Did Nature have in view our delectation when she made the apple, the peach, the plum, the cherry? Undoubtedly; but only as a means to her own private ends. What a bribe or a wage is the pulp of these delicacies to all creatures to come and sow their seed! And Nature has taken care to make the seed indigestible, so that, though the fruit be eaten, the germ is not, but only planted.
—John Burroughs, Birds and Poets (1877)
“Murciélago,” José breathed. “A bat!” And for the first time in our long work together I saw his cool reserve give way to something like wonder. The almendro seeds lay on the ground before us, grouped together in a loose pile. Where we usually felt lucky to find one or two, this trove held more than thirty—a veritable mother lode. And yet we knew there wasn’t a mature almendro tree within half a mile (eight hundred meters), too far for any rodent to carry such a horde. I knelt down and we began collecting the seeds, placing each one in a carefully numbered plastic bag. They were still fresh, their hard shells surrounded by a thin green pulp chewed into damp strands. Looking up, I already knew what I would see—the drooping, twelve-foot (four-meter) frond of a young palm tree, favorite perch of the largest fruit bat in Central America.
With a wingspan stretching to eighteen inches (forty-five centimeters), the great fruit-eating bat has more than enough flapping power to carry off almendro seeds. In flight, those huge wings make its four-inch (ten-centimeter) body look like an afterthought—just enough bones and skin to hold on to a heavy load. While fruit-eating bats often dine on figs, flowers, or pollen, the pile before us proved that almendro was something special—for the bat, and for the tree itself. Unlike squirrels and agoutis, who eat and destroy any seed they don’t misplace, the fruit-eating bat’s interest is entirely eponymous. It wants only the thin, watery flesh that surrounds the shell. Perched upside down, with sharp teeth working furiously, a bat can scrape away the pulp from the husk in minutes, dropping the seed unharmed to the forest floor below.
To me, eating almendro fruit was like gnawing on a bland, over-ripe snap pea, toughened by sun. But for the bat (or bats) that had roosted here, it was a taste sensation worth thirty round-trip flights. And worth the risk of returning again and again to a tree where owls, bat falcons, and pythons lurked, waiting specifically for an opportunity to snatch the unwary visitor. That element of danger played a vital role in the system. Without it, the bats would simply lounge in the almendro itself, gorging on fruit and dropping the seeds directly below the mother tree—unharmed, but undispersed. (Monkeys do exactly that during the daylight hours, as do smaller bats incapable of lifting the heavy fruits.) But so long as predators staked out the trees, any bat large enough would carry its prize away to the safety of a feeding roost, creating a pattern of seed dispersal so distinctive that José and I came to know these bats’ every move, without ever laying eyes on one.
I glanced again at the empty palm leaf above us before we walked on. It was a familiar sight. To confirm our hunch, we had looked up in exactly the same way nearly 2,000 times, comparing the locations of palm leaves to the locations of seeds. Whether we found them singly, in pairs, or in troves like this one, our largest yet, the dispersed progeny of almendro were twice as likely to lie beneath a bat roost. (The bats chose palm fronds for good reason: the drooping leaflets hid them from predators above, while the long, spindly stalk would shake with warning if anything tried climbing up from below.) This pattern held everywhere we looked—in isolated patches as well as large swathes of virgin forest. Back in the lab, genetic fingerprinting helped me take the data further. By tracking particular seeds from tree to roost, I could show that a bat would fly almost anyplace that an almendro came into fruit. Even trees stuck in the middle of pastures were part of the network, attracting hungry bats and co-opting them into carrying their seeds to better habitat thousands of feet away. With large rainforests disappearing, our results gave me hope that almendro—and the many species that depended on it—could persist in this new landscape of fragments, farms, and pastures.
Hiking back along our transect, we passed suddenly into blinding sunlight where the forest ended in a straight green line. Rank grassland stretched away over rolling hills dotted with remnant trees, some of them almendro. We knew the area well and weren’t surprised to see the landowner, Don Marcus Pineda, leading a donkey across a nearby field. He waved and turned in our direction. Pineda owned a lot of property and still worked it himself, clearing trees, mending fence lines, and tending a large herd of beef cattle. As he neared, I smelled something chemical from the sloshing yellow jugs strapped to the donkey’s packsaddle. Pineda told us he was heading out to spray some bracken, a prolific, inedible fern he wanted gone from his rangeland. But we knew there was more news, or he wouldn’t have gone so far out of his way to greet us. Finally, he spoke again.
“El Papa ha muerto,” he said simply—“The Pope is dead.” Marcus Pineda lived on a rugged frontier farm near the Nicaraguan border, and had always struck me as machismo personified—a tough, lined face squinting out from beneath his ever-present cowboy hat. But it was obvious this loss had hit him hard, and it shook José, too. For several minutes the three of us stood together quietly, heads bowed in the muggy heat. Pope John Paul II had been a hero in Costa Rica, where over 70 percent of the population identified as Roman Catholic. But he was more than a religious leader. His frequent trips to Latin America, his personal charisma, and his genuine interest in the region made him a beloved figure both inside and outside the church.
As a scientist, I, too, felt a fondness for John Paul. After all, he was the pope who finally pardoned Galileo, and he did more than any of his predecessors to reconcile church teachings with the theory of evolution. In discourses to the Pontifical Academy of Science, he had called Darwin’s ideas “more than a hypothesis,” and had gone so far as to imply that the Book of Genesis was allegorical, and not “a scientific treatise.” His words to the academy were brief, but if John Paul had spoken at length, he might have pointed out any number of metaphors in Genesis, many of them biological. The chapters concerning Adam and Eve, for example, do more than describe the dawn of humanity and original sin. They also tell one of the greatest seed dispersal stories of all time.
From the Renaissance forward, artists have made the scene indelible: Adam and Eve sharing a luscious apple below the Tree of Knowledge of Good and Evil, with a serpent coiled around the closest branch. Botanical purists point out that such large-fruited apple varieties didn’t become common until the twelfth century, and that the fruit should probably be a pomegranate. Whichever the species, the cunning snake had chosen a perfect lure, something that evolved for the sole purpose of temptation. To a hungry animal, the tiny pips inside an apple or the stone at the center of a date may seem irrelevant, secondary to the irresistible flesh. But the truth is the other way around. Fruit, in all its magnificent variety, exists for no other reason than to serve the seeds.
Whether a plant is growing in the Garden of Eden, in a tropical rainforest, or in a vacant lot, its investment in producing, nourishing, and protecting its seeds means nothing without dispersal. Offspring that languish on the mother or drop directly below amount to little more than a wasted effort. If they sprout at all, they won’t survive long in the shade of a fully grown parent. (In some cases, adults release toxins into nearby soil to prevent their progeny from becoming competitors.) For almendro, adding a thin layer of pulp to its seeds can entice fruit bats to carry them half a mile or more. The Tree of Knowledge did even better. According to Genesis, eating that Forbidden Fruit resulted in Adam and Eve’s immediate expulsion from Eden. Metaphorically, at least, the fruit went with them. Some depictions show the guilty couple still clutching a half-eaten apple. And if it was indeed a pomegranate, then the seeds would have been safely lodged in their digestive tracts. Either way, the Tree had put itself in a great position. With that one tempting fruit, it went from a garden-bound existence to the promise of mass dispersal with humanity across the face of the earth.
FIGURE 12.1. Albrecht Dürer’s 1504 engraving of Adam and Eve has it all—fig leaves, a tree, a snake, and the ultimate sign of temptation: fruit. Adam and Eve, Albrecht Dürer, 1504. WIKIMEDIA COMMONS.
Much has been written about the relationship between people and fruit or other crops—the way we take them with us wherever we go. Apples alone went from a single species domesticated in the mountains of Kazakhstan to thousands of varieties—people grow them on every continent outside Antarctica. It’s only a slight exaggeration to call us servants of our food plants, diligently moving them around the world and slavishly tending them in manicured orchards and fields. And it’s no exaggeration at all to call this activity seed dispersal. We do it as unconsciously as the bats do, living out an interaction between plants and animals that is nearly as ancient as seeds themselves. Fruit influences our behavior because it evolved to do so; developing flesh we find sweet and colors and shapes that attract our attention. Its power reaches beyond our farms and kitchens, touching beliefs at the boundary between culture and imagination. Look no further than the glut of grapes, pears, peaches, quince, melons, oranges, and berries festooning every basket and platter in the history of still-life art. Our desire for fruit makes it more than a symbol of temptation—it helps us to define beauty itself.
In nature, fruit is typically both delicious and fleeting, traits that help it attract just the right dispersers at just the right moment. People generally seek out sweetness, but plants can readily develop fruits to please other palates, producing proteins and fats as well as sugars. The rich packets adorning castor beans (and a host of other species) are designed to attract otherwise carnivorous ants, while the Kalahari Desert’s tsamma melon, ancestor to the watermelon, draws in all comers by satisfying a universal hot-country yearning: thirst. In any case, the desired flavor appears only as the seeds mature and prepare for departure. Before the seeds ripen, plants keep animals at bay with fruit that is bitter or downright poisonous. The physician who accompanied Christopher Columbus on his second voyage observed a group of sailors on the beach happily tucking into what appeared to be wild crabapples. “But no sooner did they taste them than their faces swelled, growing so inflamed and painful that they almost went out of their minds.” The men survived, but had probably been trying to eat manzanillo, a fruit the local Carib Indians harvested for making arrow poison. It remains toxic even when ripe, perhaps as a deterrent to insects or fungi, or to ward off all but a specialized (and as yet unknown) seed disperser. Poisonous, single-species strategies are unusual, however. Most fleshy-fruited species take the route of the apple, luring potential dispersers with something as widely desirable as the plant can afford to produce.
FIGURE 12.2. Apple (Malus domestica). An iconic symbol of temptation in everything from artwork to Bible stories to Snow White, apples play a role uniquely suited to fruit. In nature, fleshy fruits of all kinds evolved for the sole purpose of tempting animals into dispersing the seeds of plants. ILLUSTRATION © 2014 BY SUZANNE OLIVE.
“Affordability” may not sound like a botanical term, but balancing the household budget dominates the lives of plants. Energy, nutrients, and water are the coins of the realm, limited resources that must be divided among vital priorities. Spending a fortune on dispersal runs the risk of shortchanging the seeds’ nourishment or protection, not to mention the growth and defense of leaves, stems, and roots. In the world of plant economics, producing fleshy fruit is costly. Gardeners and farmers know this from experience—the “heavy feeders” in any vegetable plot always include the large-fruited crops like tomatoes, melons, squashes, eggplants, cucumbers, and peppers. Adding fertilizer or a scoop of compost tilts the balance, helping these species invest more in the production of something succulent. In the wild, plants scrape by with whatever the local soil and weather provide. But even in a good year, the huge expenditure of fruiting almost always makes the season brief, only adding to its cachet.
As one of the rarest, sweetest, and most nutritious things in the landscape, ripe fruit can draw animals from far and wide. African elephants trek miles out of their way to find favorite species like bitterbark, an odorous, cherry-sized fruit native to the Congo basin, or marula, a southern African delicacy related to mangos. In one forest, researchers mapped a network of elephant trails connecting every known adult of the balanites tree, even though it only bore fruit every two or three years. Our own species also goes to great lengths to take advantage of a wild harvest. Traditional San tribes-people in the Kalahari base their travel routes and seasonal encampments around the availability of tsamma melons, just as Australian Aboriginals in the Western Desert once did with figs, wild tomatoes, and quandong, a peach-like member of the sandalwood family. It’s not uncommon for similar fruit interests to put people and wildlife in direct competition. Friction between villagers and mountain gorillas in Uganda increases during omwifa season, when both apes and local residents hone in on the same wild groves to harvest the tree’s lumpy, aromatic fruits.
The allure of fruit begins with biology but endures in countless cultural references, from Chinese symbols for immortality (peach), wealth (grape), and fertility (pomegranate) to the traditional American token of welcome (a pineapple). Strawberries fed Freyja, the Norse goddess of love, while the Greeks paid tribute to Athena as the inventor of olives. In Southeast Asia, the Hindu deity Ganesh was famously fond of mangos, and the spreading boughs of the bodhi fig shaded both the birth of Vishnu and the enlightenment of the Buddha. (It’s a species so sacred that even taxonomists got the message, giving it the botanical name Ficus religiosa.) The bounty of the biblical Eden reflects a long tradition of describing Paradise as a decidedly fruit-laden place. In the words of the poet Hesiod, those fortunate enough to reach Greece’s famed Elysian Fields enjoyed “honey-sweet fruit flourishing thrice a year.” Islamic texts allude to eternal gardens filled with everything from dates, cucumbers, and watermelon to “the quince of Paradise.” Medieval Britons made matters even more plain, referring to the mythical homeland of King Arthur as Avalon, from the Welsh for “Island of Apples.” Scholars of etymology trace the very word Paradise to a Persian term for a walled enclosure that early Hebrews adopted to mean “fruit garden,” or simply “orchard.” But perhaps the best example of our esteem for fruit comes from English, where any successful venture is considered fruitful, and failures are known as fruitless.
With fruit so powerfully embedded in language and culture, it’s easy to forget that from a functional standpoint, sweet flesh is simply window dressing for seeds—an elaborate means of travel from here to there. The technical term for fruit dispersal is endozoochory, which would sound far more elegant if everyone still spoke ancient Greek: “going abroad within animals.” (We scientists have a great fondness for long mash-ups in dead languages. When a bat moves an almendro seed, for example, the proper description is chiropterochory: “going abroad with an animal whose hands resemble wings.”) This form of exploitation evolved early in the history of seed dispersal, almost as soon as there were creatures large enough to get the job done. Back in the Carboniferous Period, the forests that Bill DiMichele now studies on the ceilings of coal mines harbored a relatively modest community of insects, amphibians, and early reptiles. But seed ferns and primitive conifers soon pioneered a range of strategies to ensnare them, from small, skinny seed packets, which may have attracted millipedes, to fleshy seeds the size of mangos, which probably stank like rotten meat, a siren call to ancestral dinosaurs. Echoes of that era remain in the pungent seeds of ancient survivors like ginkgos, whose reek is so strong that many cities ban the planting of female trees. Virtually every ornamental ginkgo in the world is a male, producing nothing more offensive than odorless pollen.
Botanically speaking, early seed plants lacked the specific tissues that would qualify as a true “fruit.” But that didn’t stop them from developing analogs that worked just as well—sweetening the outer layer of a seed coat, for instance, or putting flesh on a nearby stem or bract. Modern conifers and other gymnosperms continue that tradition, as gin drinkers know well from the pulpy, aromatic cones known as juniper “berries.” But while animal dispersal remains common in gymnosperms, most familiar fruits evolved with the angiosperms—the flowering plants—whose seeds came in a package, by definition. That covering opened up a world of fruity possibilities, and it arose right alongside an explosion in the availability of dispersers. Birds, mammals, and flowering plants all experienced what taxonomists call a radiation, a rapid increase in species, immediately following the extinction of the dinosaurs. And while older groups, like lizards, insects, and even fish, continue to disperse seeds, the vast majority of fleshy fruits are meant to attract—and go abroad with—birds and mammals.
The best way to appreciate fruit diversity involves a simple experiment that most of us undertake several times a week: shopping for groceries. Even a tropical rainforest can’t compare to the density of species arrayed in a typical supermarket produce aisle. My home-town grocery store has been on the same block since 1929, strategically located between two other longtime businesses—the drugstore and the local tavern. On a recent spring morning, the shelves boasted seventy-one varieties of fresh fruit from thirty-nine distinct species. The smallest was a blueberry no larger than my thumbnail. Produce departments now stock them year round, but in the wilds of North America, where blueberries evolved, their ripening coincides with fall bird migrations and the pre-hibernation fruit-gorging of bears. At the other end of the spectrum, I found a bin of watermelons that weighed up to fifteen pounds (seven kilograms) each. Their tsamma melon ancestors ripen during the dry season in southern Africa, providing essential water for everything from antelopes to hyenas to people. Every fruit in the store told some version of the same story—a wild scenario made commonplace by the efficiencies of modern agriculture. Of course, many tree fruits are now propagated by cuttings, and most of the seeds in the store would eventually end up in someone’s compost bin or septic system, but their mere presence demonstrated the success of the fruiting strategy. The everyday bonanza of grocery-store produce is something like extreme dispersal in action—the fruits on display had come from as far away as Italy, Chile, and New Zealand. But they were not only well traveled. They also served as a lesson on the range of ways that flowering plants make fruit, from the obvious—like the sweet flesh of an apple—to the ones that most people haven’t really thought about—like the juice-filled hairs inside an orange, or the strawberry, whose shape and flavor come from a swollen flower base, which is why the seeds perch so oddly on the outside of the fruit.
The interplay between fruits and their dispersers affects every partner in the dance. It influences dietary habits and migration patterns as well as the timing of reproduction—for both the animals and the plants involved. But the adaptations can be much more specific. The teeth of fruit bats, for example, evolved from insect-eating cleavers into a bite with angular surfaces designed to crush and pulverize. Guenons and vervet monkeys have special pouches that stretch from their cheeks down the sides of their necks, allowing them to stuff in huge loads of fruit for safe consumption later. Startle one of these monkeys at a fruiting tree, and your last sight of it will be a distinctly bulging face leaping away through the canopy. Fruit-eating birds have developed everything from wider beaks and flexible throats to shorter intestines for processing abundant fruit supplies quickly. Parrots counter the toxins in unripe fruits by gobbling up clay rich in kaolinite, the same mineral that formed the original basis for the stomach-soothing tonic Kaopectate. I’ve watched Cedar Waxwings eat clay, too, which is hardly their only fruity distinction. They digest berries so quickly that their droppings are still sweet (which led them to develop unique rectums that absorb sugars just as well as their intestines do).
Plants, in turn, have learned to tailor their strategies to attract particular types of dispersers. Birds appreciate prominent splashes of red or black (raspberry, blackberry, cranberry, black currant, hawthorn, holly, or yew), but odor is more important for drawing in animals that are color-blind (elephants), nocturnal (bats), or whose noses are sharper than their eyes (tortoises, opossums). The pits and pips at the centers of fruit boast some of the hardest seed coats in nature, tough enough to withstand scraping, chewing, and the chemical scour of digestion. In fact, being eaten by a disperser enhances the germination of fruit seeds twice as often as reducing it. When an elephant chews the fragrant fruit of a South African marula tree, its tremendous teeth loosen woody plugs in the pit, an essential step that later allows the seed to imbibe water and sprout. The exact benefit isn’t always so clear, but digestion boosts the germination of everything from the cherries devoured by bears to the prickly-pear cactus preferred by the Galapagos tortoise. Some combination of chemical change and physical abrasion probably helps to break the seeds’ dormancy, and then there’s the end result: depositing those seeds in a warm pile of fertilizing dung. In some cases, other creatures then gather up the seeds and disperse them farther. Tree squirrels do it with the marula nuts from elephant piles, and deer mice scatterhoard the chokecherries and dogwood seeds they find in bear poop. But the most notorious example of this process takes us back to the world of gourmet coffee, where people pay up to $300 per pound ($650 per kilogram) for coffee beans plucked from the turds of the Asian palm civet. A single cup in a trendy Manhattan café can set you back nearly $100. That high price tag has inspired lucrative spin-offs from the poop of other species known to nosh coffee berries: elephants in Thailand, Peruvian coatis, and a turkey-like Brazilian bird called the Dusky-legged Guan. (Unfortunately, the civet coffee boom has also resulted in cruel schemes to force-feed caged animals. When the topic came up during my visit to Slate Coffee Bar in Seattle, barista Brandon Paul Weaver dismissed the whole craze with a memorable line: “Coffee from assholes, for assholes.”)
Dispersal by way of tasty flesh occurs in nearly a third of all plant families, from cycads to squashes to citrus. The strategy evolved again and again in different settings, because when it works, the results are dramatic. A thirsty brown hyena, for example, can eat eighteen tsamma melons in a single night, dropping their seeds over a home range as large as 150 square miles (400 square kilometers). Brown bears in a blueberry patch do even better, munching their way through 16,000 of the tiny fruits in a matter of hours. Since each berry contains an average of thirty-three seeds, that puts the blueberry dispersal rate of a single hungry bear at more than half a million seeds per day. Examples abound, and whole scientific careers have been happily devoted to exploring the nuances. But the fact remains that most seeds travel by other means.
For the vast majority of plants, seed dispersal represents the one moment of mobility in an otherwise stationary life. It determines what grows where, a fundamental organizing principle of ecosystems. As such, the process carries great evolutionary consequence, and seed plants have been coming up with variations on the theme for close to 400 million years. Fruit offers a reward, but other seeds simply hitchhike, using hooks, spines, or stickiness to catch a free ride on the exterior of an animal. (The commercial form of this strategy is known as Velcro, a product inspired by the way burdock seeds stuck to the fur of the inventor’s dog.) Some seeds launch from exploding pods, while others drop into water and drift with the tide. For many people, the most familiar dispersal experience comes from the poke of grass seeds lodged in a sock. They work their way inward with every step, eventually becoming so unbearable you’re forced to stop, pluck them out, and throw them on the ground. Mission accomplished.
In Costa Rica, José and I learned that almendros move around with help from the wings of bats. But long before bats even existed, seeds had learned to grow wings of their own. Whether gliding, twirling, wafting, or soaring, riding the wind is the most ancient form of seed dispersal, and it remains the most common. With all that practice, plants have developed means of flight (and in some cases, flotation) that transport seeds in quantities, and over distances, never dreamed of by bats, bears, or birds. The results do more than organize the placement of shrub, herb, grass, and tree. They give us yet another chapter in the long story of seeds and people—how papery wings and bits of fluff influenced everything from aeronautics and fashion to the history of industry, the British Empire, and the American Civil War. And like so many biological tales, the best place to start lies in the notebooks and journals of a certain young naturalist in the Galapagos Islands.
