Published: September 2009
Love and Lies
How do you spread your genes around when you're stuck in one place? By tricking animals, including us, into falling in love.
By Michael Pollan

We animals don't give plants nearly enough credit. When we want to dismiss a fellow human as ineffectual or superfluous, we call him a "potted plant." A "vegetable" is how we refer to a person reduced to utter helplessness, having lost most of the essential tools for getting along in life. Yet plants get along in life just fine, thank you, and did so for millions of years before we came along. True, they lack such abilities as locomotion, the command of tools and fire, the miracles of consciousness and language. To animals like ourselves, these are the tools for living we deem the most "advanced," which is not at all surprising, since they have been the shining destinations of our evolutionary journey thus far. But the next time you're tempted to celebrate human consciousness as the pinnacle of evolution, stop to consider where you got that idea. Human consciousness. Not exactly an objective source.

So let us celebrate some other pinnacles of evolution, the kind that would get a lot more press if natural history were written by plants rather than animals. (I suppose an article by a biped named Pollan will have to do.) For while we were nailing down locomotion, consciousness, and language, the plants were hard at work developing a whole other bag of tricks, taking account of the key existential fact of plant life: rootedness. How do you spread your genes around when you're stuck in place? You get really, really good at things like biochemistry, at engineering, design, and color, and at the art of manipulating the "higher" creatures, up to and including animals like us. I'm thinking specifically of one of the largest, most diverse families of flowering plants: the 25,000 species of orchids that, over the past 80 million years or so, have managed to colonize six continents and virtually every conceivable terrestrial habitat, from the deserts of western Australia to the cloud forests of Central America, from the forest canopy to the underground, from remote Mediterranean mountaintops to living rooms, offices, and restaurants the world over.

The secret of their success? In a word, deception. Though some orchids do offer conventional food rewards to the insects and birds that carry their pollen from plant to plant, roughly a third of orchid species long ago figured out, unconsciously of course, that they can save on the expense of nectar and increase the odds of reproducing by evolving a clever deceit, whether that ruse be visual, aromatic, tactile, or all three at once. Some orchids lure bees with the promise of food by mimicking the appearance of nectar-producing flowers, while others, as in the case of a Dracula orchid, attract gnats by producing an array of nasty scents, from fungus and rotten meat to cat urine and baby diaper. (Believe me, I've sniffed them.) Some orchids promise shelter, deploying floral forms that mimic insect burrows or brood rooms. Others mimic male bees in flight, hoping to incite territorial combat that results in pollination.

But perhaps the most clever deceit of all is offered by those orchids that hold out the promise of sex. And not exactly normal sex. Really weird sex, in fact.

Hoping to observe some of this plant sex, said biped recently journeyed to Sardinia, a windswept, mountainous, and lightly populated island 120 miles off the west coast of Italy that has long been known for floral biodiversity and human kidnapping. (Deceit is evidently very much in the air.) I went in search of one of the most ingenious and diabolical of orchids: the Ophrys. (Some botanists call it the "prostitute orchid.") I'd been eager to lay eyes on this orchid and meet its hapless pollinator ever since reading about its reproductive strategy, which involves what my field guide referred to as "sexual deception" and "pseudocopulation." What I learned of the prostitute orchid forced me to radically revise my estimation of what a clever plant is capable of doing to a credulous animal.

In the case of this particular Ophrys, that animal is a relative of the bumblebee. The orchid offers no nectar or pollen reward; rather, it seduces male bees with the promise of bee sex and then insures its pollination by frustrating precisely the desire it has excited. The orchid accomplishes its sexual deception by mimicking the appearance, scent, and even the tactile experience of a female bee. The flower, in other words, traffics in something very much like metaphor: This stands for that. Not bad for a vegetable.

Orchid hunting can be arduous in many places, but in the mountains of Sardinia Ophrys orchids grow like roadside weeds. When they bloom in April you can spot them from a moving car. Close up, the lower lip, or labellum, of these diminutive orchids bears an uncanny resemblance to a female bee as viewed from behind. This pseudobee, which in some Ophrys species comes complete with fake fur and what appear to be elbows and folded iridescent wings, looks as though she has her head buried in a green flower formed by the actual flower's sepals. To reinforce the deception, the orchid gives off a scent that has been shown to closely match the pheromones of the female bee.

When it comes to getting an orchid pollinated, sexual deception has an uneven success rate (more on that later), but when it does work, it works like this: The real male bee alights on the beelike labellum and attempts to mate, or in the words of one botanical reference, begins "performing movements which look like an abnormally vigorous and prolonged attempt at copulation." In the midst of these fruitless exertions, the bee jostles the orchid's column (a structure that houses both the male and female sexual organs), and two yellow sacs packed with pollen (called the pollinia) are stuck to his back with a quick-drying gluelike substance. Frustration mounts, until eventually it dawns on the bee that he has been had. He abruptly flies off, pollinia firmly attached, in frantic search of more authentic female companionship.

There was something poignant about the bee I spotted, flying around madly with what looked like a chubby pair of yellow oxygen tanks strapped to his back. He'd been deluded by the promise of sex—bee sex—when in fact all that was on offer was plant sex, and unbeknownst to the bee, now searching for a second, more satisfactory liaison, he was right in the middle of that act. Botanists have been known to refer to pollen-carrying bees as "flying penises," but of course most of the world's bees perform in that role unwittingly, with food rather than sex on the brain. Not so for the poor, deluded orchid bee.

The pollination strategy of the Ophrys is, like that of so many orchids, ingenious, intricate, wily, and seemingly improbable—so much so that proponents of intelligent design sometimes point to orchids as proof that the hand of a higher intelligence must be at work in nature. (And a rather sadistic intelligence at that.) Yet the peculiarities of orchid sex actually offer one of the great case studies of natural selection, as Charles Darwin himself under­stood. Darwin was fascinated by orchid pollination strategies, and though he was puzzled by the purpose of Ophrys's uncanny resemblance to bees (pseudocopulation wasn't observed until 1916), he taught us much of what we know about these plants in The Various Contrivances by Which Orchids are Fertilised by Insects, the volume he published immediately after The Origin of Species. Indeed, some scientists believe that had he published his orchid book first, the theory of natural selection might have encountered less skepticism than it did. Why? Because in orchids Darwin identified floral structures "as perfect as the most beautiful adaptations in the animal kingdom." He painstakingly demonstrated how even the most unlikely features of these flowers serve a reproductive function, and many of these structures are so perfectly adapted, both to the plant's requirements and the morphology of its pollinators, that they offered Darwin elegant proofs of his outlandish theory.

In one famous case, putting the final QED on Darwin's proof that evolution had tailored a flower to lure and exploit a specific pollinator had to wait a few decades. Attempting to explain why the star orchid of Madagascar would secrete a drop of nectar at the tail end of a foot-long floral spur, where no known pollinator could possibly get at it, Darwin hypoth­esized the existence of a moth with a 12-inch-long tongue, an unlikely creature that had never been observed. Vindication arrived a couple decades after Darwin's death, when entomologists unfurled the tongue of a newly discovered hawk moth and found that it measured nearly a foot long.

The orchid's baroque pollination strategies do raise challenging questions for the evolutionist, however. Since natural selection seldom rewards the unnecessary complication, why haven't all orchids stuck with the more straightforward pollination strategies based on nectar reward? And how in the world did their sexual practices get so elaborate? As for the hoodwinked pollinators, what, if anything, do they gain? If the answer is nothing but frustration, then why wouldn't natural selection eventually weed out insects so foolhardy as to spend their time mating with nature's version of the inflatable love doll?

Botanists and evolutionary biologists have come up with fascinating answers to many of these questions. John Alcock, an evolutionary biologist and author of An Enthusiasm for Orchids, proposes two explanations for why some orchids would have evolved to avoid a simple nectar reward. When botanists experimented by adding a nectar reward to a normally nectarless orchid, they found that the pollinators hung around longer, happily visiting other blooms on the same and nearby plants. This does not suit the orchid's interests, however, since inbreeding results in lower quality seeds. By comparison, outcrossing, or mixing one's genes with distant mates, increases vigor and variation in one's offspring, maximizing fitness. The sexual frustration of a deluded bee turns out to be an essential part of the orchid's reproductive strategy. Determined not to make the same mistake again, the bee travels some distance and, if things work out for the orchid, ends up pseudocopulating (and leaving his package of pollen) with an orchid a ways off. That distant orchid is likely to look and smell ever so slightly different from the first, and some botanists believe these subtle variations from plant to plant are part of the orchid's strategy to prevent bees from learning not to fall for a flower. "Imperfect floral mimicry" is the botanical term for this adaptation. Think of it: The very imperfection of the orchid's mimicry may itself be part of the perfection of its reproductive strategy.

Another reason so many orchids have gotten out of the restaurant business may have to do with the benefits of developing a relationship with a single, highly devoted pollinator. Nectar, besides being metabolically expensive for the flower to produce, is beloved by so many different animals that it attracts all sorts of riffraff that may not deliver your pollen to the right target. But if you produce a scent that attracts only the males of one particular species of bee, you can insure that your pollen will end up precisely where you want it: on the stigma of a far-flung orchid of your own kind.

The exactitude of the perfume business may also help explain the astounding diversity of the orchid family. A mutation producing even a slight change in an orchid's scent could, strictly by chance, turn out to be the key that unlocks the sexual attentions of a new pollinator, while at the same time completely turning off the original pollinator. In this way, variations in the chemistry of floral scent can function much as geographic isolation does in the creation of new species, by preventing new mutant flowers from being pollinated by older ones. The novel orchid might evolve in genetic isolation from its forebears—a prerequisite for creating a new species.

Orchids have excelled at spinning off new species, and yet there are remarkably few orchid plants in the world. Their relative rarity in the landscape puts a premium on highly customized pollination strategies to deploy their pollen as efficiently as possible—unlike grasses, for instance, which can simply broadcast their pollen on the wind. Yet their small numbers ensure their survival. If deceptive orchids were much more common, their ruses would no longer work, since they depend on the ubiquity of honest flowers. Orchid deception can succeed only in a world where most things in nature really are what they seem: where the smell of rotting meat signals rotting meat, where flowers really do offer nectar and don't dress up as bugs.

It seems fair to say that when it comes to their own sex, orchids have opted for quality rather than quantity. For while sexual deception doesn't fool all of the pollinators all of the time, it does fool some of them some of the time, and for an orchid that is quite enough. That's because each pollinium contains a stupendous number of pollen grains, and once they're delivered, every resulting seedpod contains an equally stupendous number of seeds. So while sex among the orchids may be a rare and intricately choreographed affair, what happens after the match is made is all about profligacy and chance. Orchid seeds are so tiny and minimalist they don't even contain a source of food for the developing embryo. For this, the orchid must (once again) count on the kindness of strangers—in this case, that of an endophytic fungus. If all goes right (and here again, it seldom does), the tendrils of the fungus infiltrate the orchid seed and provide the nutrients that the developing embryo needs to grow. What does the fungus get out of the relationship? Don't be so sure it gets anything—these are orchids, after all.

Gaspar Silvera is an orchid hunter and breeder in Panama given to wearing straw fedoras and married to a woman named Flor. An agronomist by training, Silvera has, since retiring from government service, devoted himself to rescuing orchids from the threat of development and to the painstaking work of propagating them. Photographer Christian Ziegler and I flew to his nursery in Chilibre after Silvera phoned us to report that one of his Coryanthes, the Central American bucket orchid, a species notoriously difficult to keep happy in captivity, had bloomed. We were hoping to witness one of nature's most dramatic PG-rated pollination scenes.

By the time we got to the nursery, the canary yellow flower, a surprisingly ungainly Rube Goldberg contraption, was already fading, though it still gave off a powerful perfume of apricots and eucalyptus. The flower had thrown open its elaborately engineered petals just a few days before, and the spicy-sweet perfume had summoned out of the surrounding woods a band of male euglossine bees, a sleek, stingless, iridescent relative of the bumblebee. The bees competed with one another for space on the slick curves of the intricately sculpted flower, directly above a labellum that forms a deep bucket, into which the flower drips a clear, slightly viscous liquid.

Nectar it is not.

Visiting bees busy themselves scraping fragrances from the waxy surface of the flower using their front legs; they then transfer the scents to tibia sacs carried on their rear legs like little wallets. Exactly what they're up to wasn't understood until 1966, when a botanist named Stefan Vogel figured out that the bees were collecting the chemical building blocks needed to create a scent. Most animals that rely on scents to attract a mate produce it themselves; not the euglossine bee, which forages for a specific set of ingredients, gathering them not only from orchids but also from certain leaves and fungi, and then mixes up the perfume by "hand." Once he's concocted his mixture, the bee spreads it on his body and flaps his wings to release a captivating scent of camphor and flowers to summon a female.

But the bucket orchid exacts a steep price for its contribution to this perfume. As the bees jostle each other for scents, one or more of them is apt to lose his footing on the slick petal and plunge into the bucket. This wouldn't be a problem, except the viscous liquid in the bucket renders the bee's wings temporarily useless. So the bee struggles mightily to clamber up the slippery walls of the bucket until he stumbles upon a series of steps, which conduct him up and out of the pool through a narrow passageway leading out the back of the flower. As the dazed and sopping bee squeezes himself through the tunnel, he passes beneath a spring-loaded device that (you guessed it!) claps a pair of yellow pollinia onto his back. If all goes according to (orchid) plan, the bee dries off his wings, flies to another Coryanthes, splashes into the bucket again, and on his way out through the tunnel unwittingly snags his yellow backpack on tiny hooks adapted for precisely that purpose. Pollination accomplished, the bucket orchid closes up shop, collapsing its extravagant petals into a wad of crumpled yellow tissue.

The case of the Coryanthes is a happy example of an orchid and its pollinator benefiting mutually, but such is not always the case. Although the euglossine bee escapes with his wallet full of scents, that's more than you can say for some other orchids' hapless dupes. If it's starting to sound as though I don't trust orchids, that's because I've seen what they can do to some of my fellow animals. There's a video on YouTube, a riveting snippet of interspecies porn, in which you can watch a wasp be utterly bamboozled, and then humiliated, by an Australian tongue orchid. The tongue orchid (Cryptostylis) lures its pollinator by deploying a scent closely resembling the pheromone of the female wasp (Lissopimpla excelsa). The male wasp alights on the tonguelike labellum, tail first, and commences to copulate with the flower, probing its interior with the tip of his abdomen until it bumps into the sticky pollinia, which attach themselves to the insect's posterior like a pair of yellow tails.

Having to play pin the tail on the pollinator is only the beginning of the wasp's humiliation. For with the tongue orchid we have passed beyond pseudocopulation into a realm even more perverse: More often than not, the wasp, in the throes of his misguided sexual exertions, actually ejaculates onto the flower.

Surely this represents the height of maladaptive behavior, and natural selection could be expected to deal harshly with a creature foolish enough to squander its genes having sex with a flower. ("Costly sperm wastage," is how the literature describes it.) That would be bad news for both the wasp and the orchid that depends on him. But as with so much else in the bizarre world of orchid sex, the matter is not quite so simple.

It appears that in some insect species, such as Lissopimpla excelsa, females can reproduce with or without sperm from a male. With it, they produce the usual ratio of male and female offspring; without sperm, they produce only male offspring. How convenient—for the tongue orchid, that is. By inducing wasps to waste their sperm on its flowers, tongue orchids are decreasing the amount of sperm available to female wasps, thereby assuring themselves an even larger population of pollinators. Not only that, but the overabundance of male wasps increases competition for females, which makes the desperate wasps less picky in their choice of mates and that much more likely to fall for a flower.

What about the poor wasp? Why hasn't natural selection killed off an insect so dumb as to have sex with flowers? The best explanation I've heard is from John Alcock, who says that although the wasp may occasionally waste his genes on a plant, his "extreme sexual enthusiasm" is still a better reproductive strategy for an insect than being cautious about one's choice of mate. On balance, having sex with anything that moves yields more offspring, even if it also leads to occasional romantic disaster.

To learn all this about orchids is to admire them more but, perhaps, love them less. And to wonder if we too have fallen prey to their deceptive charms. Like the scent-gathering euglossine bees, we use them to communicate our romantic intentions and lure mates, extracting their essence for perfumes and wearing them in corsages. Orchids have served us in this capacity since at least 1818, when William Cattley, an English plantsman, rescued a discarded orchid bulb that had been used as packing material in a shipment of tropical plants. The flowering of that specimen ignited a Victorian passion for orchids that has never really subsided.

The very name of the plant comes from the Greek word for testicle, referring not to the plant's flowers but its bulbs, organs that have long been endowed with aphrodisiac properties. But it doesn't take a Freudian to discern a strong sexual subtext in the passion for these flowers, especially among men, who any visit to an orchid show will tell you suffer disproportionately from "orchidelirium"—the Victorians' term for the madness these flowers inspire. Victorians were offended by the "blatant sexuality" of orchids, according to Eric Hansen, the author of Orchid Fever; he isn't referring to plant or insect sexuality either. "Prurient apparitions," is how Victorian critic John Ruskin described these flowers.

Prurient? Is it possible that humans can look at an orchid and, like the deluded orchid bees or male dupe wasps, see an apparition of female anatomy? (Georgia O'Keeffe certainly did.) Could it be that plant sex and animal sex have gotten their wires crossed in human brains just as they have among the bugs? That accident of evolution has proved another happy one for the orchid, for look how much we humans now do for these flowers: the prices paid, the risks to life and limb endured, the pains taken …

Those were my thoughts as I watched Gaspar Silvera deploy a pair of slender forceps to remove a pollinium from a bucket orchid that had failed to entrap a euglossine bee. ("I suppose you could say that I too am manipulated by orchids," he'd explained at the end of a shaggy tale about the lengths he goes to secure choice specimens.) Working with the steady hand of a jeweler, Silvera used the forceps to grab the base of the pollinium and then pressed it to a slit in the column of another bloom. Five years from now, Silvera may find himself with a precious new flower—and the orchid will have offspring it would otherwise not have had.

Ever since the first human-hybridized orchid bloomed (the earliest in the Western world was recorded in 1856), we humans have become important orchid pollinators too—more intentional perhaps than the orchid bees, but lured into advancing the orchid's interests just the same, assisting in its quest for world domination. Today there are some 100,000 registered hybrid orchids, most of them the offspring of improbable marriages among far-flung plants arranged by, and literally inconceivable without, us.

Not that any of this was ever in the orchid's plan. In evolution there is no plan, of course, only blind chance. But the moment that the orchid stumbled upon one of the keys to human desire and used it to unlock our hearts, it conquered a whole new world—our world—and enlisted a vast new crew of credulous animals more than happy to do its bidding. Let's face it: We're all orchid dupes now.