Sixlegged Guardian Angels

Following the attacks on the World Trade Center and the Pentagon on September 11, 2001, the United States responded with a massive retaliation against Afghanistan, followed by an invasion of Iraq. Except for the names of the some of the weapon systems (such as the F/A-18 Hornet fighter aircraft, which were subject to counterattack by Stinger missiles), insects played no part in these offensive operations. Defense against terrorism, however, is another story.

To prevent future terrorist attacks, the United States developed a staggeringly complex system of technologies and bureaucracies, culminating in the creation of the Department of Homeland Security, with an annual operating budget of $40 billion. Systems for detecting explosives, chemical weapons, and biological agents became central to the government's effort. And scientists are coming to understand that no instrument is more finely attuned to the environment, and more keenly responsive to trace chemicals, than the sensory system of insects. It should not be surprising that the U.S. government is investing millions of dollars in exploiting the potential of insects as guardians of the country.1 But this is not the first venture of this sort—nearly a half century ago, military scientists pursued a similar line of research that was also driven by a sense of urgency and fear.

In June 1977, a feeble, gray-haired former professor of medicine limped across the border into West Germany as East German secret police watched.2 Adolf-Henning Frucht was a pawn in a complicated spy exchange, the political winds of the Cold War having finally blown in his favor. Ten years earlier, the professor had been on his way to attend a conference on scientific administration in Prague. Frucht had been surprised at being asked to represent his East German medical institute at the event, given that the devoted researcher had little interest in such matters.

Frucht's surprise transformed into clarity when he realized that he'd walked into a trap, its jaws formed by the two State Security officials who escorted the frail academic from the train. After months of being grilled by the East German secret police, he was tried for espionage. The life sentence that he received was arguably fair. Frucht was, in fact, a spy.

In the early 1960s, his country's Institute for Industrial Physiology had approached the professor with a tempting offer. He was asked to direct his research toward developing a new method of detecting airborne toxins. East Germany was under siege by the West, and it was considered every scientist's patriotic duty to contribute to the defense of his nation. They believed that capitalist armies were likely to use every imaginable method to crush their opponents, including nerve gases.

Frucht began to piece together a line of research with considerable promise. He knew that nerve gases had been spawned by the insecticide industry and that organophosphate weapons would poison insects as well as humans. What he needed, however, was an insect that could serve as a canary in a coal mine, that would overtly reveal its intoxication before levels of nerve gas became lethal to people. Of course, some insects sing, but cricket trills and cicada buzzes were not sufficiently reliable to serve as an early warning system. However, one insect was identified by Frucht as having a form of communication that was dependable and intimately linked to its neurophysiology: the firefly (family Lampyridae).

Frucht discovered that even minuscule doses of nerve gases impeded light production in fireflies. Indeed, the poison functioned like a dimmer switch: the insects' light diminished in proportion to the amount of organophosphate in the environment. Although he was delighted with his scientific breakthrough, his subsequent political discovery was devastating.

With his research moving decisively toward the development of a monitoring system, Frucht began to receive visits from high-ranking officials. His conversations soon made it clear that the firefly project was anything but a means of protecting his countrymen. Rather, the East German government sought out his device to protect its own troops from nerve gases that they would use during a massive offensive against western Europe. In Frucht's mind, he was being used in preparing to launch World War III.

Sickened by his government's duplicity, Frucht began passing secrets to the West in an effort to avoid an imbalance of power that would undermine the tenuous peace. Not only was Frucht's firefly project of interest to western intelligence agencies, but his research put him in the position of being acutely aware of top-secret developments in chemical warfare. His detector would be used to protect communist forces from a new V-agent, the formula of which he passed to his British and American contacts. But like Frucht, the East German secret police were masters at detection, and his treason was eventually discovered.

Rather than running a world-class research laboratory, the former professor of medicine spent his days in solitary confinement or in menial labor. The prison library provided the only refuge for the mind of the imprisoned scientist. After a decade of surviving through sheer dint of will, he was freed in a prisoner exchange and hobbled into West Germany. Although Adolf-Henning Frucht gained his freedom, the world still is not liberated from the weapons that dimmed the glow of his fireflies.

Modern militaries are fully cognizant that nerve gases may be part of enemy arsenals, and U.S. field training manuals continue to warn soldiers that when all's quiet on the front—when the crickets are silenced (and, although not mentioned, when the fireflies are darkened)—a chemical attack may be under way.3 And given the ease of acquiring organophosphates, the battlefield may not be the only setting for their use in today's world.4 Although nerve gases are near the top of the terrorists' wish list, there is a weapon of even greater concern in the post-9/11 world.

The anthrax attacks on the offices of U.S. senators and major media in the weeks after the fiery assaults on New York City and Washington, D.C., riveted the attention of the government. Developing methods to detect biological warfare agents skyrocketed to the top of national security priorities. While using fireflies to directly monitor poisonous chemicals was a clever application of insect neurology, discovering how these creatures could provide a phenomenally sensitive means of detecting microbial agents required a deep understanding of firefly physiology. Years earlier, the American space program laid the foundation for modern technologies that exploit the biochemical "fire" of these remarkable beetles (fireflies are not actually flies).

In the 1960s, scientists at the Goddard Space Flight Center became keenly interested in organisms surviving at the earth's margins as a means of gaining insight into the nature of life on other planets.5 In the heady days of the space race with the Soviets, American researchers could already imagine sending unmanned missions to Mars and beyond. But if such explorations came to pass, how would we know if there was extraterrestrial life?

NASA needed an instrument to detect living organisms, whatever their form or function. Of course, nobody knew what sort of biochemistry aliens might possess, but a reasonable starting point would be a chemical that was universal to life on earth. While deoxyribonucleic acid (DNA) was a good candidate, this molecule was enormously complex and varied in its structure. There was, however, another chemical found in every living system: adenosine triphosphate (ATP). All organisms—from bacteria and fungi to plants and animals—use ATP to store and release metabolic energy. So what the researchers needed was a simple and reliable detector of ATP. Enter the firefly—or at least the chemical pathway found in its rear end.

The bioluminescence of fireflies is the result of a series of reactions within the light organ at the tip of the insect's abdomen. There are five ingredients that, when combined, yield the chartreuse glow. The key substances are two rather cleverly named chemicals. Luciferin is the substrate, the material that generates light. Luciferase is the enzyme, the chemical that transforms luciferin from its inactive state into the light-emitting form.6 But for luciferase itself to become activated and capable of transforming luciferin, three other chemicals must be present: magnesium, oxygen, and ATP. So in a test tube containing just luciferin, luciferase, magnesium, and oxygen, nothing happens. Add even a minuscule trace of ATP and the liquid begins to glow, and the more ATP that is added, the brighter the light.

The scientists at Goddard Space Flight Center figured that if they could devise a mechanism to collect environmental samples, disrupt cellular membranes to release the contents, inject this gunk into a reactor vessel containing the four essential ingredients of beetle bioluminescence (excluding, of course, ATP), and then use a photovoltaic sensor to measure the production of light, they'd have a life detector (see Figure 24.1).

This became the basic design of the Firefly, a 1-pound device that could be launched into the upper reaches of Earth's atmosphere, or someday put aboard a rocket's payload to another planet. The automated processing of a sample took about two minutes and the reaction itself yielded a burst of light in less than a second. The early version of the Firefly required relatively large amounts of ATP—as much as would be found in a thousand microbes. By 1975, a tenfold increase in sensitivity was achieved, and today it is possible to detect the light emitted from a sample containing a single cell.7

Early on, the U.S. military saw the potential of the original Firefly as a biological warfare detector.8 An aerosol of pathogens would yield elevated levels of ATP in atmospheric samples. Although the device would miss viruses (these wickedly simple agents have no metabolism of their own, so they lack ATP), all other biological weapons could be detected at very low

Figure 24.1. An early version of the Firefly from 1968, a device that utilized the bioluminescent chemistry of the insect for which it was named as the basis for detecting life—extraterrestrial organisms of interest to NASA or bacterial aerosols of interest to the military. The actual instrument with reaction chamber is in the center of the photograph, while an oscilloscope for signal readout is on the left and the power supply is on the right. (Courtesy of Spherix)

Figure 24.1. An early version of the Firefly from 1968, a device that utilized the bioluminescent chemistry of the insect for which it was named as the basis for detecting life—extraterrestrial organisms of interest to NASA or bacterial aerosols of interest to the military. The actual instrument with reaction chamber is in the center of the photograph, while an oscilloscope for signal readout is on the left and the power supply is on the right. (Courtesy of Spherix)

levels. Although the battlefield commander would not know exactly what pathogen had been released, the key to surviving an attack was more a matter of donning protective gear than of knowing the precise nature of the assailant. False alarms were also a possibility owing to natural pulses of airborne organisms, but these were a small price to pay compared to being surprised by wholesale germ warfare. It seems that the Soviet military concurred, as they independently developed a detector using the same principles as the Firefly.9 But modern defense must take into account tactics much different from those of the Cold War era.

Although U.S. commanders worried that Saddam Hussein would use anthrax or other biological weapons during the Iraq War, the overall sense is that today's soldiers are unlikely to encounter a microbial mist in the course of battle. If pathogens are used by an enemy, the consensus seems to be that the target most likely will be the general public. What keeps defense planners awake at night is the realization that spreading germs within an unwary nation requires a single saboteur's access to the largely unprotected food processing and distribution system. But our nocturnal insect ally may hold the key to a good night's rest in the U.S. Department of Homeland Security.

Federal statutes that assign strict legal liability to every handler in the American food chain—from farm to table—have provided plenty of economic incentive for companies to devote considerable attention to safety issues. However, recent food poisoning incidents have revealed both the fallibility of the safeguards and the startling speed with which a contaminant can spread across the country. From a terrorist's perspective, the food distribution network is a nearly ideal target.

The traditional approach to monitoring for harmful organisms in the food industry has been to swab surfaces and then culture the samples in a nutrient medium. One problem with this method is that various microbes grow in different media, so no single assay detects every kind of pathogen. The other limitation is time. Growing the microbes takes days, and by the time a positive result is obtained the contaminated food may have been distributed throughout the nation. In the best of all worlds, a facility should be able to test its products instantaneously and continuously. And here's where firefly biochemistry has proved its mettle.

By adapting the instrument used by NASA to seek alien life, the Kikkoman Corporation has developed a device to rapidly and repeatedly monitor for the presence of ATP using the principles of firefly luminescence.10 The concept is simple: there ought not to be any live organisms in food preparation areas, so life-free countertops, floors, and walls ensure consumer safety (of course, soy sauce is fermented, so there's plenty of ATP in the bottle). The problem is that we also eat the dead tissue of plants and animals, so background levels of ATP would normally swamp the presence of any living microbes in such foods. In an odd exchange of technological innovation, the solution to this problem emerged from NASA's further modification of Kikkoman's device.

The spacecrafts that were sent to explore Mars had to be built and launched under absolutely life-free conditions to avoid the possibility of introducing earthly microbes to another planet—a sort of reverse Andromeda Strain. And NASA's Jet Propulsion Laboratory found that the food industry's detector was nearly ideal for ensuring the sterility of the clean rooms where spacecraft were assembled.11 The only problem was that if ATP were detected, it would make a big difference whether it came from dead or living organisms. The former were a matter of concern, but the latter were a potential disaster.

So microbiologists in the laboratory's Biotechnology and Planetary Protection Group developed a method for sorting the living from the dead. Prior to introducing a sample to the firefly cocktail and looking for the telltale glow, an enzyme is added to degrade ATP that has leaked from dead microbes. Only then are the cells broken apart to ensure that any ATP that makes it into the detector comes from a living organism.

In a further refinement serving the interests of both food safety and national security, researchers at New York's Rockefeller University are developing pathogen-specific enzymes that would rupture only targeted cells.12 In this way, rapid and reliable tests for particular microbes, such as anthrax, are on the horizon. And with further engineering developments, some see a day in which firefly biochemistry becomes part of automated sensors attached to the water sources and air intakes of buildings.

Adolf-Henning Frucht's discovery that fireflies could warn people of nerve gases, just as canaries once warned coal miners of toxic vapors, has served as the foundation for a spectrum of technological devices to detect chemical and biological weapons. And the fundamental notion that evolution has produced phenomenally sensitive systems that can be adapted for military uses extends beyond the firefly. The capacity of dogs to locate odor sources, including explosives, is legendary. But another animal has an even more highly tuned sense of smell, a species whose capacity to detect infinitesimal traces of particular chemicals and whose potential for obedience training trumps the bloodhound. This other creature is man's best (six-legged) friend: the honey bee (Apis mellifera).

An effective guard has two essential attributes: vigilance and responsiveness. The sentry must remain alert throughout his watch and should decisively challenge an intruder. When the infiltrator is a chemical, rather than a human enemy, the same qualities are needed. However, having soldiers walking about while sniffing the air, and then shouting if they smell something amiss, would be absurd. Bees, on the other hand, make outstanding guards, as the U.S. Army found.

By the mid-1950s, Aberdeen Proving Ground in Maryland had become a deadly dump of military leftovers.13 For the better part of two decades, the army had disposed of its unwanted chemical-warfare agents, unexploded munitions, and dregs from research and production facilities in the fields of this army garrison. Seepage had turned the pastures into wastelands, and the military became increasingly concerned with finding and remediating the most toxic areas. Sending out moon-suited soldiers to take environmental samples was one option, but this was dangerous, expensive, and inefficient. So the army recruited bees for the hazardous duty.

Bees are living dust mops. Their bodies are covered in hairs that, when magnified, look like split ends. This furry coat readily picks up an electrostatic charge, so the insects are like magnets for fine particles. And their capacity to collect contaminants from the environment does not end with their fuzz.

The workers are, well, busy as bees. Their search for pollen and nectar sources means that the insects crisscross an area of about ten square miles around the hive. The foraging bees maintain a remarkable metabolic rate, stoked by large amounts of oxygen. Per gram of body weight, a flying bee inhales air at about 50 times the rate of an exercising human. And when it's hot, bees drink copious amounts of water that they regurgitate into their nest and then fan with their wings to provide evaporative cooling. Put these activities together and a beehive becomes a veritable vacuum cleaner, sucking up and amplifying trace levels of contaminants in air, water, soil, and vegetation.

There's no doubt that bees are vigilant, but a good sentry is also responsive. And the military scientists were quick to discover a means by which these insects could reveal when they'd encountered toxins. In fact, bees perform their assigned duties with military precision. Their behavioral comings and goings are regimented as long as the insects are healthy. But when the workers are intoxicated—and bees are quite sensitive to a range of chemicals—the colony's behavior changes markedly. By moving hives to various areas of Aberdeen Proving Ground and placing infrared "bee counters" at the hive entrances to reveal changes in foraging activity, the military could ascertain whether a site contained toxins. Bees were such useful environmental samplers that researchers also developed automated methods to analyze pollen, wax, honey, and even the air within the hive for traces of toxic chemicals.

Currently, the Departments of Defense and Homeland Security are funding investigations of other insects as chemical samplers.14 More than two dozen species of beetles (order Coleoptera), crickets (family Gryllidae) and moths (order Lepidoptera) are being studied for their ability to sweep various environments and collect contaminants. So far it appears that the honey bees are tough to match. Not only are they fanatical laborers, but they reliably return home after a day of work. Other insects are less cooperative and must be recovered using sticky papers, special lights, or baited traps. But using insects to wander through an area in the hope that they will accidentally encounter and inadvertently collect dangerous compounds is not terribly efficient—a bit like vacuuming your house at random rather than focusing on the high-traffic areas. At least for bees, such an approach fails to take advantage of one of these insect's most remarkable qualities. While a Hoover cannot be trained to find soiled areas of a carpet, bees can learn to seek out chemical "dirt."

The rather outlandish notion of turning bees into a full-fledged warning system has garnered the attention of America's most unconventional research organization, the Defense Advanced Research Projects Agency (DARPA). Boot camp for bees was just the sort of high-risk, high-return project for which the agency has become (in)famous. These are folks who came up with the idea of a mechanical elephant for the jungles of Vietnam, telepathy for psychic spying, and, most recently, the ignominious "terrorism futures market"—along with research behind the Internet, Global Positioning Systems, stealth technology, and the computer mouse. DARPA is pouring $60 million into 20 projects that attempt to exploit living systems for military applications. And if you're going to spend that kind of cash on developing a chemical detection system, you might as well pick a target that provides a lot of bang for the buck.

Few research and development projects seem more farfetched than using bees to detect land mines, but then not many ventures have greater potential to relieve human suffering than a low-cost, high-efficiency system for eliminating this bane of modern warfare. Not only are U.S. troops at risk from these devilish devices, but also vast swaths of valuable farmland have been rendered unusable. Officials estimate that there are 110 million unexploded land mines salted around the globe, or nearly one for every 50 people on earth. With 2,000 people killed and 20,000 maimed every month, the need is overwhelming to find these weapons for humanitarian, not to mention military, reasons. But land mines are solid objects, not vaporous substances, so how can a bee locate them beneath the soil?

In the early days of modern warfare, mines were encased in metal, so minesweepers were essentially metal detectors. But in recent times mines have become cheap mass-produced weapons, which means they're usually housed in plastic. Without metal to indicate their presence, the challenge is to detect faint traces of explosives that constantly leak from the mines. Such extraordinarily low-level vapor plumes have been exploited by scientists at Sandia National Laboratory in their development of handheld chemical "sniffers" to track down the buried booby traps. While these sophisticated instruments are effective, they are also expensive to manufacture, technically demanding to operate, and difficult to maintain. These are hardly the qualities that poor, undereducated, worn-torn countries seek when adopting new technologies. Machines are complicated and costly, but at least some animals are another story.

Dogs have proved to be highly sensitive and accurate mine detectors. The canines can be taught to associate the odor of explosives with a reward, so they become enthusiastic partners in the search for mines. Training and handling the dogs are not trivial demands, however. The animals are not cheap to maintain, and even with a very long leash (which seems advisable), the handler is in danger—not to mention man's best friend. Given these drawbacks, bees look pretty good. Moreover, the insects' antennae can beat the most sensitive doggy nose.

Honey bees can sniff out 2,3-DNT (the vaporous residue from militarygrade TNT, which commonly serves as the explosive in mines) at unbelievably low levels.15 An ounce of explosive buried in 40 pounds of sand emits a plume containing about 50 parts per trillion of 2,3-DNT in the air. This is the equivalent of a bathtub of chemical dumped into Lake Erie. And a honey bee can find this delicate aroma of explosive even when the simulated mine is 100 yards from the hive. What's more, teaching a worker bee to hunt down the leaky land mines is simpler than housebreaking a dog.

Evolution has shaped bees into quick studies. To survive, these insects must learn which plants are producing nectar amid a diverse and changing floral spectrum. Once a worker strikes pay dirt, she teaches her nestmates the location of the flowers through a remarkable "dance language." So conditioning these smart insects to associate a particular odor with food turned out to be remarkably simple.

The entomological training regimen consisted of moistening a sponge with a sugar solution to which just a hint of explosive had been added, then placing this chemical classroom where the workers were sure to find it.16 The bees quickly learned that a whiff of TNT held the promise of a sweet snack. Moreover, the insect tutorials were phenomenally efficient—tens of thousands of bees could be trained in an hour. Once the insects made the connection, they became nearly infallible guides to hidden explosives.

The proving ground consisted of a simulated minefield, in which the scientists had planted and mapped the explosives. Given 60 minutes of searching, the trained bees detected 99 percent of the mines buried within 200 yards of their hive—a task that would take hours or days using sophisticated instruments. But even with the bees trained to selectively sweep a field for land mines, a significant hurdle remained before the detection system was operational.

The military had to know not only that there were mines somewhere in the area but they needed to pinpoint their location. After all, neither infantrymen nor villagers gain a whole lot from just knowing that there are land mines somewhere in the vicinity of a beehive. The first approach was to attach tiny, rice-size radio packs to the bees and follow their movements with an electronic tracking system. But this defeated the elegant simplicity and cost efficiency of using the bees. The breakthrough came when researchers stopped trying to outthink the bees.

Jerry Bromenshenk of the University of Montana, played an important role throughout the development of the mine-detection project.17 As an entomologist who had studied bees for three decades, he understood how these insects could be transformed into entomological bloodhounds, leading humans directly to buried mines without the complexity of radio transmitters. The human overseer had merely to shed the role of a busybody scientist and take on the persona of a lazy foreman. Just watch the bees while they did all the work.

In the summer of 2003, Bromenshenk stood anxiously at the edge of a minefield where he'd placed ten colonies of his trained bees—without teensy backpacks. The movements of the bees would be tracked using human observers, video cameras, and LIDAR (a device that uses a laser in much the same way as radar or sonar use radio or sound waves). The latter two tracking systems were necessary for military researchers with a fondness for technology. But Bromenshenk was betting that a pair of binoculars would work just as well. His deep-seated hope was to field a system that could be used by both American troops and peasant farmers. And to Bromenshenk's delight, the three monitoring methods were equally capable of distinguishing a cluster of airborne bees. Not only did the insects locate the mines, but the number of bees hovering over a spot indicated the strength of the odor plume—more bees meant either a larger mine or a concentration of small mines (see Figure 24.2). However, Bromenshenk's celebration was dampened by a most troubling event.

Figure 24.2. This map was derived from applying scanning LIDAR (similar to radar, except reflected light rather than radio waves is used to detect objects) to determine the densities of bees hovering over a 2^-acre minefield. The lighter areas indicate places where bees clustered, which matched areas with high visual counts (a labor-intensive method useful when the observer is not endangered by fused mines) and regions of chemical plumes from buried mines. (Courtesy of Joe Shaw)

In the world of mine detection, the most serious problem is a false negative, in which the system indicates that nothing is present when, in fact, there is a mine. But the reverse problem is also of concern. A false positive—the indication of an explosive when there is none—diminishes efficiency as disposal technicians focus attention on something that isn't really there. And so when the bees hovered insistently over a site within a test plot that had no mines, the researchers were concerned. However, analysis of a soil sample from the location where the bees raised a supposedly false alarm revealed a low level of contamination. Apparently, an earlier, improperly documented experiment had left behind a trace of 2,3-DNT, and the bees notified the military of their embarrassing oversight.

Bromenshenk saw that his bees could help pave the way for subsistence farmers—those people most likely to have suffered the ravages of war and the lingering effects of land mines—to rebuild their agriculture. They wouldn't need to import expensive equipment when the local bees could be put into service. With a sample of explosive-contaminated soil, a dribble of sweet syrup, a squirt bottle, and a bit of patience anyone could train the insects. Then, the farmers could simply watch where the bees gathered in the fields. Moreover, once local villagers caught on to using bees as mine detectors, the wholesale restoration of beekeeping might soon follow. And agricultural development experts had long known that returning pollinators to war-torn lands is essential to restoring a people's capacity to feed themselves.

Bromenshenk's enthusiasm became infective—at least within the military-entomological complex. Seeing the remarkable strides made with trained bees, scientists from the U.S. Department of Agriculture began to imagine how wasps could be converted into mine detectors. These insects might even be taught to respond like the beagles that sniff for contraband in airports. While the bees simply hover over an odor plume, wasps naturally perform distinctive behaviors when in the immediate proximity of a food source. Jim Tumlinson conceives of a platoon of wasps that, upon finding an explosive (or any other target chemical), settle down and rub their antennae on the precise origin of the smell—or attempt to sting the odor source, which they perceive to be prey. Joe Lewis, on the other hand, favors a more elaborate approach.18

Lewis invented a hand-held odor-detection device affectionately called the "Wasp Hound." The entomological linchpin consists of a set of six-legged detectors that are conditioned using the familiar sugar-and-spice approach (where the "spice" is whatever target smell the operator wants the insects to associate with the sweet reward). The contraption draws air into chambers that hold five trained wasps in Lilliputian squeeze chutes. Whenever the insects smell the odor, they duck their heads to receive a sweet reward—and, in so doing, trip an electric eye. Although one wasp might make the occasional mistake (after all, its brain is smaller than a typewritten period), the quintet is highly reliable.

But insects are not without their limitations. Unlike soldiers, bees and wasps do not perform their assigned duties at night, in the rain, or when it's cold. The insects' ability to locate mines also declines where there are very dry conditions or there is dense vegetation. And, at least so far, the only field tests have involved simulated minefields free of bomb fragments, spent munitions, and other chemical distractions. There are, however, ways of overcoming these limitations. Although some scientists have considered the possibility of genetically engineering a better honey bee, DARPA believes that an even more radical form of engineering may hold the key to the ultimate detector—an entomological cyborg.

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