As the worms churn

To celebrate the 200th anniversary of Charles Darwin’s birth, hordes of readers are reveling in On the Origin of Species, which sets forth the case for evolution via natural selection. Others are poring over The Voyage of the Beagle, the chronicle of Darwin’s five-year, round-the-world expedition.

It’s probably safe to say, however, that only die-hard Darwinistas are cracking the spine on his last book, The Formation of Vegetable Mould, Through the Action of Worms, with Observations on Their Habits. In this work, which Darwin himself described as “a curious little book,” he discusses the role that earthworms play in the formation and erosion of soil. “The subject may appear an insignificant one,” he modestly noted, “but we shall see that it possesses some interest.” Indeed, for a short while after this book was first published in 1881, it sold more quickly than On the Origin of Species had.

But only much later did scientists begin to appreciate the widespread effects of bioturbation, the displacement and mixing of sediments by animal and plant life. Today, scientists recognize that the process has implications not just for geology, but also for archaeology, ocean chemistry, evolutionary biology and resource management. And, basically, for anyone who works in or on the ground.

For researchers who study subtle layering of sediments to understand a site’s history, bioturbation makes work complicated and renders results uncertain. Fossilized remnants of burrows can also make rock much more porous than expected, affecting fluid flow through aquifers and oil fields, for example. And new studies suggest that when it first came on the scene, bioturbation may have accelerated an evolutionary arms race among creatures. Some researchers make an even stronger claim based on other new work: Bioturbation, they argue, substantially changed ocean chemistry, rendering the seas more hospitable to life at the base of the food chain and therefore more biologically productive.

Slowly stirred

Like Darwin’s other studies of natural history, his observations of worms and the results of their burrowing were numerous, varied and took place over a considerable period of time.

In 1837, Darwin dug a hole in a pasture in Staffordshire where lime had been spread in 1827 and cinders had been dumped several years after that. Well beneath the thickly matted roots of the overlying grass, Darwin noted the layers that formed as a result of the dumping — one of black cinders and, two inches below, one of lime. In holes dug in the same pasture nearly five years after the original hole, each layer sat about an inch deeper than it had before — a result of worms’ nocturnal aboveground excursions, Darwin concluded. The worms eat soil, carry it to the surface and excrete the material in their fecal matter.

Some scientists scoffed at Darwin’s notion that something as small and insignificant as a worm could substantially impact the terrain, but Darwin countered that large numbers of worms could indeed roil the soil: In the course of a year, he estimated, the 25,000 or more worms living beneath each acre of land in his area would bring between 14 and 18 tons of material to the surface.

Most of Earth’s surface is home to burrowing animals of all sorts and sizes, from ants to aardvarks. In parts of some streams, spawning fish stir up more sediment than spring floods do. Even the floor of the deep sea, a milieu once thought lifeless, is substantially altered by burrowing creatures. They tunnel along, breaking up and exposing sediments. Previously buried material comes to the surface, and the fresh, nutrient-rich stuff gets sent downward.

“It’s like turning over a compost pile,” says Robert C. Aller, a marine biogeochemist at Stony Brook University in New York. The boost in microbial action triggered by bioturbation speeds nutrient cycling, he notes. Plants also get involved in the cycle, pulling food and water from soil.

Burrows (and the passageways created by plants’ root systems) provide pathways for rainwater, seawater and other fluids and gases to infiltrate soil and ocean sediments more readily, Aller says. Tunnels and surrounding porous sediments offer haven for a variety of microbes, some of which feed off the burrowers’ waste products.

But bioturbation can be a bane for scientists. Researchers who attempt to read the history of environmental conditions by analyzing the layering of sediments need to recognize how burrowing critters mix things up. In one of the latest examples, bioturbation in British Columbia’s Howe Sound, just northwest of Vancouver, is complicating efforts to determine the rate at which sediment has accumulated there since the last ice age. That measurement can tell scientists about rates of erosion in the mountainous area, among other things.

Lionel Jackson Jr. of the Geological Survey of Canada’s office in Vancouver and his colleagues recently attempted to assess the sedimentation rate in the sound by carbon-dating organic materials in core samples drilled from the seafloor.

In theory, the oldest materials are the deepest in the sediment column, and successively higher strata are younger. Material at the surface should be the youngest of all. In most of the team’s cores, shell ages increase steadily from shallow to deep, and the findings suggest that only a fraction of a millimeter of sediment accumulates in the sound each year. But in some of the Howe Sound cores, the radiocarbon dates don’t make sense,

Jackson reported in October in Portland, Ore., at the annual meeting of the Geological Society of America. In several instances, the shells in layers of sediment separated by a considerable distance seem to have the same age.

Evidence shows that some of those dating discrepancies result from underwater landslides that jumbled the sediments, Jackson says. But other discrepancies seem to have been caused by bioturbation that disturbed the sediments, gradually transporting shells and shell fragments either up or down from the layer in which they were originally deposited.

Similarly, archaeologists can also be vexed by bioturbation. Over time, the burrowing of small mammals, worms and beetles can disrupt a site’s sediments to the point that artifacts manufactured during a certain era can no longer help researchers estimate the date of nearby artifacts found at the same depth.

Rock-hard evidence

When loose sediments harden into rock, signs of bioturbation can be preserved. Sometimes those traces are modest, such as the now-filled burrows left by small dinosaurs (SN: 10/27/07, p. 259) or groups of fossilized termite mounds (SN: 2/28/04, p. 133). In other cases, remnants can leave a widespread mark.

Consider the Biscayne aquifer, which lies just beneath much of southeastern Florida. Field tests suggest that this limestone formation is one of the most permeable aquifers in the world, says Kevin J. Cunningham of the U.S. Geological Survey in Fort Lauderdale, Fla.

By measuring the spread of dyes and other tracers, hydrologists clocked water flow through some parts of the Biscayne aquifer at speeds of more than 350 meters per day. Yet some previous lab tests of limestone samples suggest that water should flow through the rock at around 10 meters per day, says

Cunningham. Blame for that disparity, he and his colleagues note in the January Geological Society of America Bulletin, can be pinned on the burrowing habits of ancient shrimp.

The aquifer’s limestone was laid down as shallow marine sediments during periods of high sea level in the past 500,000 years or so. During those high stands, a species of callianassid shrimp — commonly known as ghost shrimp — burrowed extensively in the shallow-water sediments. Adult shrimp of this species, which typically measure 12 to 15 centimeters long, dig 4-centimeter–diameter burrows that extend as much as two meters into the sediment, says Al Curran, coauthor of the study and a paleontologist at Smith College in Northampton, Mass.

Because these shrimp cemented their burrows’ walls with limestone mud to prevent collapse and because the aquifer’s sediments have never been deeply buried, the burrows remain intact in most layers. In fact, the flow of subterranean water through and around the burrows in recent millennia has dissolved some of the aquifer’s limestone, rendering the material even more porous. The team’s new analyses of core samples reveal that about three-fourths of the limestone in the aquifer may resemble a petrified kitchen sponge, not solid rock. High-resolution CT scans of samples indicate that between 60 percent and 70 percent of that burrow-riddled material is open space, Cunningham says.

Current computer simulations of water flow in the Biscayne aquifer, which provides drinking water for Miami and much of southeastern Florida, don’t account for the presence of such highly porous layers. Those permeable strata, though, could have profound consequences because open spaces act as a path of least resistance for flowing water, Cunningham says. So, he notes, water in the aquifer moves much more quickly than previously presumed, a concern if the water becomes tainted by pollution or pathogens.

Evidence suggests that bioturbation may be responsible for unusually porous aquifers in the Bahamas and Texas, the researchers add. It’s also possible, they say, that the porosity of some strata in Saudi Arabian oil fields — layers of rock that yield a lot of easily extracted oil — could result from bioturbation.

Digging the scene

Bioturbation plays an integral role in today’s ecosystems, but at one time it was a true innovation. Several recent studies show how a dramatic rise in bioturbation during the Cambrian led to extinctions, stimulated evolution and substantially changed ocean chemistry.

Early in the Cambrian period, which began about 542 million years ago, most multicellular animals had soft bodies that didn’t fossilize well. Also, tough microbial mats that bound the sediments together were the foundation of many seafloor ecosystems, says Katherine N. Marenco, a paleoecologist at Bryn Mawr College in Pennsylvania. “In essence, the surface was armored,” she notes. The few creatures that lived within the seafloor burrowed along horizontally just under the mats, not downward into the sediments.

But recent analyses of rocks near the California-Nevada border confirm that as the Cambrian unfolded, seafloor ecosystems changed. By about 500 million years ago, invertebrates had evolved the ability to dig deep, either to forage or to reside there. “The fossil record shows that burrows had become deeper, more complex and more common,” Marenco says. Bioturbation began to churn sediments more effectively, she and colleague David Bottjer of the University of Southern California in Los Angeles reported in 2008 in Palaeogeography, Palaeoclimatology, Palaeoecology.

By the end of the Cambrian, about 489 million years ago, subsurface organisms were so common that burrowing often erased the traces of preexisting tunnels. Gone too were the tough microbial mats, which evidently couldn’t withstand the constant disruption of sediments by newfangled burrowers.

Species that made their living on, in or just under the mats died out by the end of the Cambrian, Marenco says, but bioturbation allowed oxygenated waters to reach deeper layers of sediment and created new ecological niches.

Bioturbation also brought big changes in sea chemistry, new research suggests. Before the Cambrian, sulfate concentrations in seawater were much lower than they are today, says James Farquhar, a geologist at the University of Maryland in College Park.

Deposits of gypsum, a sulfate mineral that forms when seawater evaporates, provide evidence of this difference. The deposits are more common in rocks laid down in the Cambrian and thereafter than in Precambrian rocks. The lower the concentration of sulfate, the harder it is for evaporation to generate gypsum, Farquhar explains. Also, the ratios of sulfur isotopes in Precambrian rocks deposited as marine sediments indicate that seawater held no more than 1 percent of the amount of sulfate found in today’s oceans.

Then, during the Cambrian, sulfate concentrations began to rise, Farquhar and Don Canfield from the University of Southern Denmark in Odense report in the May 19 Proceedings of the National Academy of Sciences. Much of this shift, the researchers propose, resulted from an increase in seafloor bioturbation.

Sulfate making its way into the sea via rivers and fallout from volcanic eruptions during the Precambrian was quickly converted to sulfide minerals by microbes living in the sediments, says Farquhar. Very little sulfate remained in the water. But once creatures began churning up the seafloor, they reexposed sulfides to oxygenated waters, converting the sulfides back into sulfate. This increased the sulfate concentration in seawater.

The team’s computer models suggest that bioturbation plays a big role in boosting and maintaining today’s sulfate concentrations. If bioturbation suddenly ceased — as it might during a mass extinction — sulfate concentration would drop more than 90 percent over 10 million to 20 million years, simulations suggest. After ecosystems recover and bioturbation returns, “sulfate concentrations rocket back to normal,” Farquhar notes.

Increases in the concentrations of sulfate during the Cambrian, along with already rising oxygen levels, had wide-ranging impacts, says Timothy Lyons, a biogeochemist at the University of California, Riverside. These chemical changes boosted the solubility of trace metals such as copper, molybdenum and iron, which microbes at the base of the ocean’s food chain use in a variety of metabolic pathways. In essence, says Lyons, bioturbation made the ocean a better, more biologically productive place to live and may have opened the door to a broader diversity of creatures.

Although bioturbation undoubtedly accelerated the ancient increase in sulfate concentrations, it probably didn’t trigger that shift, Lyons cautions. He argues that the first animals to dig deep during the Cambrian probably couldn’t have done so until oxygen levels in the sediments were already suitably high — a trend that would have, on its own, boosted sulfate concentrations to some degree.

Nevertheless, he adds, “any way you slice it, all these effects are linked.” Bioturbation must have made a difference in the ocean’s evolving chemistry, he argues — an evolution that yielded today’s highly productive seas.

Quite a result from a curious phenomenon that, as Darwin noted more than a century ago, appears insignificant at first glance.