Issue Date: October 19, 2015
Night Crawler Chemistry
This year is the International Year of Soils, so designated by the United Nations. Don’t worry if you didn’t know that. Many people don’t think about soil, or even know what it’s made up of or how its inhabitants are vital to its health—and by extension to our survival. What Leonardo da Vinci said some 500 years ago is still true today: “We know more about the movement of celestial bodies than about the soil underfoot.”
Of course, scientists have since learned something about Earth’s epidermis. They have classified thousands of soil types by their mineral compositions and now know that soils are full of bacteria, fungi, protozoans, nematodes, insects, and the random mole, gopher tortoise, or burrowing owl.
But less well understood is how soils are processed and remodeled by an often-overlooked subterranean chemical engineer: the earthworm. Researchers are still trying to fully understand the outsized role earthworms play in the global cycling of carbon, nitrogen, phosphorus, organic matter, and metals. In some cases, it’s for the better, but in others, it’s for the worse. And either way, that role is growing as earthworms slowly repopulate the northern regions of the planet from which they were long absent.
These are the concerns of soil science professor Josef H. Görres of the University of Vermont. He’s an earthwormologist. Görres and his colleagues sift through the leaf litter and dig into the ground of New England’s forests searching for different types of earthworms to study the physical, chemical, and biological effects they are having on forest ecology.
Görres isn’t the only person who will tell you how beneficial earthworms are as ecosystem managers. Farmers and home gardeners love the wriggly creatures for improving soils by decomposing wood and leaves from plants, speeding up the release of nutrients, aerating the ground, and aiding water drainage.
The cylindrical critters work their way through soil using ringlike muscular segments covered with small bristles that aid locomotion. Earthworms maintain their figures with a hydrostatic skeleton made up of a fluid circulating through their bodies. This fluid also keeps them moist, so they can breathe through their skin—earthworms lack lungs—and it helps lubricate and cement their tunnels. The animals have no eyes but instead find their way around with photosensitive cells in the skin and with chemical receptors concentrated near their mouths.
The grand feature of earthworms, though, is their digestive system. Earthworms constantly push their food along with waves of muscular contractions. They use mineral particles to help grind up organic matter they encounter and have microbial partners in their gut that produce enzymes to help do the rest.
As earthworms move through the soil, they’re digesting and glomming all the stuff together. What passes out their backsides is an organic-rich aggregate, called castings. In fact, most of the soil where earthworms live is earthworm poop. Charles Darwin, in a book he wrote about the habits of earthworms, estimated that the animals can collectively produce 10 tons of castings per acre per year, and they add 1 to 2 inches of topsoil to the ground in 10 years.
Earthworm castings “are like pixie dust,” Görres says. The material, similar to compost, helps promote plant growth, prevent disease, control insects, and more, he notes. “But we don’t know all the reasons for it or all the ways it works.”
Chock-Full Of Chemistry
Earthworms enrich soil by increasing the bioavailability of nitrogen, phosphorus, and potassium, the key components of synthetic mineral fertilizers. Fertilizer is rated on the percentage of those elements in the material—for example, a common garden fertilizer is 10-10-10. Earthworm castings would weigh in around 3-1-1, Görres says, depending on what they are munching. But earthworms enrich soil in other ways, too.
As earthworms churn through soil and break down animal and vegetable matter—they aren’t picky eaters—they are helping produce an amorphous material known as humus. Consisting of the remnants of cellulose, starch, lignin, and other diverse biomolecules, it forms the characteristic dark brown top layer of the soil. Humus harbors nutrients, retains water, and promotes good soil structure.
For example, humic acids in this material are a set of oligomeric molecules derived from lignins and tannins that play a role in shepherding trace metals and other micronutrients into plants, serve to buffer soil pH, and function as plant growth promoters.
One problem earthworms have to contend with as they dine is that leaf litter is high in polyphenols. Plants produce these compounds in part to defend against insect pests. But the polyphenols can trigger earthworm enzymes to clump up and stop working, leading to indigestion.
To compensate, earthworms perform a unique feat of chemistry. Jacob G. Bundy of Imperial College London and coworkers recently reported that the animals produce surfactant molecules—dialkylfuransulfonates called drilodefensins—that prevent enzyme malfunction (C&EN, Aug. 10/17, page 9).
Like us, earthworms also rely on bacteria in their gut to oxidize and refashion plant and mineral matter into a more nutritious form. The key is a good collection of enzymes: pepsin to deconstruct proteins, amylase for polysaccharides, cellulase for cellulose, and lipase for fats.
But for all the good that comes from earthworms’ digging ways, Görres says, they have a dark side. With their chemical processing and their network of tunnels, they can speed up leaching of fertilizer and pesticides from fields and orchards into streams.
Earthworms have also invaded new territory, such as New England’s forests, where they hadn’t lived for more than 10,000 years. In the forests, they are eating away the valuable organic layers that have built up and altering the trafficking of carbon, nitrogen, and trace metals through the ecosystem. Scientists suspect earthworms may have a larger role to play in global climate change than previously realized.
There’s so much chemistry going on that it’s opening a can of worms to keep track of it, Görres says. “We could use the help of chemists who want to satisfy their ecologist leanings to better understand the specific chemical pathways by which these creatures act.”
The story of how earthworms became invasive species started some 11,000 years ago, Görres explains. During the last glacial period, earthworms migrated south or were wiped out in Vermont, where he works, and across much of the northern latitudes of the planet. When Europeans began settling in North America by the 1600s, they reintroduced earthworms, perhaps on purpose in some cases, but typically by accident.
A primary source would have been ship ballast, a mixture of soil and gravel that the settlers dumped on the land, Görres says. Other sources might have included potted plants. Today, the main culprits for inadvertently spreading earthworms are bait from recreational fishing, logging activity in forests, and spreading mulch or compost from garden centers and municipal recycling programs.
Görres and his colleagues have identified 18 earthworm species now living in Vermont. Fourteen of them hail from Europe, and four are Asian. They go by exotic names such as night crawlers, red wigglers, crazy snake worms, and Alabama jumpers.
The Asian species actually represent a “second wave of invasion,” Görres says, which parallels the increase in global trade in recent decades. Görres and his colleagues want to understand the role the earthworm immigrants have played in soil carbon and nitrogen cycling as onetime forests were converted to tilled farmland and as some of that farmland has been abandoned and is reverting to forest.
Worm-free forest floors in Vermont are covered with a so-called duff layer, a spongy mat of decomposing organic matter that has built up over centuries, Görres says. But in parts of Vermont and in much of the U.S., the duff doesn’t exist anymore. The worms have eaten it all. In areas with the duff layer, ferns, shrubs, and annual plants thrive in the understory below the tree canopy. Without the layer, Görres sees forests with bare ground.
“Earthworms are changing the basic layering of forest floors and disrupting the lives of trees and understory plants that depend on this system,” Görres points out. “Plants that count on the duff layer as a germination medium or a seed bank will no longer be around.” In addition, without understory plants, he says, deer browse more on sugar maple and paper birch saplings. These changes could one day make maple syrup hard to come by.
Besides earthworms’ effects on forest vegetation, scientists are keen to learn more about how the organisms alter the nitrogen and carbon cycles in forest soils.
For example, Görres and his colleagues are finding that forest soils where earthworms prowl are accumulating nitrate. In the nitrogen cycle some microorganisms break down urea from plants and animals to make ammonia. Nitrogen-fixing microbes separately pull N2 from the air to make ammonia. Other microbes convert the ammonia to ammonium and then to nitrate, a process called nitrification.
Different plants have different preferences for the nitrogen species—some like ammonium, others nitrate, Görres explains. Earthworms speed up nitrification, however, and because ammonium is a relatively short-lived nitrogen species, nitrate accumulates. In addition, nitrate is negatively charged, making it relatively mobile in soils, he says. Positively charged species tend to get trapped by the soil’s humic acids. That means nitrate can readily leach away and contaminate groundwater and streams.
Once this nitrate reaches waterways, Görres adds, it can cause unwanted explosions of algae growth that suck up oxygen in the water and choke out other plant and animal life. The nitrification process also releases nitrous oxide, N2O, a compound that contributes to smog and is one of the top three greenhouse gases of concern along with carbon dioxide and methane.
Any discussion of greenhouse gases also involves the carbon cycle. Many research groups are trying to determine whether earthworms are adding to or reducing the amount of organic carbon in soil, and, as the next step, reducing or adding to global CO2 emissions.
Some carbon gets trapped in earthworm castings as the animals digest organic matter. In that case, it’s not immediately available to soil microorganisms that could break it all the way down to CO2. But earthworms do pick out carbonate from leaves and completely metabolize some compounds to CO2. Plus they generate some CO2 as they breathe, though they don’t exhale CO2 like humans do. Where all the CO2 goes is interesting, Görres says.
The primary way the creatures process CO2 is through calciferous glands attached to the esophagus, which are unlike anything that is known in any other animal, Görres says. With the aid of the enzyme carbonic anhydrase, the glands produce a milky suspension of calcium carbonate. The suspension, which amounts to a few milligrams of CaCO3 per day, precipitates to form granules, which the earthworms expel in their castings. “It’s a remarkable case of biomineralization,” Görres says.
Scientists aren’t sure about the purpose of this CO2-fixing scheme, he points out. It could be to neutralize humic acids in the leaf litter to make them more nutritious for the worms or to control pH for reproduction. Studies show that the granules can last for several years before dissolving. That means they could be playing a role in sequestering CO2.
Another possible reason for the CO2 processing, or maybe a consequence of it, is to govern calcium levels. “When you go to a place like in Vermont where the earthworms are invasive, you find more available calcium in the soil,” Görres notes. “It could be there naturally, or maybe the earthworms are making it more available on purpose.”
Certain plants, such as the jack-in-the-pulpit, a wildflower, thrive when earthworms are present, Görres says. “We see a lot of them, and some really big ones.” The growth might be related to the extra nitrate, but Görres thinks it has more to do with calcium oxalate the plants produce.
Deer tend not to munch on plants that are high in oxalic acid, Görres explains. “It tastes sour to them or gives them the sensation of stinging needles on their tongue. One theory is that plants survive by utilizing the extra calcium in earthworm soils to produce extra calcium oxalate.” When these plants thrive, they yield more organic matter for earthworms to munch on. Görres and his group carried out experiments with jack-in-the-pulpit and found more oxalate in the plants when earthworms are in the soil.
Earthworm Heavy Metal
Besides processing carbon and nitrogen, earthworms also serve as little miners prospecting for metals as they bore through leaf litter and soil. On the one hand, earthworms break up soil particles, releasing essential metals for plants. On the other hand, the worms absorb toxic metals and tend to accumulate them.
Scientists aren’t sure how problematic earthworm redistribution of toxic metals in the environment might be. But one concern is that night crawlers loaded up with such metals could be detrimental to the birds, frogs, salamanders, and small mammals that feed on them.
Justin B. Richardson of Dartmouth College’s department of earth sciences investigates trace metals in the environment and often finds himself digging into the forest floor of New Hampshire and Vermont collecting soil samples. Richardson started out tracking metals as a graduate student in Andrew J. Friedland’s lab at Dartmouth. The forest soils they study contain a lot of legacy pollutants that drifted into the region from points south and west, including lead from the use of tetraethyl lead as an antiknock agent in gasoline and mercury from coal-fired power plant emissions.
Richardson kept finding earthworms everywhere he was digging. And he started noticing that the soil’s top organic layers, which typically accumulate the toxic metals, were not as they should be. “Those layers are no longer there; they are gone,” he says. Earthworms had consumed them and taken their legacy pollutants as well.
Richardson and Friedland connected with Görres and his colleagues to investigate the earthworm-metal conundrum. They collected more organic layers, mineral soil, and earthworms. The researchers measured concentrations of essential metals (Cu, Mo, Ni, Zn, Se) that plants and animals need as enzyme cofactors and micronutrients, as well as toxic metals (As, Cd, Pb, Hg, U) that aren’t used by most organisms.
Metal uptake depends on the earthworm species and the location, the Dartmouth-Vermont team found, but generally the worms are redistributing metals. The fact that earthworms accumulate metals is no surprise, Richardson explains. But the kicker is that the worms had attained concentrations of lead, mercury, and selenium that could present a toxic dose to other animals.
“You wouldn’t want your chickens eating these worms,” Richardson says. And as earthworms become more prevalent, they may become a more integral part of the diets of birds and other animals, he notes. In addition, when earthworms die they quickly decompose in the soil, so metals in the worms remain in concentrated form.
“Earthworms disrupt what forest soils do well: serving as a natural filter for pollutant metals to prevent them from entering food webs,” Richardson says.
Some people worry about cows contributing to global warming through the methane they release, but earthworms may have an even larger effect on greenhouse gas emissions, and one that is growing. Environmental scientist Ingrid M. Lubbers of Wageningen University, in the Netherlands, is trying to determine its scale.
Lubbers notes that about 20% of global CO2 emissions as well as about 33% of CH4 and 66% of N2O emissions come from soil. Lubbers and her colleagues study how earthworm activity influences greenhouse gas emissions in agriculture. They recently conducted comprehensive reviews of research papers on the effect earthworms have on carbon and nitrogen cycling and plant growth, as well as the amount of CO2 and N2O earthworms produce.
In one meta-analysis of reported experimental studies, the group found that earthworms on average provide a 25% increase in crop yield compared with test plots without earthworms, Lubbers says. The magnitude of this effect depends on the presence of crop residue above the ground without tilling or belowground with tilling. Other factors include earthworm density and the type and rate of fertilizer used.
Despite promoting plant growth, which pulls more CO2 out of the air, earthworms neither increase nor decrease the net amount of organic carbon stored in soils, Lubbers and her colleagues found in another meta-analysis. But earthworms do increase N2O emissions by 42% and CO2 emissions by 33% compared with tests without earthworms.
Lubbers thinks the analyses have implications for farming practices. Farmers have been turning to no-till agriculture because it reduces erosion, requires less fuel, and provides an upscale home for earthworms to increase harvests. “But earthworms appear to strongly reduce any benefit for mitigating greenhouse gas emissions over the classic but less sustainable approach of plowing and applying a higher rate of fertilizer.”
Lubbers and her colleagues are also in the process of conducting their own experiments on earthworm greenhouse gas balances, comparing no-till approaches to conventional tilling. So far, they have confirmed the meta-analysis findings—that earthworms don’t increase organic carbon storage in farming but do increase CO2 and N2O emissions (Sci. Rep. 2015, DOI: 10.1038/srep13787).
“We speculate that if the global distribution of earthworms increases, as it is in North America, for example, that the impact of earthworms on greenhouse gas emissions is going to increase globally,” Lubbers says.
The interests of researchers such as Görres and Lubbers are scientific. But they know policy implications loom: The better society understands the roles that oceans, plant life, microorganisms, and creatures such as earthworms play in cycling of carbon, nitrogen, and other elements, the better leaders can decide what to do, if anything, about corralling industrial emissions.
The chemical engineering that earthworms take part in is just one story unfolding in soils. Indeed, soil awareness is the purpose of the UN’s International Year of Soils. “The multiple roles of soils often go unnoticed,” commented José Graziano da Silva, director-general of the UN’s Food & Agriculture Organization, when he announced the International Year of Soils last December.
“Soils constitute the foundation of vegetation and agriculture. Forests need it to grow. We need it for food, feed, fiber, fuel, and medicines,” Graziano da Silva said. “Yet soils don’t have a voice, and few people speak out for them.”
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