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ANATOMY OF A ROSE -- EXPLORING THE SECRET LIFE OF FLOWERS |
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SEVEN: Dirty Tricks WHERE I LIVE IN southwestern New Mexico, yucca stalks of creamy white flowers bloom during the summer rainy season. These plants blaze up suddenly like candles in the desert, twelve feet high. Overnight, a scrubby field turns into a menorah. Most yucca species are odorless, although many secrete a bit of nectar at the base of the ovary. This nectar may date from a time before the coevolution of yucca and yucca moth. For the yucca has only one pollinator and, on reaching adulthood, that ascetic insect does not eat or drink at all. Breaking out of their cocoons, rising from the ground, yucca moths copulate in the white, waxy yucca flowers. The pattern varies among species, but typically a fertilized female moth climbs up a stamen in a flower and bends her head over the top of the anther. Uncoiling her tongue, she uses it to steady herself. With special mouthparts, she scrapes away the pollen and holds it fast in her forelegs, collecting pollen from as many as four stamens. Now the yucca moth flies away to another flower in another yucca. There she pushes through the stamens and pierces the ovary, where she lays an egg. Then she moves up the tubular stigmas to pollinate the flower, pushing down pollen into the stigmatic duct. Often she lays another egg. After each one, she may move up again, rocking back and forth, pollinating the stigma, laying another egg, pollinating the stigma. Yuccas are self-incompatible. By going to another plant to deposit her pollen, yucca moths cross-fertilize the yucca. By pushing pollen into the stigma, yucca moths are among the few insects that are active, rather than passive, pollinators. In this way, they ensure food for their larvae. An unfertilized yucca flower soon falls from the plant. The ovules of a fertilized flower produce seeds. The yucca moth larvae hatch in the ovary and consume up to 15 percent of these seeds. Nourished, the larvae chew a hole through the fruit wall, drop to the soil, and stay cocooned until they emerge in a year or two or three. Enough seeds remain for the yucca to propagate. All this sounds like an Aesop's fable in which the protagonists behave unusually well. When we think of flowers and pollinators, we often think of this kind of relationship. It is called mutualism: The butterfly feeds on the honeysuckle in exchange for transporting pollen. Two different species have evolved to depend on each other.
Yucca Flower Most mutualisms are generalized. Pollinators visit many plant species, and plants rely on many different pollinators. A one to one relationship, like the yucca and yucca moth, is less common. Charles Darwin wrote, "Natural selection cannot possibly produce any modification in any one species exclusively for the good of another species; though throughout nature one species incessantly takes advantage of, and profits by, the structures of another." In the case of the yucca, natural selection has created an exceptional partnership. It seems a model of cooperation. It is almost a parable. In their incessant way, other species quickly take advantage. Closely related to the yucca moth, the bogus yucca moth never transports pollen but also flies to a yucca flower, where it lays its eggs, which hatch into larvae that eat yucca seeds. This moth lays her eggs not just in new flowers but in already fertilized and developing ovaries. Not only does the moth fail to pollinate the plant, but fruits from these flowers will now have too many larvae, with too many seeds eaten. Yuccas respond by shedding flowers (before they can seed and fruit) that are overinfested with insect eggs. Flowers insufficiently pollinated also tend to be aborted. In the end, the bogus yucca moth, which tries to cheat the system, won't reproduce as often as the moth that plays fair. Botanists use the Spanish word aprovechado, "one who takes advantage," for an animal that benefits from a mutualism without providing any return benefit. All pollination systems are vulnerable to opportunistic aprovechados. Moreover, pollinators themselves can turn into aprovechados. Instead of approaching a flower from the front, contacting the pollen-laden anthers, honeybees sometimes enter from behind and steal nectar by inserting their tongues between the sepals and petals. In the biologist's vernacular for crime, this nectar theft is known as "base working." In flowers whose corolla has fused into a tube, thieving insects must forcibly bite through the tissue. Short-tongued bumblebees are notorious for using their mandibles to pierce the corollas of toadflax, daffodils, and columbines. Distinct from theft, nectar robbing is a more aggressive breaking and entering, in which the flower is damaged. Secondary thieves now enter the hole to steal nectar for themselves. This is not a world of trust. Windows must be barred, doors locked. Flowers do what they can to protect themselves. Some have a leathery, hard-to-pierce calyx. Firm, overlapping leaves or bracts at the base also deter robbers. Dense inflorescences are another strategy. Because the yucca and the yucca moth have evolved so tightly to fit each other's needs, they are particularly susceptible to aprovechados. They suffer, as well, from codependency. The reproductive success of one species depends on the reproductive success of the other. When farmers in the desert spray for agricultural pests, killing the yucca moths as well, the yuccas are left without a pollinator. Statuesque, in full bloom, they light up the horizon. Serenely, they wait. No one comes. This is botanical Shakespeare. As well as using cross-fertilization, some yucca species propagate vegetatively, cloning themselves in a lonely fashion. It's a fall-back plan, a secret bank account, something your lover cannot possibly imagine, something you somehow forgot to tell him. *** BECAUSE PLANTS DON'T MOVE, we think of them as nicer than animals. This is pure prejudice. As one researcher wrote, "cheating pollinators seem to be more rare than cheating plants." Many flowers have the bad habit of exaggerating their virtues. They may have bushy hairs on their stamens or a bright yellow coloring so that the stamens look richer in pollen than they really are. Small anthers top large, attractive filaments that resemble anthers. In some plants, the sterile part of an anther puffs up into a nutritious-looking "dummy." Flowers engage in what can only be called rough sex. In one orchid, a gentle touch on a tiny flower part causes the stem of the pollinium (a sac of pollen grains) to snap like a metal spring, catapulting the stem and its disk of sticky pollen onto the surprised bee. Sometimes the bee is knocked out of the flower. If a mischievous human tried this with a pencil point, the pollinium would sail for almost a yard. Other flowers similarly slam, hurl, or slap pollen onto an insect's body. The ejection of pollen can be violent. Its placement can also be unfortunate. One orchid attaches its pollinium -- the stem and disk -- to a hawkmoth's eye. Although the pollen is transferred to another orchid, the relatively large stem remains glued in place. Proportionally, this would be like having a hockey stick hang from your eyeball. Some pollinators, such as birds and hawkmoths, can be seen with multiple pollinia studding their tongues. Darwin theorized that these animals, unable to feed, would soon die. First, though, they could pollinate a few more flowers. Even the "nicest" flower can turn suddenly ruthless. In the common milkweed, pollen sticks so persistently to the visiting bumblebee that sometimes, as the bee tries to flyaway, its entangled legs tear off. A surprising number of flowers don't have anything to offer an insect but aggravation. As many as one-third of orchid species rely on deceit. Some specialize in pseudocopulation. Some look like a safe place to breed. Many smell like a food source, but instead of the promised reward, these flowers have invested in a dizzying array of chutes, passages, turnstiles, chambers, entrances, and exits. Beloved by gardeners around the world, orchids have all the ambiance of a carnival fun house. Drawn to one blossom by its pleasing stench, a fly settles on a tongue-like lip only to find itself flipped backward and downward, embraced by two springy "arms," and held fast. The scene starts to resemble a James Bond movie. The lip is hinged and balanced to respond to the fly's weight, and the two flower arms force the fly to struggle, removing any pollinium on its abdomen. Eventually, like James Bond, the fly escapes. In the European lady's slipper, a fruity scent and a bright yellow color attract bees through an opening into the slipper or lip area. Large bees can usually exit, although a few insects get trapped and die. A small bee cannot fly out again and keeps sliding on the smooth, turned-in petals. After buzzing its wings and casting about, the bee finds a passage through the back of the flower, guided there by the light from translucent windows near the lip's base. As the insect squeezes past the stigma and stamen, any pollen it carries is left behind. New pollen is smeared onto its thorax. The lady's slipper's plan is not foolproof. Some insects get away without having been properly accessorized. Also, experienced bees will avoid the flower. Prudently, the lady's slipper sends out rhizomes, underground stems that can root at a distance and produce a new, clonal plant. In yet another orchid, one that rewards the euglossine bee with perfume, the big, drop-dead gorgeous flower hangs down and exhales an attractive scent. Part of its lip forms a bucket filled with liquid secreted by the flower. The base of the lip is slippery. The visiting bee loses its foothold and falls into the tiny swimming hole. Again, the exit is a hidden tunnel that passes the orchid's stigma and anthers. Here a bee might be caught for as long as thirty minutes, while pollinia are transferred to the base of its abdomen. A few flowers don't bother to provide exits. The gnats that visit a certain arum lily in its female stage, when the stigma is receptive, will die in its lower chamber. If the gnats are carrying pollen from another arum lily, they will not die in vain. The flower has been fertilized. Gnats that visit the arum in its male stage, when pollen is being released, will find an exit and go free, nicely dusted. The common jack-in-the-pulpit has male flowers and female flowers on two separate plants. Lured by the odor of fresh fungi, gnats fly to the flower and tumble into its chamber. Lucky gnats tumble into a male flower, which provides an escape. Unlucky gnats tumble into a female flower. A particularly ugly scene takes place on a large, sweetly scented water lily. In the male stage, the lily offers an abundance of pollen-covered stamens to a host of hoverflies, bees, and beetles. For three or four days, each morning, the flower opens to offer a banquet Roman in scope and delight. Humans also take pleasure in the water lily. Many flowers are known for their beauty. But this flower seems to have reached a kind of Ur-beauty, an ascension to Buddha-hood. In the female stage, the same lily opens and looks somewhat different. Now the stamens are without pollen and encircle a pool of liquid in the flower's center. At the bottom of the pool is the flower's flat, round stigma. The background music changes. We know what this means. We want to warn that little hoverfly: Don't land on that stamen! Oblivious, the insect teeters on the now-smooth stamen surface. The hoverfly slips and tumbles into the pool. Desperately the victim struggles, but the tall stamens offer no foothold. The liquid contains a wetting agent that clings and pulls at the lightest insect. The fly sinks beneath the liquid and drowns. The pollen on its body washes away, gently settling over the implacable stigma. Sometimes, I am even touched by those carrion feeders trying to lay eggs in flowers that resemble rotting meat. They are clearly trying to do the right thing, breeding in a place that will provide food for their young. Fungus gnats are similarly poignant. In flowers that mimic fungi, the parents leave satisfied, covered in pollen. The eggs hatch into larvae that will die of starvation. Some flowers try to hurry things along. In American wild ginger, the tissues of the flower are extremely poisonous. *** PLANTS AND POLLINATORS are part of a mutualism more like an arms race than a marriage. In order to get more food or lay more eggs, the pollinator develops a new strategy. The plant counters. One side builds a missile. The other side builds an antimissile -- and a bigger bomb. The generation that wins threatens to destroy the system that supports them both. The water lily cannot afford to murder too many hoverflies, or the jack-in-the-pulpit too many gnats. The deceitful orchid must not be too successful, or its pollinators will starve to death. On their part, bumblebees and moths and hummingbirds had better not steal or cheat with such impunity that they fail to pollinate any flowers at all. Missiles. Defenses. Antiaircraft. Images of battle come easily when you remember that many animals like to eat plants, not just sip nectar or collect pollen. Plants and insects have been at war forever, and pollination systems probably evolved out of that dynamic. Feeding beetles somehow shifted into pollinating beetles. In the end, of course, when a flower cannot co-opt or avoid or out-strategize an enemy, it may have to destroy him. The army worm feeds on daisies. The daisy's defense is to produce a chemical mildly toxic in the dark and highly toxic in ultraviolet light. As the worm eats the plant, it absorbs this chemical which eventually moves through its circulation system to the surface of its skin. On a nice spring day, the sun shines warmly. First the army worm glows florescent blue. Then it shrivels up and turns black. A caterpillar known as the leaf roller has a counterdefense. It bends the petals of the daisy over itself and secures them with threads of silk. Safe in the dark, protected from sunlight, the leaf roller begins to eat. Some plants go so far as to collude with their enemy's enemy. When spider mites start feeding on a lima bean plant, the plant emits a blend of volatiles. These chemicals attract another species of spider mite, a carnivorous one that eats the first population. Alliances make for strange bedfellows. Ants steal nectar from flowers. But most ants have a natural disinfectant that kills pollen sperm; typically, ants are not good pollinators. Plants sometimes respond by erecting barriers between the ground and the flower, sticky zones on the upper part of a stem or pools of dew that surround a stem and stop climbing insects like ants. Plants also offer decoy nectaries, set away from the flower. In some flowering species, these supplies of nectar are exchanged for a guard of stinging, biting ants that protect the flower from other egg-laying insects or from corolla-piercing bumblebees. The flowers must also protect themselves chemically from their own guard ants, which are still thieves and cannot be allowed too close. This is another parable of mutualism. Or another example of criminal racketeering. We will find a story and a meaning in this because we are human and because story and meaning infuse our lives, just as scent infuses the life of the bumblebee. *** IN THE EIGHTEENTH century, mutualism was a parable, of the perfect adaptations created by God. In a divinely balanced Nature, each creature had an unchanging role. All the parts of Nature worked together harmoniously, cooperatively, much as the parts of a human system should work together, each in his or her place, from peasant to king. Science often reflects society, and we often want society to reflect what we know about the natural world. In the nineteenth century, the Industrial Revolution and new ideas of capitalism emphasized struggle in a healthy economy. Socialism and communism were counterresponses -- a belief in mutual and shared power. Today we still seesaw between these two ideas, in politics and in botany. Cooperation is nature's basic organizing principle. Competition is nature's basic organizing principle. In the environmental movement of the 1970s, biologists seemed to shift toward the former. They have shifted now toward the latter. One of these biologists recently wrote: Plant and animal pollinators are mutualists, each benefiting from the other's presence. But the mutualism is neither symmetrical nor cooperative. Indeed, pollination derives evolutionarily from relationships that were fully antagonistic. The goals of plant and animal pollinators remain distinct -- in most cases reproduction on one hand and food gathering on the other -- and this leads to conflict of interest rather than cooperation. Like sailors looking for land, scientists look for organizing principles. Physicists call it the grand unified theory. We are all looking for a grand unified theory. We all want the story that will organize the confusing parts of life. The idea that function includes beauty astonishes me. The idea that beauty includes violence knocks me for another loop.
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