellulose using microbes found in termite guts. Their goal is to produce biofuel at a price that is competitive with gasoline derived from fossil fuels. Their approach involves sequencing DNA derived from termite gut extract, a task at which they are so successful that they soon become overwhelmed with data. By the time Margonelli completed the research for her book, the team has reduced the cost of their biofuel from around $100,000 to $30 per liter. But the complexity of the microbe assemblage in the termite digestive system is so great that they are unable to scale up the process and reduce costs further.
Héctor García Martín, a Spanish physicist, is the quixotic hero of the JBEI team. He abhors the seemingly ad hoc methods used by the biologists, as well as their view that life is so complex that it cannot be reduced to simple laws. A condensed matter physicist, he wants to understand metabolism, which he describes as the big underlying system enabling life, so that he can reduce it to definable terms. Ultimately, biology defies reduction, though Martín does achieve a small victory by bringing order to the lab’s procedures and reporting methods.
The scientists investigating Margonelli’s second area of interest—termite sociality—are led by the Harvard-based roboticist Radhika Nagpal. When the group turns up at a research station in Namibia, they seem badly out of place. Tied to their computer screens, they rarely emerge to enjoy the glories of the Namibian desert, and when a local entomologist cooks them a feast of game, local sausages, and stuffed squash and calls them to the table, they don’t even look up.
Margonelli describes their research in Namibia as “incredibly strange.” In their quest to make robotic termites, they set up an experiment in which they observe real termites as they modify molded daisy shapes made of colored earth. The purpose is to enable description of termite movement in terms of “chirps.” Chirps are pulses of sound that engineers feed into “black boxes” (mechanisms whose inner workings are unknown) to observe what comes out. Margonelli describes the exercise as “turning an electronic pulse into a termite playground.” Incredibly, the researcher conducting the experiment sees the living termites as “a distraction”: “In a perfect world he would reconstruct what termites do by ignoring them entirely,” says Margonelli.
The robotics researchers imagine that termites are “‘stateless automata’—memoryless identical machines that only react,” and this is the kind of robot they are attempting to create. Yet arguably the biggest single breakthrough reported in Underbug dramatically upended this view of termites. It was made in 2013, when a member of the robotics team worked out how to track individual termites as they go about their work. Immediately, it became clear that each termite is unique: out of a group of twenty-five termites in one petri dish, for example, only two were devoted to construction (though another four helped occasionally), while nineteen “just ran around.” Far from being mindless automata, the termites “do whatever they felt like: dig, take up soil and clean the dish, sit around.”
The only way to interpret these findings, the researchers concluded, was that “the informed individuals have a purpose. They have an opinion.” Margonelli concludes that the function of “informed individuals” as leaders in animal collectives as diverse as fish, birds, and ants, not to mention some human societies, is profound. The strength of the system is that it does not depend on single leaders, yet it takes advantage of their abilities in ways that “reduce the likelihood of following a really eccentric” individual “with a bad idea, which is something humans might want to look into.”
Though they initially entirely misunderstood termites, the roboticists achieve huge success when they manufacture some tissue-box-sized robotic termites (dubbed TERMES) that cooperate to build walls from plastic blocks by following a simple set of instructions. They are the first robots ever to do this, and so signal was their achievement that in February 2014 they made the cover of the prestigious journal Science, and the robotics team was invited to demonstrate them at the annual meeting of the American Association for the Advancement of Science.
Despite their considerable achievements, the TERMES robots are far from the sophisticated swarms of miniature, insect-like automata that some roboticists think will exist in the future. Stuart Russell, a Berkeley-based roboticist, for example, thinks that the Predator drones of the future will be bee-sized and carry a one-gram charge able to puncture a human cranium—“the perfect assassin,” Margonelli says. As Margonelli contemplates the military funding of the robotics project, those future swarms of miniaturized automata begin to worry her. One night, with time on her hands, she Googles the desert in Arizona where her work on the book began and discovers that Predator drones were flying overhead as she hunted for termites. After being used for years to track and kill people in places like Afghanistan, Yemen, and Pakistan, the drones had, “without any democratic discussion,” come to the US.
Mark Hagerott, a navy captain who has served in the Persian Gulf and Afghanistan, is deeply concerned about robotic warfare. He thinks that we are about to cross a threshold beyond which human empathy will be removed from armed conflict. He spends his days traveling to conferences and warning governments that they must agree to a treaty on robots in war before they deliver “incredible power” to despots. Yet he sees the technological development of the mini-drones as unstoppable, which raises a series of enormously difficult moral choices for governments deploying the new weapons.
As humans become ever more interconnected, and ever more capable of mimicking the complex chemistry and function of insects, how will our future be influenced? Margonelli says that “right now a termite mound is a thing, a construct of fungus and termites and natural history. Someday we will live in it, with all its symbiotic by-products, its paradoxes of abundance and control, and its peculiar self-organized construction.” Despite falling far short of Marais’s The Soul of the White Ant in clarity and poetry, Underbug is an extraordinary provocation. Those willing to follow its meandering arguments may find intriguing clues to humanity’s fate.