Abstract

Up and down. Up and down. Earthworms slowly wriggle their way through the soil, eating leaves, burrowing holes, leaving behind nutrients … and completely altering the forest floor. While people usually perceive earthworms as good for the soil, forest soils invaded by earthworms are a different story. “The forest floor is an organic-rich soil layer, and it's just candy for the exotic earthworms that are invading forests in the non-glaciated regions of North America,” says Peter Groffman of the Cary Institute of Ecosystem Studies who has been researching these invasions with funding from the National Science Foundation. “They burrow through [that layer], mix it with the [underlying] soil, and stimulate microbial growth. It's a physical, chemical, and biological transformation of that forest floor into something else, and it has huge implications for the health of the forest.” The forest floor is the top layer of forest soil, and it is made up of fallen leaves, roots, stems, branches, and bark, all at varying stages of decomposition. Groffman is working to learn how exotic earthworms invade and affect northern temperate forests and their soils in North America. Natural history tells us that glaciers eliminated native earthworms from these forests 15,000 years ago, and they have been without them ever since. But Groffman says that about 30 years ago, people began to notice that earthworms from Europe and Asia were colonizing some forests in northeastern North America. Now, up to 16 different species of earthworms can be found in these soils. The European worms in question are mainly from the Lumbricidae family and include the surface dweller Lumbricus rubellus and the deep-burrowing common night crawler Lumbricus terrestris. Groffman says these were introduced to the United States during colonial times. The more recent Asian species are from the genus Amynthas. Invasive species are a problem in many areas of the United States. They are insects, animals, or plants—both terrestrial and aquatic—that become established in ecosystems where they traditionally weren't present. In many of these ecosystems, native organisms and environments have evolved in tandem for millennia. Throwing off this balance and forcing an ecosystem to take on a new species can cause a lot of strain. Establishment of invasive species is aided when they don't have any natural predators in the area. This allows their population numbers to rise unchecked and overwhelm native species, which have no natural defenses against the invasion. The most obvious effect of an exotic earthworm invasion in northern forests is that the forest floor would disappear within just two to five years. This drew the attention of researchers because that layer is considered very important. The top layer of forest soils in North American forests, the forest floor, is being transformed by exotic earthworms. Photo by Samantha Cillo. When the forest floor disappears, so do the organisms that live there. These invasions harm the biodiversity of the soil, which serves as habitat for a large number of organisms—from salamanders, small mammals, and ground-nesting birds to beetles and plants. “Many of the organisms that used to live in the forest floor can't live there anymore because it's gone,” Groffman says. “It's a classic case of habitat loss reducing biodiversity.” Along with decreasing biodiversity, the disappearance of the forest floor can increase the susceptibility of the soil to erosion and drought, alter its ability to store, or “sequester,” carbon long term, and modify the cycling of carbon, nitrogen, and phosphorus. “We would like to think that our forests are sequestering carbon from the atmosphere,” Groffman says. “These ecosystems are large natural reservoirs of carbon and play a role in curbing climate change. However, when earthworms invade, they transfer much of the carbon from the forest floor back into the atmosphere. In addition to directly eating and respiring some of the forest floor organic matter, they also mix organic matter into the soil, stimulating microorganisms that also eat carbon and send it back into the atmosphere.” Surprisingly, the nitrogen content of some of the soils Groffman studied did not decline along with carbon. This caused the carbon-to-nitrogen ratio to decrease, which can reduce the forest soils’ ability to hold on to the nitrogen from the atmosphere or from runoff from adjacent agricultural lands or urban areas. When it comes to phosphorus, earthworms may be causing two effects. At the surface, earthworms appear to cause losses of the phosphorus that plants need, but at the same time, some earthworms seem to be bringing up phosphorus from deep down in the soil, which is not in a form that plants can use. It really depends on the species of earthworm in a particular soil because some burrow deep, and others stay closer to the surface. The loss of phosphorus from the surface soil is a concern because this nutrient can pollute downstream lakes and rivers. The loss of the forest floor can also make a forest more susceptible to drought. The forest floor can act like mulch to keep the soil moist. Moreover, earthworms disrupt the interactions that trees have with mycorrhizal fungi, which help roots to take up nutrients. Together, these effects could reduce tree health. The reasons for the invasion are complex and likely due to multiple factors. Groffman says that there is a strong possibility the invasion is human-driven and that habitat fragmentation is to blame. “If you have long tracks of forest where there's very little human activity, you're much less likely to have invasive species introduced there,” he explains. “But as we cut the forest into smaller and smaller pieces and have more human interaction with the forest, you're much more likely to get invasions.” Additionally, there's a hypothesis about people's fishing habits causing invasions. Exotic earthworms may be found around lakes simply because it's good habitat for them. But Groffman says that anglers may also be inadvertently introducing them by discarding earthworms they use as bait at their fishing site instead of taking the leftover worms with them. Climate change may also be facilitating earthworm invasions. As certain areas experience warmer temperatures, earthworms that usually wouldn't be able to persist over winter are able to move in and establish themselves. Forest fragmentation (top) and people's fishing habits (bottom) could be two reasons for the earthworm invasion. Top photo courtesy of Wikimedia Commons/ Larrousiney. Bottom image courtesy of Flickr/Sarah and Jason. “For a lot of species, there are reported temperature tolerances, so, for instance, we weren't supposed to see some of these species in areas of New York where we have been working,” Groffman says. “Now, it's possible we had incomplete data on their tolerance, but it's also possible that the earthworms are now able to persist in these areas because the climate is warming.” While the invasion may be human-driven, the solutions can be as well. The problem is multifaceted. Scientists must first work to change the perceptions of these earthworms so people become aware that they aren't good for some soils. Then researchers need to attempt to change people's behavior so that they stop accidentally introducing them into forest soils. One of the few solutions to eradicate a current invasion is to use pesticides, but “we don't necessarily want to be spraying pesticides all over our forests,” Groffman notes. Another idea is to use chemicals to make the soil more acidic so that earthworms can't live there. But, this practice can cause harmful side effects, similar to when a forest falls victim to acid rain. Instead, scientists use their resources to prevent the spread of invasive species because they are so hard to get rid of once established. “Some researchers, such as those at the Great Lakes Worm Watch have done really great work with education and outreach programs to teach people to be more careful with worms when they fish or use worms for composting,” Groffman says. “It's hard to convince people that something they've known to be beneficial all their lives is actually harmful and a problem.” He adds that researchers have had luck explaining that earthworms are harmful by using examples of some of the more recent invasive species in their outreach and citizen-science education programs. The demonstrations help change public perceptions because some invasive species look and behave differently than the earthworms people have experienced for decades in their gardens. This helps people realize they are dealing with an invader and are more likely to work to prevent their spread. That said, earthworms are not all bad. They are useful for loosening up compacted soils, and they are fantastic in compost piles, greatly speeding up the conversion of organic materials into compost. But these are not desirable functions in forest soils, Groffman explains. Most forest soils are not compacted, and speeding up decomposition and nutrient cycling can increase nutrient losses to surrounding environments. Some researchers have had luck explaining that earthworms are harmful by using examples of some of the more recent invasive species in their outreach and citizen-science education programs. Photo courtesy of Great Lakes Worm Watch. Of course, forests in other parts of the world do naturally have earthworms, he adds. But those forests function differently than forests in northern North America. “The forests we are studying are changing from a state where they didn't have earthworms to a condition where they do,” he says. “So there is going to be a transition phase, with rapid loss of the forest floor and then a more stable phase once the earthworms become established. These new forests have thinner forest floors, less carbon storage, and less biodiversity.” Groffman admits it can be an uphill battle to draw attention to these invasions because they occur under everyone's feet, but he hopes research can help make scientists and citizens both more aware of the issue. While there is a lot of interest in invasive species such feral pigs and zebra mussels in the Great Lakes, soils receive little attention. “Often times, soils are overlooked in general, and then when it comes to invasive species in the soil, they are further ignored,” he says. “People overlook invasive species in the soil just because they're not that obvious. But their detrimental effects in the future will likely be very obvious.”

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