The deer that passed through the mandala last night was careful in its choice of browse. The viburnum shrub had stored food in branch tips, readying itself for spring. These young tips were not yet toughened and woody. The shrub’s tender growth has now been robbed, digested, and reinvested in deer muscle or, if the nibbler was a doe, in the body of a fawn in her womb.
The deer had help. Freeing the food locked inside the tough cells of twigs and leaves requires a partnership between the very large and the very small. Big multicellular animals can nip off and chew woody material, but they cannot digest cellulose, the molecule that constitutes most plant matter. Microbes, tiny single-celled organisms such as bacteria and protists, are physically puny but chemically powerful. Cellulose does not give them pause. Thus is born a gang of thieves: animals that walk around and grind up plants, paired with microbes that digest pulverized cellulose. Several groups of animals have independently developed this plan. Termites work with protists in their gut; rabbits and their kin harbor microbes in a large chamber at the end of their gut; the hoatzin, an improbable leaf-eating bird from South America, has a fermentation sac in its neck; ruminants, including deer, have a huge bag of helpers in a special stomach, the rumen.
Microbial partnerships allow large animals to use the vast stores of energy locked up in plant tissues. Those animals, including humans, that have not entered into a deal with microbes are limited to eating soft fruits, a few easily digestible seeds, and the milk and flesh of our more versatile animal cousins.
The saplings in the mandala were pinched between the deer’s lower teeth and the tough pad on its upper jaw that takes the place of upper front teeth. The woody morsels were sent to the back teeth to be ground up, then swallowed. When these pieces hit the rumen they entered another ecosystem, a huge churning vat of microbes. The rumen is a sac that branches off the rest of the deer’s gut. All food, except the mother’s milk, is sent to the rumen before it can move into the rest of the stomach, then on to the intestines. The rumen is surrounded by muscles that churn the contents. Flaps of skin inside the rumen act like baffles in a washing machine, flipping the food over as it moves.
Most microbes in the rumen cannot live in the presence of oxygen. They are descendants of ancient creatures that evolved in a very different atmosphere. Only when photosynthesis was invented, about two and a half billion years ago, did oxygen become part of earth’s air and, because oxygen is a dangerous, reactive chemical, this poisoning of the planet wiped out many creatures and forced others into hiding. These oxygen-haters live to this day in lake bottoms, in swamps, and deep in the soil, eking out an existence in oxygen-free environments. Other creatures adapted to the new pollutant and, using an elegant sidestepping maneuver, turned the toxic oxygen to their advantage. Thus was born respiration using oxygen, an energy-liberating biochemical trick that we have inherited. Our lives therefore depend on an ancient form of pollution.
The evolution of animal guts gave the oxygen-hating refugees a potential new place in which to hide. Not only are guts relatively free of oxygen, they also have every microbe’s dream: a continual supply of minced food. But there was a problem. Animal stomachs are generally full of acidic digestive juices designed to tear apart living tissue. This prevented most animals from harboring plant-digesting microbes. However, the ruminants changed their stomachs, mastering the hotelier’s art, and they have been rewarded by a four-star rating of evolutionary success. The centerpiece of this hospitality is the position and friendliness of the rumen, which comes before the rest of the gut and is kept neutral, neither acid nor alkaline. Microbes thrive in this churning spa. The animal’s saliva is alkaline, so the acidic products of digestion are neutralized. Any incoming oxygen is soaked up by a small team of bacterial chambermaids.
The rumen functions so well that scientists equipped with the most sophisticated test tubes and vats have not been able to replicate, let alone beat, the growth rate or digestive prowess of the rumen’s microbes. The rumen’s performance is due to the exquisite biological complexity that thrives in its pampered chambers. A million million individual bacteria of at least two hundred species swim through every milliliter of rumen fluid. Some of these microbes have been described; others await description or discovery. Many of the microbes are found only in rumens, presumably having diverged from their free-living ancestors during the fifty-five million years that have passed since the rumen’s origin.
Within the rumen, the bacterial proletariat is preyed upon by a bevy of protists, all of which are single-celled but hundreds or thousands of times bigger than the bacteria. Fungi parasitize these protists, infecting then bursting the fat cells. Other fungi float free in the rumen fluid or colonize scraps of plant material. The diversity of life in the rumen makes possible the complete digestion of the plant remains. No single species can fully digest a plant cell. Each species takes a small part of the overall process, chopping up its favorite molecules, harvesting the energy it needs to grow, and then sending back its wastes to the rumen fluid. These wastes become another creature’s food, building a cascading web of disassembly. Bacteria destroy most of the cellulose, aided by some fungi. Protists have a special fondness for starch grains, perhaps regarding them as potatoes to accompany their meal of bacterial sausages. Nutrients in the rumen are passed up a miniature food web, then released back into the rumen’s fluid, mimicking the nutrient cycles of larger ecosystems. The deer’s belly contains a mandala of its own, an intricate dance of lives, sustained by hungry lips and teeth. Young ruminants must build their rumen community from scratch, a process that takes several weeks. During this time, they nibble their mother, the soil, and the vegetation, gathering and swallowing the microbes that will become their helpers.
The rumen’s ecosystem is a self-sacrificing mandala, embodying endless change. Microbes are carried out of the rumen along with digested plant cells. They travel to the second part of the deer’s stomach and are swamped with acid and digestive juices. For these microbes, the gut’s hospitality has ended. The innkeeper kills and digests them, pocketing their proteins and vitamins along with the liquefied plant remains.
The rumen retains plant solids and the microbes that cling to them, ensuring both the complete digestion of the plant and the continuity of the rumen’s microbial community. The deer hastens the breakdown of these solids by bringing them back into its mouth, chewing the cud, then swallowing the pulverized remains. This rumination allows the deer to “wolf” down its food, literally on the hoof, then chew it in a safe hiding place, away from real wolves.
As the seasons change, the deer’s browsing moves from one part of the plant to another. The woody food of winter will change to springtime greenery, then autumn acorns. The rumen adapts to these changes through the gradual waxing and waning of the members of its community. Bacteria suited to digestion of soft leaves increase through the spring, then taper away in winter. No top-down control by the deer is needed to direct this change; competition among the rumen inhabitants automatically matches the rumen’s digestive capabilities to the food available. But sudden changes in diet can disrupt this elegant molding of the rumen community to its environment. If a deer is fed corn or leafy greens in the middle of winter, its rumen will be knocked off balance, acidity will rise uncontrollably, and gases will bloat the rumen. Indigestion of this kind can be lethal. Young ruminants face a similar digestive problem when they suckle their mother’s teats. Milk would ferment and create gas in the rumen, especially in immature animals whose rumens have yet to be fully colonized by microbes. The sucking reflex therefore triggers the opening of a bypass that sends milk past the rumen, into the next part of the stomach.
Nature seldom throws rapid dietary change at ruminants, but when humans feed domesticated cows, goats, or sheep, they must address the rumen’s needs. These needs do not necessarily conform to the desires of human commodity markets, so the rumen’s balance is the bane of industrial agriculture. When cows are taken from pasture and suddenly confined to feedlo
ts to be fattened on corn, they must be medicated to pacify the rumen community. Only by stamping down the microbial helpers can we try to impose our will on the cow’s flesh.
Fifty-five million years of rumen design versus fifty years of industrial agriculture: we face questionable odds.
The deer’s effects in the mandala were subtle. At first glance, shrubs and saplings appear unmolested. Only close observation reveals the missing tips of branches and the short, amputated stubs of side shoots. About half the dozen shrub stems in the mandala have been trimmed, but none of them have been cut back to stumps. I infer that deer and their microbial companions are frequent visitors to the mandala, but the deer are not starving. They can afford to nibble the succulent ends of twigs, leaving the woody stems behind. This choosiness is becoming a threatened luxury among white-tailed deer in the eastern forests. Across much of the deer’s range plant defenses are deployed in vain: deer populations have expanded rapidly, and the teeth and rumens of these growing hordes have sterilized the forest of saplings, shrubs, and wildflowers.
Many ecologists claim that the recent growth of the deer population is a continentwide catastrophe. Equivalent, perhaps, to throwing corn into a winter rumen; the community is thrown into an unnatural disequilibrium. The case against the deer seems unassailable. Deer numbers are growing. Plant populations are in decline. Shrub-nesting birds cannot find nest sites. Tick-borne diseases lurk on suburban lawns. We have eliminated predators, first Native Americans, then wolves, then modern hunters, whose numbers dwindle each year. Our fields and towns have cut the forest into ribbons and rags, creating the edge habitat in which deer love to feed. We have carefully nurtured deer populations with game-protection laws that time the hunting season to have the smallest possible effect on the deer population. Surely the forest’s viability is endangered?
Perhaps, but a longer view adds some mists of uncertainty to this black-and-white portrait of the role of deer in the eastern forests. Our cultural and scientific memories of what a “normal” forest should look like arose at a peculiar moment in history, a moment when deer, for the first time in millennia, had been extirpated from the forest. Large-scale commercial hunting in the late nineteenth century edged the deer population toward extinction. Deer were eliminated from most of Tennessee, including from this mandala. No deer visited the mandala between 1900 and the 1950s. Then, releases of deer transplanted from elsewhere, combined with elimination of bobcats and feral dogs, gradually pushed the population of deer upward until the 1980s, when deer were once again abundant. A similar pattern was replicated across the eastern forest.
This history distorts our scientific understanding of the forest. Most of the scientific studies of eastern North American forest ecology in the twentieth century were conducted in an abnormally unbrowsed forest. This is especially true of the older studies that we use as a benchmark to measure ecological change. The benchmark is misleading: at no other time in the history of these forests have ruminants and other large herbivores been absent. Our memory, therefore, recalls an abnormal forest, limping along without its large herbivores.
Disquieting possibilities grow out of this history. Wildflowers and shrub-nesting warblers may be experiencing the end of an unusual era of ease. “Overbrowsing” by deer may be returning the forest to its more usual sparse, open condition. The surviving diaries and letters of early European settlers lend some support to these ideas. Thomas Harriot wrote from Virginia in 1580 that “of… deare, in some places there are great store”; Thomas Ashe reports in 1682 that “there is such infinite herds, that the whole country seems but one continued park”; Baron de La Hanton continues this theme in 1687: “I cannot express what quantities of deer and turkeys are to be found in these woods.”
The writings of these European colonists are suggestive but hardly definitive. Their letters may be biased by boosterism for the colonists’ project, and they were entering a continent whose human occupants, most of whom were hunters, had just been decimated by disease and genocide. But the stories of genocide survivors and the archaeological evidence left by their ancestors suggests that deer were abundant even before the Europeans arrived. Native Americans cleared and burned forests to encourage the growth of young vegetation that, in turn, fired the deer’s fecundity. Deer meat and hides made human life possible in the winter, and deer spirits danced through the mythology of these first human inhabitants of the Americas. Historical and archaeological information therefore all points to the same conclusion: deer were plentiful inhabitants of our forests before guns removed them in the 1800s. The deerless forests of the early and middle 1900s were aberrations.
The case against our modern deer phobia deepens when we look back beyond the arrival of humans on this continent. Temperate forest has been growing in eastern North America for the last fifty million years. In those ancient times, the forest grew in a thick band across Asia, North America, and Europe. This swath was cut into fragments by the cooling of the earth’s climate, especially by the periodic ice ages that pushed temperate forests southward, then drew them northward as the ice retreated. Now, the remnants of this forest grow in widely separated patches in eastern China, Japan, Europe, the Mexican highlands, and eastern North America. The temperate forest’s dance across the continents has one unvarying theme: the presence of mammalian browsers, often in large numbers.
The deer that walked across the mandala is one of the last representatives of a much larger plant-trimming bestiary. Giant ground sloths hulked their rhino-sized bodies around the forest, browsing vegetation. They were accompanied by woodland musk oxen, giant herbivorous bears, long-nosed tapirs, peccaries, woodland bison, several species of extinct deer and antelope, and, most dramatic of all, the mastodons. The mastodons were relatives of the modern elephant, with tusks and a broad, low head. They stood three meters tall at the shoulder and browsed through the northern edge of the eastern forest. They, like many other large herbivores, went extinct at the end of the last ice age, about eleven thousand years ago. The ice ages had come and gone before, but this thaw brought with it a new predator, humans. Shortly after the arrival of humans, most of the large herbivores were gone. The smaller mammals were minimally affected by this extirpation; only large, meaty creatures disappeared.
Fossil evidence of these large herbivores abounds in caves and swamps across the eastern United States. These fossils provided fuel for the nineteenth-century debate about evolution. Darwin thought these animals were further evidence for the idea that the natural world is always in flux. He commented, “It is impossible to reflect on the state of the American continent without astonishment. Formerly it must have swarmed with great monsters; now we find mere pygmies compared to the antecedent, allied races.” Thomas Jefferson disagreed, believing that giant sloths and other creatures must still be alive. After all, why would God create them, then kill them off? Creation reflected God’s perfect handiwork, therefore nature would unravel if pieces were allowed to fall away. Jefferson instructed the explorers Lewis and Clark to bring back reports of these creatures from their trek to the Pacific coast. The expedition found no evidence of living mastodons, sloths, or any other extinct creatures. Darwin was right; pieces of creation can be destroyed.
Like the footprints left by the deer’s visit to the mandala, the passing herbivores have left signs in the architecture of some of our native plants. Honey locust and holly trees have thorny stems and leaves. These thorns are deployed only to three meters’ height, twice as high as any living herbivore can reach but exactly the right height to deter the extinct mega-browsers. The honey locust is doubly lost because its seedpods, which are two feet long, are too large for any living native species to consume whole and thus disperse the seeds, although they are perfectly sized for large extinct herbivores such as mastodons and ground sloths. Osage orange’s milky softball is another fruit whose seed-dispersing partner has died. Similar fruits on other continents are eaten by elephants, tapirs, and other large herbivores of the kind that exist only
as fossils in North America. These widowed plants wear history on their sleeves, giving us a glimpse into the bereavement of the whole forest.
The structure of ancient forests is forever hidden from us, but the bones of extinct browsers and the stories of the first Americans suggest that this was not an easy place for shrubs and saplings to thrive. North American forests have experienced fifty million years of browse, followed by ten thousand years of drastically reduced mammalian herbivory, then one hundred strange years of no browse at all. Might the ancient forests have been patchy and sparse, kept trimmed by herds of wandering herbivores? Certainly these herbivores had enemies of their own, which are now gone, or almost so. The sabertooth cat and the dire wolf are extinct; the gray wolf, mountain lion, and bobcat are rare. In the western United States, the giant American lion and the cheetah both preyed on the plant browsers. The existence of these many species of large carnivore is further evidence of the abundance of herbivores. Giant cats and wolves need giant herds of food. The only places in the world that sustain large populations of carnivores are well endowed with browsers. After all, carnivore flesh is just plant matter passed up the food web. So, abundant fossil evidence of large predators is strong evidence for heavy browse on plants.
Humans have eliminated some predators but have lately added three new deer-slaying creatures: domestic dogs, immigrant coyotes invading from the west, and automobile fenders. The first two are effective predators of fawns; the latter is the main suburban killer of adults. We face an impossible equation. On one hand, we have the loss of tens of species of herbivores; on the other we have the replacement of one type of predator by another. What level of browse is normal, acceptable, or natural in our forests? These are challenging questions, but it is certain that the lush forest vegetation that grew in the twentieth century was unusually underbrowsed.
The Forest Unseen_A Year's Watch in Nature Page 4
