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Reshaping Decades-Old Scientific Theory

How simple things influence salt marshes and coastal ecosystems

Duke Marine Lab's Brian Silliman

There are snails in Brian Silliman's boots, mud splattered across his waders, and slices from cordgrass leaves on his arms. As he pushes deeper into the waist-high grasses, shells crunch underfoot and something darts through the shadowy water below. A crab perhaps. Or maybe a snake or baby alligator.

He stops, shifts for better footing in the spongy soil, and bends to get a closer view.

Silliman is in his happy place.

At age 40, Silliman, who joined the Nicholas School faculty last summer as Rachel Carson Associate Professor of Marine Conservation Biology, is among his generation's most astute observers of salt marsh ecology.

His meticulously executed field studies have reshaped decades-old scientific theory about how salt marshes and other coastal ecosystems work, the roles animal communities play in them, and human impacts on them.

Since 2001, he's published more than 100 peer-reviewed papers; co-edited two books; won awards from the National Science Foundation, the Andrew Mellow Foundation, and the American Society of Naturalists; and been named a David H. Smith Conservation Fellow at The Nature Conservancy and a visiting professor at the Royal Netherlands Society of Arts and Sciences.

It's heady stuff. But today, as he intently scans the surrounding marsh grass for signs of unusual activity, Silliman is focused on something closer at hand. He's searching for inspiration.

"When I'm looking for a new project, I jump into the field. If I observe something happening that, theoretically, shouldn't or couldn't be happening, I'm hooked," he says. "I'm drawn to things that seem to run counter to expectations."

It's a path he's followed since his undergraduate days at the University of Virginia, when, at the end of his junior year in 1994, he turned down a summer law internship to take part in a National Science Foundation Research for Undergraduates program in a salt marsh on the Virginia coast.

"I majored in history and environmental science and intended to go to law school, but didn't want to look back on the NSF program as a missed opportunity," he says. "I'd never been to a salt marsh before. The idea of doing field research appealed to me and spending the summer at the coast also sounded good. So I went. And it changed my life."

salt marsh snail

Baby marsh snails hiding from predators in the furls of dead leaves, Photo by Brian Silliman


Getting His Feet Wet

His first assignment in the NSF program was to come up with the research project he wanted to conduct.

"In field work, you have to use what the environment provides," he says, "so I walked out into the marsh and looked around. I figured I could either work with the snails that were filling my boots or the crabs that were constantly under my soles."

Silliman was particularly intrigued to notice that periwinkle snails, the most common animal species in eastern U.S. salt marshes, were climbing up and down the leaves of many cordgrass plants.

"They were feeding on the grass in an unusual way, cutting the leaves with their teeth and eating fungus out of the cuts," he explains. "This puzzled me. Marsh grasses were considered invincible -- so tough and fibrous that they were inedible while alive. According to what I had learned in class, animals weren't supposed to be eating them. Yet I was observing the most abundant animal in the marsh doing just that. So I asked: Are these snails affecting the growth of the grasses? Answering that became my summer project."

Using wire fencing from a local hardware store, he built a cage around a plot of grass to prevent snails from getting in. At the end of the summer, the grass inside the cage towered over unprotected clumps nearby.

"It was like a monster Chia grass poking up in the middle of the marsh. The cage had protected it and revealed that snails were exerting top-down control of the marsh. That was very novel," he says. He proudly presented his findings and hypothesized that the snails could strongly regulate cordgrasses' growth.

An outside reviewer brought in by NSF to evaluate the students' projects believed he was wrong and challenged him on it.

"He politely pooh-poohed what I had done," Silliman recalls. "So I got excited and knew I had found something neat, and decided that instead of going to law school I would stay on and go for a PhD cover in ecology to prove my observation was right."

After completing a master's degree in environmental science at Virginia in 1999, he headed north to Brown University to pursue a PhD in ecology and evolutionary biology under Mark Bertness, one of the world's leading salt marsh ecologists. There, Silliman built upon his initial observations about snail-grass interactions to conduct a broader study of the role animals play in marsh productivity.

His findings upended prevailing scientific theory.

"By showing that crabs and other marsh predators inhibit the snails, which in turn inhibit the grasses, I was able to demonstrate that marsh productivity and health are not just controlled by nutrient availability. Animals play a role, too," he says. "Field experiments I conducted in North Carolina, South Carolina and Georgia showed this was not just a localized phenomenon."

Silliman's discovery of this simple "trophic cascade" implied that overharvesting of snail predators -- including commercially harvested species like blue crabs -- might be an important but previously unrecognized factor contributing to the massive die-off of salt marshes that was occurring across the southeastern United States.


11-foot American alligator entering a fully marine salt marsh creek to forage on fish, sharks and rays, Photo by James Nifong

The research yielded another surprise, as well.

It turns out that the snails were farming fungus on the marsh grass. By cutting the grass with their teeth, they were creating an environment inside the cuts where invasive fungi could establish themselves and grow. It was the first example of fungus farming in a marine environment beyond insects, and it suggested that these snails were actively increasing their species' odds of survival by generating their preferred food source, not just eating whatever they found.

"This was a previously undemonstrated ecological mechanism through which grazers in a marine ecosystem exert top-down control of plant productivity,"

Silliman says. "Clearly, these organisms were doing more than we gave them credit for."


A Broader Focus

Silliman's research under Bertness at Brown yielded two peer-reviewed publications in the Proceedings of the National Academy of Sciences (PNAS) and established him as a young ecologist to watch.

A subsequent paper, published in Science in 2005, less than a year after he completed his PhD, confirmed his stature. By then, the massive die-off of southeastern salt marshes stretched from Louisiana to Georgia. Hundreds of thousands of acres of vital marsh habitat had been lost. Because the die-off coincided with a severe region-wide drought, many experts assumed the drought was to blame.

Based on his studies of the trophic cascade and the effects of overgrazing, and his knowledge of marshes' natural resiliency, Silliman suspected it wasn't that simple.

"I investigated and discovered the dead marshes were teeming with snails," he says. "There were 2,000 to 3,000 snails per square meter. You couldn't even see the ground in some places."

Some scientists theorized that the snails were attracted to the dying grass, but field studies Silliman conducted in the following months suggested otherwise. His work showed that as drought killed off some grasses within a marsh, snail populations began congregating in the remaining live patches. When they achieved critical mass in these patches, they killed this grass, too, and then spread to new areas of grass, which they also killed.

"It wasn't just the drought," he says. "We found that salt stress and snail stress are additive. When drought reduces water flow and increases a marsh's salt content, plant growth is reduced by 50 percent. If you add in snail overgrazing, plant growth is reduced by another 50 percent. It's a 100 percent loss. You have a dead ecosystem."

It was the first time any research had shown that climate stress could trigger runaway consumption by grazers in any marine ecosystem.

Follow-up studies over the next four years in salt marshes in Chile, Brazil and Argentina proved the phenomenon of grazer control of marshes and overgrazing wasn't isolated to the United States.

"We showed that you could no longer hold up salt marshes as trophy ecosystems that were controlled only from the bottom up by nutrients, or as systems that could handle just about anything humans or nature threw at them," says Silliman, who by this time was a tenure-track member of the biology faculty at the University of Florida. "Marshes are resilient, but they have a breaking point."


Lessons from Louisiana

Five years after the publication of his groundbreaking Science paper, Silliman turned his attention to another massive die-off of salt marshes. This time, however, there was no question of where to place the blame.

"I remember watching the first news reports about the BP oil spill and feeling sick when I saw the oil washing up on Louisiana's marshes," he recalls.

To assess the damage and see if remediation efforts would work, he applied for $200,000 in funding from BP as part of their legal settlement. His team was on the ground in Louisiana three months later. They focused their study in marshes along Barataria Bay on the state's southeastern coast, where some of the heaviest oil came ashore.

"It looked like a thick black belt stretching for miles along the shoreline. You could see the grasses underneath it were dying and decaying," he says. "Their roots were dissolving, leaving nothing to hold the soil in place."

With little time to waste, Silliman set two chief goals for his team's research. First, they would establish to what extent the oil spill was accelerating the loss of the region's marshlands, many of which were already rapidly disappearing as the result of erosion. Second, they would document how long the oil-induced die-off continued, and what factors sped or delayed the regrowth needed to slow future erosion.

By measuring erosion over the next two years at three heavily to moderately oiled sites in Barataria Bay and comparing it to erosion in three unaffected marshes, they found that oiled marshes in the bay were receding by about 10 feet a year -- about twice the rate of non-oiled marshes.

"Doubling the rate of erosion is huge, especially in an area where you have rapid erosion taking place already," notes Silliman. "If there had been a hurricane after the spill, the losses and erosion would have been even worse."

The accelerated erosion lasted for about 18 months. By then, enough roots and grasses had regrown on exposed marsh flats just behind where the oil hit to establish a new line of defense. Silliman and his team published their findings in PNAS in late 2012, just months after taking the final measurements.

It was important to get the paper out as quickly as possible, he explains, because it challenged one of the major theories of marsh ecology. Past studies on how salt marshes respond to oil spills had been done in small patches in marsh interiors, where the oil was introduced to test plots by the researchers. Those studies suggested marshes could recover relatively quickly. But in this case the spill affected around 45 linear miles of marshes, and the oil landed on the much more vulnerable edge of the marshes, where rapid erosion was already occurring.

"This taught us a lesson," Silliman says. "Using small-scale tests to predict how an ecosystem will respond to a disaster like an oil spill has serious limitations. We need to scale up our research. Location and scale really matter."


Proud to be a Dukie

In 2013, Silliman left the University of Florida to join the Nicholas School faculty as Rachel Carson Associate Professor of Marine Conservation Biology at the Duke Marine Lab in Beaufort. Although he earned his undergraduate and masters degrees at a rival ACC school, and was raised in Louisville, Ky. -- where, rumor has it, they play basketball, too -- he jumped at the chance to become a Blue Devil.

"From a professional perspective, the history of the Duke Marine Lab was a huge draw. It's one of the most influential marine science institutes in the world," he says. "And from a personal perspective, how could I say no? I come from a big basketball family. My uncle, Olympic gold medalist Mike Silliman, played with Coach K at West Point."

The proximity of Beaufort to the marine environment doesn't hurt, he adds. His office in the newly opened Orrin H. Pilkey Research Laboratory overlooks Beaufort Inlet and the Rachel Carson National Estuary. And in off-hours, he and his wife, Stephanie Wear, lead scientist for coral reef conservation at The Nature Conservancy, love exploring local marshes, creeks and beaches with their children, Parker, 7, and Leah, 4.

"Parker loves snakes and reptiles, and has even caught alligators with me, and Leah loves to collect shells and marsh plants," he notes with pride.

Despite moving his lab and family more than 650 miles from Florida to North Carolina, the pace of Silliman's workplace productivity hasn't slowed. He's preparing to teach two courses at the Marine Lab, one on marine ecology and the other on Caribbean ecology and conservation, taught partly in the Caribbean.

He's assumed duties as director of the Certificate in Marine Science and Conservation program for undergraduates. And 10 new studies of his, many conducted with former students at Florida, have been published or accepted for publication. They include a study in the online Journal PLOS ONE that used innovative imaging technologies to reveal novel insights into the foraging behavior of alligators, and a paper in PNAS last December that -- once again -- reshaped scientific theory by showing that it's quality, not just quantity, of species diversity that matters when it comes to enhancing how well a marsh ecosystem functions.

A lot of his findings may sound like simple common sense, he acknowledges with a laugh. Of course the quality of species diversity matters. Of course animal communities play important roles in marsh functioning. Can anyone be surprised that the size and location of test plots matter?

"These things should surprise no careful observer. But they do," Silliman says. "That's what I love about field research. The most creative things, in hindsight, often seem the simplest."