The Power of Ecosystem Engineers

After 5 years exploring the world aboard the H.M.S. Beagle, English naturalist Charles Darwin retreated to a country home in Kent to ponder all that he had observed and to develop what would become his theory of evolution. Oddly enough, he also began then a lifetime study of earthworms. In 1837, only a year after stepping off the Beagle, Darwin appeared before the Geological Society of London and asserted "that all the vegetable mould over the whole country has passed many times through, and will again pass many times through, the intestinal canals of worms."1 By vegetable mould, Darwin meant what we call humus, the dark, rotting organic matter that harbors much of the nutrient wealth of soil.

Critics quickly objected that worms are far too small and weak to produce such a large impact on soil. This struck a nerve with Darwin. "Here we have an instance of that inability to sum up the effects of a continually recurrent cause, which has often retarded the progress of science," he wrote many decades later, after facing similar objections to his theory that natural selection, acting on slight inherited differences, among individuals over untold generations, gives rise to new forms of life.2 Darwin would spend more than four decades studying worms, confirming the power wielded by large numbers of little things working over time. Although he did not label the work of worms good or bad, his writings helped burnish the positive image that earthworms enjoy today. It wasn't always so.

Earthworms have endured great swings in reputation through the ages. Aristotle called them the "earth's entrails" because they digested soil and debris, and like the early Egyptians, he believed they promoted soil fertility.3 But over the centuries, it seems, worms slipped in farmers' estimations into the ranks of pests and destroyers of crops. By the 18 th century, English parson and naturalist Gilbert White felt the need to defend earthworms against the "detestation" of gardeners and farmers—gardeners because they lamented the "unsightly" mess worm castings made of their garden paths, and farmers because they believed wrongly that "worms eat their green corn." In truth, White wrote, "the earth without worms would soon become cold, hard-bound, and void of fermentation; and consequently sterile."4 Today, earthworms receive little but good press in popular gardening magazines. They are among the few soil creatures that almost everyone recognizes and almost universally regards as "good"— industrious and benign icons of soil fertility. A sign I noticed on one museum exhibit on biodiversity summed up the popular wisdom: "If you spy a lot of earthworms in the ground, you're probably looking at healthy soil."5

That's why, when Cindy Hale gets up to talk about earthworm damage in Minnesota's maple forests, her audiences usually respond with open-mouthed disbelief. Most of her listeners are as unaware as I was that the worms in our northern gardens, fields, and forests are not natives. There are no native worms across most of the upper swath of North America, I soon learned, a void that some scientists blame on the advance and retreat of Pleistocene glaciers (1.8 million-11,000 years ago). Our night crawlers, leaf worms, red wigglers, and other common backyard worms are mostly European invaders that hitchhiked here a century or more ago in ship ballast or on the root balls of imported plants and then settled into human-dominated landscapes. In recent decades, earthworm introductions to natural areas have accelerated as the import of bait worms for sport fishing and compost worms for vermiculture (raising earthworms to compost organic waste) has grown into a multimillion-dollar industry. Hale, a research associate at the Natural Resources Research Institute, University of Minnesota, Duluth, for example, has been watching invasion fronts of exotic bait worms fan out from fishing resorts and boat landings into Minnesota's previously worm-free north woods. She explains to audiences how the advancing worms devour the thick duff of the forest floor and make life difficult or impossible for many native wildflowers, tree seedlings, and small creatures above and below the ground.

"After they get beyond disbelief, people wrinkle up their foreheads and ask: 'So, does that mean earthworms are bad?'" Hale recounts. "I say, 'They're not bad or good. Worms just do what they do, and in some places we like what they do and in some places we don't like what they do. It's not a yes or no question.'"

In fact, the more I learned about what earthworms do, the more naïve it began to seem to caricature these complex and influential creatures as helpful or harmful, as I had once done. Although misplaced worms are causing unwanted disturbances in many natural habitats, in other parts of the world researchers are learning to harness their powers to restore fertility and enhance crop production on degraded lands.

Biologists have long described the earth's 3,000-4,000 earthworm species as "bioturbators" because of their earth-churning ways. But worms do more than plow through the soil, swallow dirt, and excrete it some distance away. Worms swallow and break up leaf litter, organic debris, and microorganisms, living and dead. Inside the worm, this fragmented organic material is mixed with soil, digestive juices, and mucus, creating a feast for gut-dwelling microbes, as well as other decomposers that survive the passage. Beneficial microbes such as nitrogen-fixing bacteria and mycorrhizal fungi get moved from place to place by passing through worms, too, as do disease agents and their natural enemies. Worms cast or excrete enriched, gummy soil in the form of tiny clumps or aggregates, creating hotspots

Earthworm Mucus Composition
Earthworms are called "ecosystem engineers" because their burrowing not only churns the soil but also changes the habitat of other plants and animals, for better or worse.

of biological activity and enhanced nutrient cycling that influence the composition and perhaps the species diversity of the soil community for weeks or months. Further, as worms burrow and feed, they usually increase the porosity of the soil, aerating it, improving its structure and water-holding capacity, and creating channels for water to drain and roots to penetrate. Thus, earthworms are not just biological plows. They create and modify habitat and alter the resources available to other creatures in their sphere of influence—called the "drilosphere" —just as plants do in the rhizosphere, the neighborhood adjacent to their roots where microbes thrive on exuded sugars.6

Although ecologists have long focused on predation, competition, parasitism, and symbiosis as key interactions that shape ecosystems, habitat creation was not singled out for study until the early 1990s. That's when ecologists came up with a descriptor for creatures that engage in it: "ecosystem engineers." With that, earthworms took their place amid the ranks of beavers, elephants, woodpeckers, prairie dogs, gophers, ants, termites, burrowing shrimp, and other earth-moving creatures whose routine activities both transform the character of the land and the seabed and shape the vital ecological processes that take place above and below ground.7

Although Darwin didn't use the word, it was the engineering work of worms that fascinated him most. He purposely placed chunks of stone on the surface of a pasture near his house and waited 29 years to see how deeply worms would bury the material by bringing up deeper soil layers and casting it on the surface (7 inches, he learned, or one-quarter inch per year). Similarly, with a remarkable detachment few of us could muster when it comes to our own landscaping, Darwin watched for more than three decades as a flagstone path in his lawn sank and finally disappeared under layers of worm castings. Meanwhile, he meticulously monitored the actual weight of castings brought up each day from individual worm burrows. In the end, Darwin concluded that worms working underground were swallowing and bringing to the surface more than 10 tons of earth every year on each acre of English countryside.8 More than a century later, Patrick Lavelle of the Laboratoire d'Ecologie des Sols Tropicaux in Paris found that earthworms in the tropics can ingest as much as 200-400 tons of soil per acre per year.9

Lavelle and others recognize that soil engineers—and indeed, all soil animals—are resources that need to be tended, whether they are used as "therapy" for degraded lands, enhancers of crop production, or indicators of the ecological impact of agriculture and other human land uses. Like human engineering activities, however, the dams, tunnels, and earthworks of soil engineers—especially misplaced ones— can sometimes degrade rather than enhance our land and water. Hale is one of a growing number of ecologists, foresters, and land managers who are coming to recognize that releasing powerful creatures in the wrong places—or eliminating them from their native habitats—can wreak unwelcome changes in ecosystems we value.

Hale's answer to the uninitiated—school children, foresters, ecolo-gists, and skeptical writers alike—is to invite them into the sugar maple woodlands of Chippewa National Forest, a popular fishing and boating area in northern Minnesota. That's where I meet her one mid-morning in late June, in the little town of Cass Lake that serves as the national forest headquarters. At that time, she is just finishing up her doctorate on the impact of worms on these hardwood forests. A Du-luth native, Hale is a bit older than most graduate students, the result of what she genially calls her "nonlinear career." After earning an undergraduate degree in ecology, she "went off and did jewelry design for 5 or 6 years, and seasonal temp jobs all over on wolves, owls, plants, anything I could get." When she decided to go back to graduate school, it was to work on old-growth forests in Minnesota. Worms were not on her radar screen then.

Before heading into the woods, Hale and I and another curious writer stop for lunch at a modest resort with rental cabins and a marina. It's Friday, and trucks pulling trailered boats are already streaming past on Highway 2 from Duluth. The bait shops around Minnesota's 14,000 fishing lakes will do a brisk business this summer weekend in night crawlers and leaf worms (also called red worms), two European species known formally as Lumbricus terrestris and Lumbricus rubellus. By Sunday afternoon, thousands of fishermen will be trailering their boats again and dumping any leftover worms onto the ground near marinas and boat launch ramps. Unless, that is, they've seen the "Contain those crawlers!" posters Hale has been distributing. Her message is simple: Dumping worms in the woods harms the forest, and it's illegal. Dispose of leftover bait in the trash.10

It's the seemingly harmless act of bait dumping, repeated every weekend for decades, that has set in motion an unwelcome change in these woods, Hale recounts over lunch. Starting in the 1980s, soil scientist Dave Shadis and a handful of other biologists working in the Chippewa National Forest had noticed changes in the understory plant community at several sites. Maple seedlings were growing sparser, and so were ferns and wildflowers such as large-flowered trillium, yellow violets, bellworts, Solomon's seal, and wild ginger. It wasn't until 1995, however, that Shadis thought about worms as culprits. That year he read an article about the disappearing understory in New York's urban woods.11 The changes were occurring in wooded parklands overrun by earthworms. When Shadis went out to his own affected forest sites and dug, he found worms. In places where the un-derstory remained unchanged, he found no worms.

A few years later, Shadis led a group of ecologists on a field trip to see the contrast between worm-free and worm-infested woods. Hale, then a master's student, went along.

"Everybody was just blown away," Hale recalls. "Because most of us didn't even know worms weren't native or that they could have negative impacts. That's completely contrary to everything we've ever learned since we were this high"—she stoops to hold her hand at knee level—"about worms being these benevolent little creatures who just spend their time serving us."

When it came time for her to pick a Ph.D. topic in 1998, Hale remembered Shadis's observations and decided to pursue the worm connection with the help of her advisor, Lee Frelich, director of the University of Minnesota Center for Hardwood Ecology.

"It's been rewarding," says Hale, who plunged into public education about worms as eagerly as she embraced the research. "The first few years, we were like voices in the wilderness. It's been as much a sociological experiment as a biological one, seeing how people—not just the lay community but the scientific community—react to this research and the implications of it."

After lunch, we drive east on Highway 2, then turn south down a bootleg-shaped neck of land called the Ottertail Peninsula that juts from the north shore into Leech Lake. We park at the edge of a wood and Hale begins unloading her gear: a long-handled garden bulb planter she uses for taking soil cores, a foot-square metal frame, two plastic jugs, and a large tub of ground yellow mustard purchased from a food co-op in Duluth.

The western shore of this peninsula is lined with fishing resorts built between the 1920s and the 1950s that are the source, apparently, from which the worms have been fanning out into the woods, she says.

"That's what we see across this region, a very distinctive pattern of these leading edges of worm invasion radiating out from sites like boat landings, fishing resorts, things like that," she explains as she fills the jugs with a dilute mustard and water solution. "People who had been watching the change in the understory vegetation—although they didn't link it to earthworms at the time—noted that the change jumped this road about 15 years ago. And now it's about 300 yards into this stand. So we're going to walk in, cross what we call the visible leading edge—which is where you start to see forest floor again—and then beyond to what we consider relatively worm-free conditions with thick forest floor and lush native plants."

By "forest floor," Hale means what is variously called vegetable mould (in Darwin's day), leaf mold, compost, duff, or among soil scientists, mor humus. It's a spongy, springy surface layer composed of many seasons worth of rotting leaves, twigs, bark, animal remains, and other detritus. If you push aside the identifiable leaves and other crispy bits in the upper inch or so, you will find a dark, slippery mat of skeletonized leaves and other older material that is slowly losing its identity and substance to the feeding of a threadlike network of white fungal hyphae. Worm-free sugar maple forests are known for their slow, thrifty nutrient cycling, and the carbon and nitrogen in a fallen leaf may sit locked away in the duff for 3-5 years like banked wealth before soil animals and decomposer microbes break the material down and release the nutrients for reuse.

Since nothing was known about the actual worm populations here when Hale began, her strategy was to pick several sites in Chippewa where the forest floor and the plant community were visibly changing, then mark off a series of plots at each site along a 500-foot transect running from the changed into unchanged forest. Ever since, she has been documenting shifts in the worm populations, forest floor, upper soil horizons, and understory plants as the worms march on. In the first 4 years of her study, the invasion front of worms advanced as much as 100 feet.12

It has rained heavily for the past week, and now the midday sun is enveloping us in steamy heat. We gladly follow her into the cool, dappled shade of the sugar maples. A thin layer of soggy leaves that dropped last fall still coats the bare ground. Hale predicts most of this litter will be gone in a few weeks. The worms at this heavily invaded end of the transect rev up the pace of nutrient cycling, consuming the whole year's leaf fall and incorporating the carbon and nutrients into the soil during the 2-3 months they are active. (Worms in Minnesota hunker down in the soil or litter and wait out the frigid winters. In the droughty summer months, some go into a torpid state called estivation—similar to hibernation, but in warm weather.)

A little farther into the woods, Hale kneels down and brushes aside the leaves.

"Underneath you see tons and tons of earthworm cast material —or worm poop—these granular, kind of globular piles of soil. You can see a lot of worm burrows exposed to the surface." She scoops up some material and holds out a 1-inch glob. "This is a piece of a midden, literally just a pile of cast material that night crawlers form around their burrow. And it often has lots of these little tufts of leaf petioles and veins because that's the remnants of the leaves that they've ingested and pulled down into their burrow."

She stands and pushes the bulb planter into the cleared spot with her foot, pulling out a 7-inch core of soil. She removes it from the metal tube and holds it up for us to see. "The A horizon is this black upper layer, about 5 inches thick," Hale explains. "Then below you can see it starts to grade slowly down to this buff-colored soil. This is the top of the E horizon where the organic materials are leaching down from this A horizon." At the worm-free end of this transect, she says, we will see a thick O (organic) horizon—the forest floor layer—

then a very thin or no A horizon atop a very thick, light-colored E layer. When worms arrive, they consume the organic layer, churn and work it in their guts, mix it with mineral soil, and excrete what becomes a thick A horizon.

A few days later, in an old-growth maple and basswood (linden) forest preserve called Wood-Rill just west of Minneapolis, Lee Frelich would tell me that soil scientists long mistook the thick A horizon at that worm-infested site for a "plow layer."

"They think these woods have been logged and farmed and abandoned back to woods," he recounted. "But as forest ecologists, we knew this site hadn't been logged. So how do you get a plow layer without plowing? Well, the answer is, earthworms are plowing." Frelich has spent most of his career studying the effects of fires and windstorms on forests. His attention turned to worms when the landowner who donated Wood-Rill as a preserve asked what had happened to the wildflowers he enjoyed as a child. "So I came out here and looked and discovered it was the worms," he recalled. "Then I had to get into the worm thing because obviously, we couldn't ignore it."

Both Frelich and Hale believe the worm invasion went unnoticed by land managers for too long because people trained in forestry seldom recognize changes in soil organisms, while soil scientists often don't know what the plant community should look like.

The dark soil Hale is holding out now looks to me like what I'd want in my garden, and I say so.

"That's exactly it," she agrees. "In fact, when I give talks to people, they say 'that looks like good, rich black garden soil.' And I say 'you're right,' because that's exactly what it is. But that's not what's supposed to be here in the native worm-free condition. And it changes everything, changes all the ground rules of the ecosystem. A lot of people say, 'but this is really good soil, why don't the native plants do better in this soil?'"

The general answer is that native plants have developed in the absence of earthworms at least since the retreat of the glaciers.

"So most of the native understory plants here root almost exclusively in the forest floor layer [organic horizon], and many have very complex seed germination and dormancy strategies. Some may take two or three freeze-thaw cycles for full germination, and during that time the seeds have to be protected from desiccation, freezing, predation. A forest floor does that really well."

As the total mass of earthworms has increased on her sites over the years, Hale has watched the abundance and diversity of wild-flowers and other herbaceous plants as well as the density of tree seedlings plummet. Sites where the forest floor was once at least three-fourths covered with lush greenery are now three-fourths bare ground. Earthworms have been primarily responsible, but an overabundance of deer has also taken a toll. Hale and Frelich theorize that some of the more robust native plant populations knocked back by the arrival of earthworms might eventually rebound, even in the face of heavy deer grazing. Some plants, such as sedges, even thrive with worms because, unlike most native plants, they do not depend on a partnership with mycorrhizal fungi, which can be disrupted by the activities of earthworms. Rare plants, on the other hand, may drop to such low numbers that they are driven locally extinct by the combination of worms and deer. The rare goblin fern, for example, a species that grows mostly between the duff layer and the mineral soil and does rely on mycorrhizae for sustenance, is likely to be completely eliminated from worm-invaded sites.13

We stop to look at some stalks rising from the ground. "These are wild leeks, one of the first things to come up in the spring." Hale pushes aside the sparse litter to reveal a small white bulb poking partially above the soil. The half-exposed leek bulb reminds her of another anomalous reality here.

"Contrary to everything you've heard about earthworms, we actually see an increase in soil compaction and bulk density [the weight of soil in a certain cube of space] as a result of earthworm activity," Hale says. "There's almost a doubling in bulk density in these sites relative to the worm-free sites."

I look skeptical. What about all the burrowing and casting that's supposed to increase the pore space and fluff the soil?

"These native woodland soils are so light and so low density that the earthworm cast material is much more dense," she responds. "So we actually get an increase in compaction. As the forest floor is eaten, the soil sinks anywhere from 4 to 6 inches and you get exposure of those root crowns. We see a big increase in sapling mortality because of it as earthworms invade."

Sure enough, as I turn around I see a large yellow birch, its roots snaking atop the soil surface like the roots of tropical forest trees. At Fre-lich's Wood-Rill site, which lost its protective forest floor decades ago, the bare worm-worked soil is plagued by erosion as well as compaction.

The effect is not confined to temperate forests. In central Amazonia, where tropical rain forests have been cleared to create cattle pastures, the soils quickly lose two-thirds of their original "macro-fauna" species—including ants, termites, millipedes, spiders, mites, beetles, and native earthworms—and are overrun by dense populations of an aggressive nonnative earthworm, Pontoscolex corethru-rus. The pasture soil, already compacted by the heavy machinery used in clearing the forest and by the trampling of cattle, gets dramatically denser as it is passed through the guts of worms at the rate of about 40 tons per acre each year. Patrick Lavelle and his colleagues found that without the "decompacting" activities of ants, beetles, and other soil animals to break up the cast material into smaller granules and restore porosity, the soil becomes impervious to infiltration by air and water and discourages plant growth.14

Hale picks a spot and sits down, brushing aside leaves again to reveal bare soil. She pushes the metal frame she carries into the soil an inch or so and slowly pours in about a half gallon of the milky-yellow mustard water she's carried with her. Within seconds, the ground is squirming with small, irritated worms. Most of them are juveniles and hatchlings only one-quarter- to one-half-inch long. They hardly seem the sort to drive large ecological transformations. She begins picking them up with tweezers and dropping them into a shallow plastic dish of alcohol.

Earthworms are difficult to identify to species until they're sexually mature, so Hale usually samples in fall when a larger proportion of these worms will have reached adulthood. After picking out two dozen from the first flush of worms, she pours on a second dose of mustard water. The rain has brought a fresh hatch of mosquitoes that dart at our necks and faces as we sit staring at the new crop of worms surfacing in the extraction frame.

Hale and her colleagues have found seven species of earthworms invading here, all members of the European Lumbricid family. Together they cover the three basic ecological groups of earthworms. First are the litter-dwelling or epigeic species, worms you'll often find in your compost heap but seldom in your garden soil. They're small-bodied red-brown worms that live in and feed upon the litter layer or near the surface of the mineral soil. At this site, the epigeics are Dendrobaena octaedra, Dendrodrilus rubidus, and L. rubellus, the aptly named leaf worm.

Second is a single species of anecic or deep-burrowing worm, the night crawler L. terrestris, now found throughout most of the world. (The traditional term for widely introduced worms such as L. terrestris and the tropical P. corethrurus is "peregrine" species—essentially, wanderers.) Anecic species are usually very big, pigmented worms that live in permanent burrows as much as 6 feet deep and feed on fresh surface litter that they pull into the burrow opening and mix deep into the soil profile.

Third are the endogeics, meaning "in soil," which form lateral-branching tunnels 15-18 inches below the surface as they feed. The endogeics here are larger bodied but nonpigmented species in the genera Aporrectodea and Octolasion. (Tropical P. corethrurus is also en-dogeic.) Endogeics consume soil and feed directly on the organic matter it contains, as opposed to fresh litter, so you seldom spot them on the surface. Yet gardeners who pull a plant up by the roots will often see Aporrectodea caliginosa, the common grayish pink field worm, coiled in the roots.

Hale fishes with the tweezers in the plastic tray, trying to show us how to tell the worms apart. I find it difficult to distinguish even the colorless endogeics, however, because the dark soil in their innards shows right through their transparent "skin" or cuticle. These beasts possess no eyes or ears, yet their segmented bodies are studded with light receptors and they flinch at touch or vibration.

"This is a sexually mature adult worm. It's got the clitellum, that smooth little band or necklace that you think of when you think of earthworms." She holds up a 2-inch worm and points out the smooth saddlelike patch near the head end. For those who know what to look for, the clitellum can be used to tell worm species apart. It's also important in worm sex.

All Lumbricids are hermaphrodites, meaning they have both male and female equipment. Some can self-fertilize but many mate sexually, lining up head to toe and encasing themselves in a slime tube secreted by the clitellum to help maintain what can be an hour-long embrace. With each worm playing both male and female roles, each later produces a cocoon using a layer of skin sloughed from the clitellum.

Hale gathers up her equipment and we move on toward the less invaded end of her tract. She once brought a group of resource professionals out here and showed them what we've just been seeing: the absence of a forest floor, the scarcity of maple seedlings, and the abundant sedges. "A couple of them said, 'but this is what most of the forests look like,'" she recounts. "Many of these were people from southern Minnesota, which is much more heavily impacted by human activity and has very few worm-free sites remaining. And when we finally got up ahead to the worm-free site with the thick forest floor, they just shook their heads and said, 'this makes me realize, I may never have seen a worm-free site.' It was an incredibly powerful revelation to realize that all of their impressions of what a natural forest looks like may be based on something that is heavily impacted by an exotic species."

As we follow the worms forward, we begin to spot a scattering of trillium, blue cohosh, spikenard, and yellow violets, flowers that have virtually disappeared behind us. Here, Hale points out, "there are lots of little two-leaf maple seedlings. In many of the worm-free areas we can get sugar maple seedling densities of 100-200 per square meter [slightly larger than a square yard], as opposed to one or two in the worm-impacted areas."

Hale takes another soil core from this recently invaded spot. It shows a thin remnant of forest floor, little more than an inch of A horizon, then a long plug of fine silty beige soil. The thinning of the forest floor doesn't bode well for the future of the wildflowers around us. Meticulously, she pokes the divot back in its hole and moves ahead.

The ground becomes spongier as we near the end of her transect, and Hale looks for a clearing amid the plants and seedlings to set up her frame and extract more worms. Here the duff layer, the organic horizon, remains several inches thick. She pushes it aside, clearing a spot for the metal frame, and pours on a whole gallon of mustard water. Within seconds, tiny white Dendrobaena are thrashing on the surface. Even the adults among them are less than an inch long.

"Well, even though I euphemistically refer to this as the worm-free end, it's really not worm free," Hale sighs. "But there's a smaller suite of species, biomass is lower, and it's been invaded for a much shorter period of time."

It's also not surprising to Hale that the worms we're seeing here are litter-loving Dendrobaena. It turns out that worm species invade in predictable succession in this forest, and tiny Dendrobaena takes the lead. Hale has also learned, both from this field study and from greenhouse experiments, that different worm species create dramatically different ecological impacts. In these sugar maple forests, the arrival of Dendrobaena has almost no impact on forest floor thickness or on understory plants. "But when the leaf worm L. rubellus shows up, we see very rapid removal of the forest floor and also bigger declines in native plant populations. These worms literally eat the forest floor out from underneath the roots of the plants." The species declines to low levels as it destroys its own habitat, leaving the later arriving night crawlers and the endogeic species to dominate.

Despite the accelerated pace of decomposition and nutrient turnover spurred by these invaders, Hale's studies turned up another counterintuitive result: the amount of nitrogen available to fertilize plant growth actually declines in the worm-worked soil here. Her studies don't explain why, but others have found that earthworm activity can increase nitrogen losses, either in the form of nitrate leaching into groundwater or as gaseous nitrogen and nitrous oxide released to the air by microbes.15 Even in crop fields where farmers value many earthworm species for their positive effects on plant growth, there is a suspicion that deep-burrowing anecic worms such as night crawlers can increase the movement of nitrates, pesticides, and other pollutants down through the soil and into groundwater.16 Indeed, a recent study in an Ohio cornfield found that nitrogen leaching from plots with high earthworm populations was 2 1/2 times as great as in plots with low levels of worms.17 In places where invading earthworms don't cause detectable leaching or even speed up nitrogen cycling, the worms still can dramatically alter the way the system handles soil carbon, nitrogen, and phosphorus. The clear message is that ecosystems with earthworms— especially those where worms were previously absent—can work quite differently than ecosystems without worms.18 How a forest or other ecosystem responds to earthworm invasion will vary with the species of worms involved, the nature of the ecosystem itself, environmental conditions at the site, and even past land uses. Finally, the activities of worms will interact in complex ways with other human pressures— acid rain, climate change, exotic pests and diseases, timber and farming practices—that are also driving changes in our lands and waters.

Exotic worm impacts are increasingly drawing the attention of researchers and land managers, from the maple forests of upstate New York to the aspen forests of Canada, the oak savannas of California, and the boreal (subarctic) spruce-fir forests of Russia. Hale and Fre-lich have expanded their inquiries into boreal spruce and aspen as well as beech hardwood forests. Meanwhile, Paul Hendrix of the University of Georgia is leading an effort to see what happens in regions where European and Asian earthworms encounter some of the 90 or so species of native earthworms in the United States, from North Carolina to the Oregon coast. So far, the most dramatic effects of exotic worms, at least in North America, have been seen in areas long devoid of native earthworms.19 Yet newer arrivals with different traits have the potential to transform both native earthworm communities and areas long ago reshaped by European earthworms. A whole suite of Asian worms in the genus Amynthas, for instance, is now spreading into natural areas, from New York to the hills of Georgia and even the borders of Great Smoky Mountains National Park.

"This is the next problem in the northeast forests," Patrick Bohlen told me, referring to Amynthas. A researcher now at Archbold Biological Station in Lake Placid, Florida, Bohlen previously investigated the impacts of European worms on soil processes in New York maple forests.20 Now Asian worms are spreading toward these same forests from urban areas where they arrived either in the soil of potted plants or as contaminants in shipments of bait or compost worms. Unlike European worms, which usually slip into new territory without drawing the immediate attention of the general public or even scientists, Amynthas species make a dramatic entrance.21

"Their casts are very distinctive, and they really transform the forest soil surface into a pile of crumbs," Bohlen says. "Their behavior is distinctive, too. If you pick them up or disturb them, they move like wiggly snakes or flip in an S shape." Amynthas are annual species that hatch in spring and die in fall, so to perpetuate themselves they reproduce in huge numbers. The soil can literally appear to be writhing with worms. "When people encounter it, they very often react to these worms as to pests," Bohlen says. "They're aghast. It's off-putting."

What effect Amynthas will have in the long run is anyone's guess. Ecologists and foresters are still trying to follow the ripple effects of European worms through invaded communities. Some of the long-term effects of invasion are visible in places such as Wood-Rill—bare, eroding soil, sparse understory, and minimal seedling regeneration under centuries-old trees. And there are the unseen effects such as reduced nitrogen availability. No one knows yet what this means for the growth rate of trees and the future productivity of the forests themselves, data Frelich considers critical for the region's forest industry as well as for conservation.

As for other soil denizens, worm activities and the loss of the forest floor seem to be particularly hard on fungi, including mycorrhizae, as well as on litter-dwellers such as springtails, mites, and millipedes. Above the ground, species such as ovenbirds that nest in thick forest floors are expected to suffer, along with birds that require a lush un-derstory. Already, loss of the forest floor in Chippewa has reduced the numbers of small masked shrews and red-backed voles that forage for insects, seeds, and fungi in the duff; yet deer mice and wood mice appear unaffected.22 In the worm-invaded woodlands of New York, adult red-backed salamanders seem to benefit by feasting on exotic earthworms.23

Many ecologists worry that the real beneficiaries of exotic worms, however, will be other exotic creatures that further alter the soil as well as life aboveground. In Hawaii, for instance, exotic worms have spread into the native forests, providing a protein source for feral pigs that physically damage native vegetation and spread the seeds of exotic plants. It's a synergistic onslaught that leads to what one ecol-ogist has called "invasional meltdown."24 In the forests of New Jersey, researchers find higher nitrate concentrations as well as higher densities of European earthworms under invasive barberry shrubs and wiregrass than in the soil under native shrubs.25 The same holds true for invasive buckthorn shrubs in the Chicago area.26 Conservation managers who try to restore invaded areas like these by removing barberry or buckthorn and replanting native shrubs may find their efforts foiled from below by the legacy of changes in soil nutrient cycling and the worm-dominated soil community.

"The more you think about it, the cascades of potential effects are really dramatic," Hale comments. What can be done to halt the worm invasion or restore the invaded ecosystems? I ask. Earthworms cannot be eradicated once they invade, but Hale believes we can protect uninvaded sites and slow the advance of worms elsewhere.

"Expansions of established earthworm populations are really quite slow, maybe 30 feet a year," she points out. "If you do the math, it takes a couple hundred years to go a kilometer [two-thirds of a mile]. So if we can prevent new introductions in sites that are still worm free, we can buy ourselves hundreds of years to find solutions. The education component is very important here."

Another useful management strategy is to prevent new species from joining the mix of invaders. "People say, 'if there are already earthworms invading a site, why does it matter if I release earthworms?' And my answer is that we might not have the whole suite of species, and the type of impact you get depends on the species assemblage." Minnesotans should even be wary of Asian Amynthas species, which apparently don't survive the region's harsh winters, Hale says. A warming climate could remove that limit.

Finally, reducing other pressures on worm-invaded ecosystems might help native plants and animals survive.27 One key pressure in Minnesota is deer grazing, as alluded to earlier. "We're not convinced that many of these native understory plant species are incapable of coexisting with earthworms," Hale says. But the intensity of deer grazing means plants knocked back by worms get little opportunity to recover. Frelich's team fenced off two i-acre areas at Wood-Rill to exclude deer and within a few years saw blue cohosh, bloodroot, trillium, bellworts, and other plants nearly eliminated outside the fence by the worm invasion springing up from seeds long dormant in the soil. "These plants have probably been germinating for decades," Hale believes, "but as soon as one little green thing pops up from the bare ground, the deer eat it."

Inside the deer-free enclosures, Frelich's team is also testing whether electroshocking the ground to remove most of the worms from small patches will eventually allow the forest floor there to recover and nutrient cycling to return to preworm dynamics. It's an interesting experiment—one that Frelich expects to continue for 20 years or so—but an unlikely management option. I asked Frelich what would be the best he could realistically hope for at Wood-Rill.

"I hope the result of this experiment is that the plants grow quite well in the presence of earthworms but without deer," he offered. "Because if it turns out all you have to do is control the deer, that's a whole lot easier than getting rid of the worms."

I've spent much of this chapter exploring the deleterious effects of earthworms because these accounts have helped to jar my own stereo types about worms and provide vivid illustrations of the power soil animals can wield in shaping the world we experience. Yet I wouldn't want to tip the reputation of earthworms back toward 18th-century "detestation."

Over the past century, earthworms—mostly Lumbricid species in temperate regions—have gotten generally good marks from agricultural researchers and promoters of organic gardening for their ability to enhance plant growth. Two cases in particular have become textbook classics. One involves Dutch "polders," pastureland reclaimed from the sea by diking and draining in the 1950s and initially devoid of earthworms. Intensive grazing by cattle and sheep quickly compacted the young soil and damaged grass production. Night crawlers and other Lumbricids were introduced to some of the degraded pastures in the early 1970s. As the worms slowly spread, they incorporated the mats of dead grass on the surface into the soil, speeding development of an A horizon, aerating the soil, improving water infiltration, and enhancing grass production.28 In the second case, European worms introduced into New Zealand pastures also dramatically improved grass yields.29

In recent decades, several hundred studies in the tropics involving a wide assortment of earthworm species, crop plants, and soil types have demonstrated that worms usually boost plant growth. A review of these studies by George Brown of Brazil's Embrapa Soybean and a number of colleagues revealed that increases in plant growth average nearly 60 percent, and increases in grain yield for crops such as rice and maize average 36 percent when worms are added. The biggest growth enhancements show up in some tropical tree crops and tea bushes, as well as panic grass, an African grass widely planted for forage in the American tropics. Other plants such as oats gain little, however, and the yield of cowpeas, peanuts, and cassava drops in the presence of worms.30

Such findings have led to new work for earthworms. For example, Lavelle and Bikram Senapati of India's Sambalpur University have developed an earthworm treatment for degraded soils that has dramatically boosted both yields and profits on aging tea estates in southern India. Some of these plantations have been operating for a century or more, and despite increasing use of fertilizers, the soils suffer from declining organic matter levels, reduced water-holding capacity, acidification, compaction, erosion, nutrient leaching, and up to 70 percent loss of soil organisms—including most native earthworms. Senapati and Lavelle's "bio-organic fertilization" technique involves adding organic waste—various combinations of tea prunings, cow manure, and compost—in trenches dug between the tea rows, along with inoculations of exotic P. corethrurus and a mix of other earthworms. Rejuvenation of the soil by this method has increased tea yields from 80 to 276 percent on various estates, and the technique is now being applied to tree and shrub crops in other countries such as China and Australia as well as India.31

Earthworms dominate the world of soil engineers, but they are rare in arid regions. In drylands and a number of other regions, termites, ants, beetles, millipedes, and a diverse suite of other native soil animals head the ranks of soil turners and engineers, often producing a variety of complementary effects such as the compacting and de-compacting activities already mentioned. Termites and ants that excavate subterranean galleries and nest chambers and transport litter and plant material underground—and termites that feed directly on soil, like endogeic earthworms do—profoundly influence the structure and the flow of materials and energy in the soil.32 According to Bert Holldobler and Edward O. Wilson of Harvard University, "One third of the entire animal biomass of the Amazonia terra firma rain forest is composed of ants and termites, with each hectare [2.5 acres] of soil containing in excess of 8 million ants and 1 million termites."33 Unlike earthworms, other soil animals are seldom deliberately introduced to rehabilitate degraded land. Increasingly, though, scientists are experimenting with ways to take practical advantage of native soil biodiversity. In part, that means altering practices such as plowing, pesticide use, depleting organic matter, clearing forests, and heavy grazing that are generally harmful to the soil community, especially larger soil animals. Earthworms, termites, and ants, for instance, are all terribly sensitive—though in different ways—to changes in the intensity of human land use at the margins of tropical forests. A major effort is now under way in fields and pastures carved from tropical forests to improve the sustainability of subsistence agriculture as well as protect biodiversity.34 In sites where land is already degraded, other researchers are devising ways to harness the rehabilitative powers of soil animals such as termites by creating conditions that lure them back to work.

Farmers in the dry tropics often regard termites and ants that forage on grass and plant litter as pests because these animals attack crops, especially when the land has been stripped of all other vegetation. In the impoverished Sahel region of western Africa, however, termites are being encouraged to perform a service similar to that provided by earthworms on Indian tea plantations. Continuous farming along with overgrazing and trampling by cattle in this region along the southern edge of the Sahara desert has left much of the surface bare and crusted, impervious to water and unable to support plant life. Inexpensive and low-tech methods of soil rehabilitation are urgently needed, and native termites, it turns out, are up to the task. Researchers find that when crusted soil is mulched with woody material, straw, or cattle dung, termites quickly arrive to consume it. These are mostly "higher" termites in the subfamily Macrotermitinae that can carve out miles of subterranean galleries per acre, drawing organic matter into the soil, breaking up the surface crust, increasing porosity and water infiltration, and allowing plant roots to penetrate. Within only a year, native plants reestablish on the denuded land and crops such as cowpeas yield modest harvests.35

Such successes are testament to Darwin's insight that large numbers of little things have the power to alter landscapes. Certainly scientists and land managers today cannot afford to discount, as Darwin's contemporaries did, the potential of earthworms and other soil animals to reshape the world we experience, for better or worse.

Oplan Termites

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