he 65-foot research vessel Squilla is idling in the lee of a stone jetty that shelters Plymouth Sound from the turbulent waters of the English Channel. On her aft deck, four men are hovering around a massive stainless steel tripod suspended from the Squilla's deck crane, ignoring the rain sheeting off their yellow rubber slickers and coveralls.
"It's a boy's toy," Melanie Austen quips as we watch from the partial shelter of a bulkhead. Austen is a marine ecologist at Plymouth Marine Laboratory, and two of the hooded yellow figures are her graduate students. The Squilla has brought us out into the sound this August morning from the Barbican, a gray stone wharf that has served the city of Plymouth on England's southwest coast for more than 300 years. It was from the Barbican that Charles Darwin set off aboard the Beagle and Robert F. Scott set off to the Antarctic. Austen and her students have set off to explore another little-known frontier barely a mile from the wharf.
The tripod suspended just above Squilla's deck cradles a box corer about a foot cubed. One of the students, Mike Townsend, and postdoctoral researcher Dave Parry, along with two crewmen who are bantering in a Plymouth patois the researchers call "barbicanese," are preparing to hoist the whole apparatus over the side and drop it to the floor of the sound where the steel box will sink about 18 inches into soft mud. When the team begins to winch the corer upward again, a steel plate will swing into place under the box and deliver us an intact chunk of the seafloor. A chunk of dark ooze teeming with life, Austen assures me.
"What you think of as plain, boring mud has got quite a lot of things living in it," she asserts. She is talking about what ecologists call the "benthos," the plants and animals living on and in the sea bottom. Because oceans cover more than 70 percent of the globe, the submerged sediments we will be coring today constitute a sample of the most extensive ecosystem on earth. They also harbor one of the earth's richest animal communities. Some 100,000 sediment species have been identified, but that may represent less than 1 percent of the creatures living in the sand, gravel, and mud—mostly mud—of the ocean floor.1 There may be 100 million nematode species alone in the abyssal ooze, and 500,000-10 million species of deep-sea "macrofauna"— medium-sized animals such as polychaete worms, burrowing shrimp, clams, and snails.2 The estimates vary wildly because scientists have only limited samples from which to extrapolate across 137 million square miles of largely unexplored seafloor. Whatever the numbers, it's clear that the benthos remains even more firmly concealed in the "black box" of the sediments than life in terrestrial dirt. To help remedy this, marine scientists from more than 50 countries began in 2000 a decade-long Census of Marine Life, using an array of new technologies to track and identify creatures from nematodes to plankton to tuna. Just as on land, however, the effort is hampered by limited funding and by a dearth of experts who know how to identify and classify organisms, especially sediment creatures.3
As with soil creatures on land, life in submerged sediments is increasingly at risk from a variety of human activities: fishing practices such as bottom trawling and dredging—the equivalent of plowing the seabed—as well as rising water temperatures from climate warming, aquaculture, oil exploration, waste dumping, installation of telecommunications cables, introductions of nonnative species, and eutrophication from excess nitrogen and phosphorus washed off the land. (Eutrophication results when excess nutrients cause algal blooms, which fuel a population explosion among microbial decomposers at the seafloor that leads to reduced oxygen in bottom waters.) Austen and her colleagues believe threats to the benthos will eventually make their mark throughout the entire ocean food web, from plankton to fish and whales. She and her students are out here to investigate what else we lose besides living diversity when we destroy seafloor habitat.
The men grab the legs of the tripod to steady the corer as the crane lifts it and swings it over the starboard rail. One of them releases the tension on the cable and the corer drops out of sight below the green surface of the sound. Minutes later, they hoist it back, streams of mud and seawater mingling with rain as they lower the corer onto the deck. They detach the box of sediment from the tripod and slide it across to where Austen and the rest of her team, student Kirsten Richardson and a field technician, are waiting.
Two of them drain the seawater from the top of the box, and then Austen jams a second corer—a stainless steel cylinder that looks like an oversized cookie cutter—into the cube of mud. Once they lift the corer off and clean away excess muck from the outside of the cylinder, they lift it over an empty 5-gallon bucket and let the round plug of mud slurp intact into it. Back in the lab, across the vast grassy sward of Plymouth Hoe from the Barbican, each white plastic bucket will become a mesocosm, a miniature replica of the seafloor world.
Today one of the team's goals is to collect 14 of these sediment cores. Their second objective is to capture any creatures they happen upon—specifically, seafloor "engineers" such as polychaete worms (marine cousins of earthworms), burrowing shrimps, urchins, mol-lusks, and other macrofauna that stir and aerate the sediments just as bioturbators do on land. In 1891, a decade after Darwin published his treatise on the engineering powers of earthworms, scientists began to investigate the work of their marine relatives—specifically, burrowing polychaetes known as lobworms. Marine scientists have since come to believe that these and other creatures that burrow in sediment
Seafloor creatures such as burrowing shrimps, clams, polychaete worms, and brittle stars stir and aerate the sediments, enhancing the cycling of nutrients that support the ocean food chain.
are vital to nutrient cycling in the oceans, just as bioturbators on land hold significant sway over nutrient processing.
More than 80 percent of all the decomposition and nutrient cycling that takes place on the earth occurs in sediments on the continental shelves and slopes up to 1.2 miles deep, although these areas represent only 16 percent of the area covered by seas.4 Most of the dead organic matter that is broken down and recycled in these sediments arrives in the form of algae (phytoplankton) that grows on the bottom in shallow areas or that dies and sinks down from sunlit surface waters, along with fecal matter and carcasses of animals ranging in size from zooplankton to worms to whales. Closer to shore, terrestrial runoff including fertilizers and other human wastes can also form an important part of the organic matter input. The nitty-gritty work of recycling all this material is handled by bacteria and fungi, just as in terrestrial soils. These microbes dine on organic matter and release as waste various forms of nitrogen and other nutrients. One microbial waste product, nitrate, is a key fertilizer of the algal growth that forms the base of the ocean food web.5 One-third to one-half of the nutrients needed to fuel the growth of algae in the seas above the continental shelves is released from the sediments.6
Just as on land, however, the activities of larger sediment animals enhance the nutrient cycling process. Like earthworms, marine bioturbators burrow, bulldoze, stir, and "rework" bottom sediments as they feed, increasing the penetration of water, organic particles, oxygen, and other dissolved substances deeper into the sediment, where decomposer microbes do their work. This stirring also speeds the release of microbial wastes such as nitrate from the sediments to the water column.7 By creating hotspots of microbial activity, bioturbators also attract pinhead-sized animals known as "meiofauna"— nematodes, flagellates, ciliates—that dine on the microbes or their leavings and thus accelerate the recycling of nutrients tied up in mi-crobial cells. Altogether, the presence of bioturbators can as much as triple the metabolism of seafloor communities—that is, the oxygen breathed in and the carbon dioxide released. Only a fraction of this reflects the breathing of the bioturbators themselves; most comes from enhanced activity of decomposer microbes.8
What then would it mean for the health of the oceans and the diversity of sea life—including economically valuable fish stocks—if human activities such as bottom fishing greatly reduce or eliminate the work of bioturbators? Are some of these creatures more important than others to sustaining healthy seafloor habitats? How quickly can various benthic communities recover from different types and intensities of fishing? As the United States, the nations of the European Union (EU), and others move toward more comprehensive ecosystem management of fisheries, these questions have become increasingly significant. It is this larger EU interest that drives today's muddy work by Austen and her team.
"Oooh, there he goes," Austen exclaims as her hand darts into the muck of the next core. She pulls out a 2-inch mud shrimp that she spotted trying to make its escape. With her other hand, she pokes around the core surface and pulls out a chunk of the shrimp's burrow, a tube with sides the thickness of a clay flowerpot, slightly brownish in color compared to the dark gray mud from which the shrimp fashioned it. This shrimp is Upogebia, an orange-colored suspension feeder that pocks the seafloor with its large burrow openings. Suspension feeders are animals that filter organic particles from the water. Many suspension feeders, including Upogebia, some polychaetes, brittle stars, scallops, and clams, nestle into the sediments and poke tentacles, arms, antennae, or siphons into the water to capture food. Others such as sponges, anemones, moss animals (bryozoans), sea squirts, and some crustaceans live atop the sediments.
Austen tells me there is another, smaller shrimp in these waters, the ghost shrimp Callianassa—Greek for "beautiful queen"—whose single oversized claw can be nearly half the length of its body. It is a deposit feeder, meaning it actively mines the sediments for organic particles. Callianassa also serves the role of a "conveyor belt" for bringing up buried organic matter, foraging deep in the sediment and casting fecal pellets on the surface like a night crawler. As it burrows and feeds, it pimples the seafloor with volcano-shaped mounds.
Shrimp are territorial and will fight if thrown together, so Mike Townsend opens up a Toby Teaboy—an orange plastic tea infuser lined with nylon mesh—and cages Austen's mud shrimp before dropping it into a bucket of seawater. He also drops in a half dozen i-inch, cone-shaped Turritella snails that he and the others have combed from the mud. Out here where they live and work, these snails are depositfeeding bioturbators. Most people encounter them in shell shops, however, sliced lengthwise into decorative cross sections for use in crafts and beadwork.
Another box load of mud arrives and Austen points to the poly-chaete burrows and tubes pocking its surface. She fishes in the mud and hands me a 2-inch-long pinkish brown worm called Nephtys. Each of its body segments sports a pair of footlike parapodia ending in a cluster of bristles. The worm wriggles sideways in my palm, each segment moving in sequence in an incredibly fluid motion. Indeed, Nephtys is commonly called the shimmy worm for this undulating motion by which it swims. Some 10,000 species of polychaetes have been described, but the actual number may be two or three times that. These bioturbators can be found in the top 2-4 inches of almost all marine sediments, usually in great numbers, and are often among the first midsized animals to colonize new or disturbed sediments. Among them are a rich diversity of suspension feeders, deposit feeders, mud swallowers, algal grazers, predators, and even a few parasites.9
As the hours pass, the number of shrimp-filled Teaboys and less belligerent creatures in the bucket grows, as does the number of sediment-filled buckets lined up along the stern rail. Everyone is smeared with mud, despite the rain.
"I have friends who think being a marine biologist is a glamorous job," Kirsten Richardson tells us as she tries to rinse the mud from the ends of her plaited hair with cold seawater.
Austen says her 11-year-old nephew should be out here: "He thinks it's a bit exciting having an auntie who's a marine biologist. Of course, it's not always as nice as this when we go out," Austen adds, pushing wet strands of hair from her face. Although she is teasing, she has indeed done this same work in much worse conditions, coring seafloor mud in coastal waters from Greece to Norway, in winter as well as on wet summer days such as this.
Were you one of those students who thought marine biology would be glamorous? I ask. "Oh, yeah! Didn't we all?" she laughs. "Slinging buckets of mud around. I'm sure it wouldn't be many people's cup of tea. But everybody's got their thing. There aren't many people who get to do the glamorous cetacean [whale] work," she says without a hint of envy.
Actually, Austen began her research career focusing on creatures even less charismatic to most people than shrimp and worms: pinhead-sized creatures known collectively as meiofauna, especially nematodes. She still spends part of her time investigating what influences their biodiversity—say, why there are more nematode species in one part of an estuary than another. "I've always looked at ecology in that respect: Why do different communities have different diversity?" she says. "Now this is leading into, does that diversity matter? This is the next step." The question has drawn her into a number of international collaborations and projects, but it has not pulled her away from the mud.
By now, everyone is dishing into the dark ooze as they clean up the cores and hold out offerings to me: brittle stars, a lovely little whelk, a tiny sea cucumber, a half-inch spiny cockle named Acantho-cardia, a 1 1/2-inch ottershell clam called Azorinus that sports two siphons and makes two holes in the mud, and a larger clam Lutraria, which has a single big muscular siphon.
Austen holds up her open palm to show me another polychaete, an inch-long "sea mouse" also known as Aphrodita. I ask why the Greek goddess of love and beauty shares her name with this creature, which looks to me like a hairy little slug. "Because they're really pretty underwater," she says. "Their bristles are iridescent."
Someone offers me another little brittle star, Amphiura, a creature that lives just beneath the sediment and waves its arms in the water to capture food particles. Next comes a 1-inch burrowing sea urchin—Echinocardium, the heart urchin. Echinocardium and a similar Norwegian heart urchin, Brissopsis, serve as living bulldozers, pushing their way through sediment as they feed.
Austen rakes her fingers gently through the silky mud atop another core and holds up five more Turritellas. "You can get 10 raking the top like that, so they must be doing something down there," she asserts.
By the time the final core has been slurped into its bucket, the skies are clearing. In the Squilla's galley, we fix tea and snack on ginger cake as the vessel motors a short distance across the sound to Jenny-cliff Bay where the nearshore bottom is covered with muddy sand. The crew breaks out a small sampling dredge—an iron ring big enough for a person or two to slip through and fitted with a mesh bag formed from several layers of netting. They toss it over the side and the boat chugs slowly in a circle for a few minutes, dragging the gaping mouth of the dredge through the sediment. This dredge is largely for my benefit, although the team also hopes it will yield more creatures to populate their laboratory mesocosms. The crew winches the dredge back up to the rail. The net is full to the ring with mud, so they try hosing it with seawater. As I watch, it seems the mud is being held together by a thick mat of plant roots, as though a large and terribly root-bound potted plant had been tipped out into the net. But there is no garden beneath us. The mat is a tangle of worm tubes made by the polychaete Melinna. Dave Parry peels open one of the brown rubbery tubes and pulls out a 1 1/2-inch-long worm.
The vessel moves closer to the shore and the crew drops the dredge again. This time they shovel the catch into plastic laundry baskets, and Austen and her team begin pawing carefully through the muck, intent as treasure hunters at an estate sale. Their efforts yield a tiny sea squirt, a tiny crab, and a literal handful of other prizes. As we motor back toward the Barbican, the sun breaks through the clouds.
About 30 percent of the world's fish catch comes from bottom fishing using towed trawls and dredges as well as immobile or fixed gear such as gill nets, long lines, and various crab and lobster traps.10 Marine scientists have grown increasingly concerned about the chronic upheaval created by this industrial fishing gear on seafloor habitats and creatures. Bottom trawls—heavily weighted, bag-shaped nets that can have mouth openings wider than the length of an American football field—are primarily used to catch shrimp and groundfish such as cod, haddock, and flounders. Dredges are rakelike devices with bags— usually with rigid openings—used to collect scallops and clams. Hydraulic clam dredges blast the seabed with jets of water, turning sediments to slurry and floating clams upward to be sieved out by the rakelike prongs or blades of the dredge.11
No agency keeps figures on the global extent and frequency of bottom fishing, but one research team estimates that trawlers plow up about 6 million square miles of seabed annually—an area about 20 percent the size of the Atlantic Ocean and 150 times greater than the area deforested by loggers worldwide. In some areas, trawls drag the seafloor multiple times a year.12 Prime fishing grounds such as the North Sea and the Gulf of Maine, for instance, get trawled at least once a year, disrupting food webs in the sediment and water column over a large part of the world's continental shelves.13 Increases in the size and power of fishing vessels and mechanization of gear have greatly extended the reach of such trawlers. About 40 percent of trawling now takes place in deeper waters beyond the continental shelves, including slopes, canyons, and isolated submarine peaks known as seamounts, which are extensively trawled for fish such as orange roughy and blue ling.14
Historically, the deep sea bottom was considered a nearly lifeless desert, but a landmark study in the late 1960s disproved that notion.15 Indeed, recent assessments have suggested that the deep sea may support a richer array of species than the continental shelf, and abyssal mud habitats host highly complex communities of polychaetes, mol-lusks, and small buglike crustaceans such as amphipods (sand hoppers) and isopods (sea centipedes and sea lice).16
The direct effects of such fishing on the seafloor have been extensively studied, but the significance of those effects is still hotly debated. Dragging heavily weighted gear over the ocean bottom homogenizes the terrain, reducing natural crevices and hills (but creating new ridges in the tracks of the trawl), crushing or burying worms, sea grasses, sponges, and corals, and eliminating predators such as flatfish, crabs, and shrimp.17 Further, up to 85 percent of the mass of sea life scooped up in a trawl may be unwanted "bycatch," creatures that are dumped overboard dead or dying.18 Some marine scientists have compared trawling the seabed to clearcutting forests, a practice that would draw public outcry were it visible to us.19
A report by the U.S. National Research Council in 2002— prompted by legislation that now requires fisheries managers to address the impact of fishing on "essential fish habitat" as well as on fish stocks themselves—found that the ecosystem effects of trawling depend, understandably enough, on what type of gear is used in what type of habitat, and how often and how extensively the area is fished. In general, the most vulnerable are stable communities, seldom subjected to natural disturbance and filled with largely sedentary, long-lived species such as corals, sponges, sea grasses, and large clams, as well as gravel and mud habitats. Least vulnerable are communities of mobile, hard-bodied, short-lived species inhabiting naturally changeable environments such as sandy areas swept by bottom currents. The effects of fishing disturbance are cumulative, and the severity depends on the frequency of trawling and dredging. Repeated passes with trawls and dredges may or may not reduce benthic species diversity, but they do drive a change in the types of species in the area, usually a shift from relatively large animals toward small, fast-growing, opportunistic creatures.20
Some in the fishing community have argued that this change can be beneficial. Trawling is analogous to plowing a field, the reasoning goes, and in heavily trawled areas of the North Sea the result might even be an increased crop of fish food—mainly worms—along with enhanced stocks of commercially important flatfish such as Dover sole and plaice. But the 2002 National Research Council report concluded that this notion doesn't hold up to scrutiny. Indeed, studies published in that same year found that beam trawling (beam trawls are funnel-shaped nets fitted underneath with many heavy "tickler chains" that rough up the sediments to scare buried flatfish up into the nets) dramatically decreased the number of large animals without affecting the amount of polychaetes that serve as prey for flatfish.21 What's more, the relationship between mud-dwellers and fish stocks is clearly more intricate than the direct provision of food for bottom-feeders. For example, complex seafloor habitats are known to be important for the survival of many types of fish, providing nursery grounds for juveniles as well as hiding places and food stores for adults.22 And then there are the invisible ripple effects of such trawling practices on the diversity and productivity of the oceans that are only beginning to draw serious attention.
Back in Austen's office at Plymouth Marine Laboratory, I watch as she pulls up two bright blue sonar images on her computer screen. The left image shows an expanse of seafloor mud pocked with holes— burrow entrances. The right image shows only a series of parallel lines like furrows in a cornfield. The furrows are trawl scars, Austen tells me. No holes are visible.
"Using side-scan sonar, we can see the effects of fishing on the bioturbators visually just like you can on land," she says. It's not quite like walking through a forest and looking for earthworm burrows, but technology is allowing ever greater access to a frontier that is otherwise invisible and inaccessible.
"This is in Norway where we compared trawled areas and non-trawled areas and took samples," she resumes. "It's especially obvious there's a big difference in habitat there. You can actually count the number of burrow entrances before and after trawling from the video. These holes are made by Calocaris, a burrowing shrimp that only goes to about 6-10 centimeters [2-4 inches] depth. That's the same depth the trawl will go to in these sediments."
What she is showing me on the screen are the obvious direct effects of the fishing practice in reducing the number of burrow entrances —and presumably the bioturbators that created them. For Austen and her colleagues, the key question is, so what? Do the creatures in the sediment really affect the functioning and the productivity of what's above the sediment?
"That's what we're trying to find out," she explains. "Most people have been asking whether the community of animals on a bit of seabed is the same or different after you haul a trawl over it. People have been accumulating that sort of evidence for a long time. But people haven't really thought about, okay, so what if the benthos changes, is that a bad thing or is that a good thing, and what's it affecting? Why does it matter for the rest of the ecosystem if you have just worms there? We're asking, does that change nutrient cycling? And if it does change nutrient cycling, does that really matter? We want to develop predictions about how primary productivity will change in response to fishing practices in specific fishing lanes from the Aegean to the North Sea. Then from that, we also hope to use fisheries models to see if a change in primary [algal] productivity actually leads to a change in the productivity of the fisheries as well."
Along with research partners in the United Kingdom, Ireland, Norway, the Netherlands, Greece, and Poland, Austen is exploring these questions as part of an EU-sponsored project called COST-IMPACT—"Costing the impact of demersal [near-bottom] fisheries on marine ecosystem processes and biodiversity."23 The team includes economists as well as marine scientists, and their goal is to use the results of their research and modeling to help managers and policymakers examine tradeoffs between current fishing efforts and protection of seafloor habitat, biodiversity, ecological processes, and the long-term vitality of the fishery.
It's all part of the drive toward "ecosystem management" of fisheries, Austen says, although that term means different things to different people: "To many of the world's monitoring agencies and government agencies, it used to mean—and sometimes still means— looking at multispecies fisheries instead of just looking at a single fish stock. Or maybe they will look at a single fishery species and its food chain—cod, and what the cod eat, and what eats the cod. For other agencies, 'ecosystem' means looking at social changes, and who's affected by how we manage the seas."
The first step for the research team has been to summarize results from the growing number of fishing impact studies to try to pin down just what is likely to happen when a certain type of gear is dragged through a specific type of seafloor habitat, and how long it takes the habitat and the community to recover from that fishing practice. Using a statistical procedure called meta-analysis, the researchers have integrated the sometimes inconsistent findings of 101 different experimental studies conducted in the seas off various parts of Europe, the Americas, Australia, and South Africa and involving different combinations of fishing gear and habitat.24 It would be another 10 months after my visit before the analysis was complete, but the results broadly confirmed many of the expectations from previous synthesis efforts using fewer studies.25 The most severe effects on the benthos occur when scallop dredges (metal frames with rakelike teeth and attached chain-mesh bags) are towed through habitats full of corals, sponges, sea grasses, animal burrows and tubes, and other "biogenic" features, for instance, or when dredging takes place in the muddy sand of the intertidal zone (the shoreline area between the high and low tides). On average, intertidal dredging in muddy sand reduces either the abundance of a specific animal species or the total number of benthic species by an astounding 72 percent. It can take years for such communities to recover and for the furrows left by the dredge to be erased. Large, slow-growing sponges and soft corals can take as much as 8 years to rebound after being crushed by a dredge. In contrast, poly-chaetes in sandy habitats regularly scoured by waves or currents may spring back in a matter of months.
Besides learning which gear causes the greatest impacts in a given habitat, researchers also need to learn more about the work of various creatures that live in harm's way. What happens when you eliminate this type of urchin or that shrimp or worm from a seabed community for months or years? This is where the buckets of mud and animals Austen's team collected this morning fit into the picture.
Austen leads me into a large, relatively cold, and dimly lit room adjacent to her office. This is the mesocosm lab where mud cored from the seabed and plopped into buckets is used to investigate the work of benthic animals. Rows of gray fiberglass tanks run almost the length of the room, each divided into four seawater-filled sections. The air temperature is kept at 59° F to help keep the water cool. Covers made of black landscape cloth draped over bamboo frames sit atop most of the tank sections or wells. All of this is designed for the comfort of creatures accustomed to the cold, dark subtidal seafloor. We have to raise our voices to be heard over the noise of the pumps moving saltwater through the tanks.
The newly collected Turritellas and other creatures the team pulled from the mud of the sound are sitting in black plastic holding tanks at the back of the lab now—except for the shrimp in their Teaboy cages, which are floating in one of the wells. Austen points out that a few of these creatures are on the shortlist of animals already known from past studies to be important for nutrient cycling. These include burrowing shrimps like Upogebia and Calocaris, heart urchins, brittle stars like Amphiura, small clams, and large worms such as polychaetes and sausage-shaped spoon worms (Echiurans). Even among these significant players, there are hierarchies of influence, Austen and her colleagues are finding. For instance, bulldozing heart urchins and burrowing shrimps have stronger impacts on nutrient cycling than Astarte and nut clams, brittle stars, or polychaetes such as Nephtys.26
Austen and Townsend position a rolling electric winch and begin lifting buckets from the morning coring into the wells one by one. The winch is necessary, Austen says, to prevent "benthos back," an injury caused by too much lifting of heavy buckets of mud. Townsend is using these and other cores to compare bioturbation in sand and mud sediments and a year later will be able to report that bioturbators have definite effects on nutrient cycling in these habitats, although as expected, the effects are stronger in mud than sand.27
On the floor at the back end of one long tank I notice smaller half-gallon buckets of sediment. Austen tells me these are filled with thousands of nematodes, protozoa, copepods, tardigrades, flat worms, ribbon worms, and other pinhead-sized animals. She imagines the sediment literally "fizzing" with the activity of a thousand of these tiny creatures, and she wonders how their accumulated impact might compare with that of 70-80 clams, shrimp, worms, or other large bioturbators.
Some nematodes and copepods do form burrows; others churn sediments as they feed or migrate up and down. Indeed, some marine scientists believe these tiny animals with their vast numbers may greatly influence the physical, chemical, and biological properties of sediments, including nutrient cycling, perhaps as much as the larger sediment animals in some habitats. Some of the larger animals actually serve in the ranks of "pinheads" during their juvenile stages. During that time, the teeming community of tiny animals just might help shape the assemblage of larger animals that share their habitat by preying on their larvae and influencing the living conditions the larvae must endure.28
Trawling, in general, seems to increase not only polychaete worms but also possibly the pinhead community.29 Austen points out: "You get a shift to these smaller organisms, but whether they can actually substitute for all the ecosystem functions of the macrofauna and create a simplified system that can keep up nutrient cycling, we just have no idea."
She thinks that's unlikely, however, because tiny animals cannot stir up the deep sediments enough to let oxygen in and allow the nitrate wastes given off by microbial decomposers to diffuse into the water column.
"If you've got a diverse mix of bioturbators doing different things at different levels in the sediment—urchins bumbling around, worms moving up and down, bivalves at the bottom creating burrows, shrimps creating burrows—you end up with quite a deep oxygenated zone in the sediment," Austen points out. If the sediment harbors only tiny animals such as nematodes and copepods, the oxygenated layer will be much thinner. That means the nitrates produced during decomposition are more likely to end up in low-oxygen sediments where other bacteria will deactivate them [that is, denitrify the nitrate by converting it to biologically unusable nitrogen gas]. If less nitrate is released into the water, "then you've got less algal productivity and probably less fisheries," she says. "So in a nutshell, we think that probably a well-mixed and oxygenated sediment layer is likely to be the key thing, and to maintain that, we need a diversity of these bigger bioturbators."
Bioturbators perform other important work in the sediment besides stirring things up and indirectly servicing the food chain, and when they are reduced or eliminated by trawling, their loss can have ripple effects on the biodiversity of the seafloor.30 Austen and Stephen Widdicombe, a senior scientist at Plymouth Marine Laboratory, have shown in a multiyear series of experiments at a mesocosm lab in Norway that some of these creatures exert a strong influence over which other species are present and in what numbers in their communities. Changes in the species of major bioturbators present—even shifts among species that are considered functionally similar in their feeding and sediment-disturbing habits—or changes in the density and distribution of bioturbators can alter the fate of other species in the community.31 Dense patches of heart urchins scattered here and there through the sediment, for instance, can lead to greater diversity in nematode communities across a region.32 The more heart urchins, brittle stars, or sea mouse polychaetes, the higher the biodiversity of other species in a community. The predatory polychaete Nephtys has the opposite effect—at high densities it lowers the diversity of other species in the neighborhood. In contrast, Calocaris shrimp, despite their burrowing, seem to exert no detectable impact on the diversity of other species in the community. All of the bioturbators just mentioned can be reduced or eliminated by trawling.33
Evidence from the fossil record suggests, in fact, that these "biological bulldozers" have exerted a powerful influence over sediment communities ever since they began to proliferate and diversify in the Devonian period 395 million years ago. Their rise has been credited with causing a parallel decline of immobile suspension feeders in soft sediment habitats. Many suspension feeders found in marine mud today are mobile burrow-forming species such as the mud shrimp Upo-gebia and the brittle star Amphiura. Rates of bioturbation and thus sediment stirring and disturbance are believed to have increased several orders of magnitude with the diversification of urchins, shrimps, lobsters, sea cucumbers, crabs, and other bulldozing animals. Some biologists believe the resulting acceleration in nutrient cycling helped to fuel greater algal productivity, diversification of algal species, and an explosion of new species of planktonic animals (zooplankton) that feed on algae.34
All these revelations about life in the mud may be exciting to ecolo-gists, but how is a fisheries manager supposed to weigh the work of an urchin or worm or clam—or an entire fishing lane teeming with such beasts—against the social and economic benefits of a prosperous fishing industry? For that, Austen and her colleagues are turning to economists.
"If we say something is important, agencies want to know what to do about it," Austen says. "So we've got economists who are looking at these issues: If nutrient cycling changes, how do we put a value on that? If the biodiversity changes, can we value that? We are trying to set up a decision-support system for management to help them weigh up the pros and cons and balance biodiversity against economic outcomes, jobs gained, et cetera, by adversely affecting the benthos. What happens if you limit fishing or gear types in certain areas or declare marine protected areas? That's where this could and should go."
Attempts to value the ecological services a healthy ocean provides have been few and have focused at a global scale. In 1997, a team of ecologists and economists led by Robert Costanza, now director of the Gund Institute for Ecological Economics at the University of Vermont, created a stir when they estimated the minimum value of the world's ecosystem services and "the natural capital stocks that produce them" at US$33 trillion per year. (Natural capital includes trees, animals, rivers, oceans, and other natural resources and systems that generate goods and services vital to human welfare, including the creation of manufactured capital such as machines and buildings.) The global oceans account for two-thirds of that value because of their vital role in regulating climate and the cycling of water, nutrients, and carbon; absorbing and diluting contaminants; and providing us with food, recreation, and employment.35 What portion of that value is supplied by the mud-dwellers of the global seas? The mud-dwellers of a regional fishing ground? How is that value affected by various fishing practices?
Although economists and marine scientists grapple with answers that will fit into cost-benefit calculations, fisheries managers are beginning also to acknowledge the intrinsic value of some seafloor habitats. Since the 1990s, for instance, the extent and intensity of bottom trawling in U.S. waters have been reduced as managers closed some areas to fishing, restricted fishing seasons, or required gear modifications to minimize bottom contact, usually in response to declining fish stocks. A prime example is the ban on trawling in the wake of a collapse in cod and haddock stocks in New England and off Georges Bank (east of Massachusetts).36
At the urging of ecologists and environmental groups, some unique benthic communities such as slow-growing deepwater corals— most of them only now being explored and charted—have gained protection from trawling in a few areas: the Oculina Banks off Florida's Atlantic coast, some coral beds off Nova Scotia, 19 seamounts in New Zealand waters, and an extensive reef area off Norway.37 Just that morning, in fact, we had heard on BBC radio that the EU would issue an emergency ruling closing the coral-rich Darwin Mounds off the northwest coast of Scotland to trawling for 6 months while European nations considered a permanent closure.
Soft-bottom marine life is getting little, if any, protection right now in most of the world, and few environmental advocates champion its cause. Yet in Austen's view, the vast subtidal mud plains are to ocean life what the Serengeti plains are to African wildlife.
"The analogy I've often used is this: If you go to the Serengeti plain and look at all the mammals that are there—zebra, wildebeest, lions—they're all completely dependent on the grass. And if the grass were plowed up on a regular basis, the rest of the stuff on top would disappear sooner or later. I think we're talking about the same sort of habitat here. If you just keep plowing up the seabed, you're eventually going to lose the life in the waters above it, one way or another."
It occurs to me, however, that as fish stocks collapse, we might not be able to tease out these bottom-up effects on the food chain that Austen is talking about from the impacts of overharvesting, ocean warming, pollution, and all the other direct human affronts to the oceans. By 2002, for instance, 72 percent of the world's ocean fish stocks were being harvested faster than they could reproduce.38
"It's a bit of a race, isn't it, whether they just scoop up so many fish that that has a quicker effect than what they're doing to the seabed," Austen acknowledges. "They're undermining it from two levels, top-down and bottom-up. We're just looking at how important is the bottom-up effect at the moment, and there are plenty of fisheries people who are looking at how important is the top-down cascade effect of taking out the top predators, then the ones below, then the ones below them. You're hitting it both ways, and neither can be terribly good long term. You can't make a sustainable fishery like that.
"If you went into the Serengeti and just plowed up bits of it occasionally in a controlled way, then you could probably keep it so that you'd have just enough habitat to maintain viable populations. But there's no way you can keep plowing up more and more of the seabed and maintain populations; and there's no way you can keep harvesting more and more fish and maintain viable populations forever."
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