Decades of dinner: underwater community begins with the remains of a whale.

Oceanographer Craig Smith remembers standing on the deck of a research ship in 1987, amazed at what two grad students had brought up from the deep. The team was nearing the end of a research cruise off the coast of California, and the students had taken the submersible Alvin down 1,200 meters for a final dive along a familiar route. While the craft was being hoisted back on deck, Smith glanced into its basket of collected samples.

"I could see big bones," Smith says. One bone, curved like a rib, was as thick as a thigh and as tall as a man. A hefty vertebra lay against it. They could only be bones from a whale, but the ocean bottom is hardly littered with whales, as Smith knew all too well. He'd done his dissertation on organic matter that sinks to the ocean floor, but he'd never seen a whale down there. And, despite much effort, he'd never managed to sink a whale carcass.

When the students climbed out of Alvin, they reported that during a navigation wobble off the old route, they had happened upon a full whale skeleton, the first ever recorded on the ocean floor.

The videos that the graduate students brought up contained an even bigger surprise, which tipped off Smith to a new world. The videos showed clams that Smith recognized as relatives of those observed in the remarkable underwater communities that had been discovered a decade earlier around deep-sea vents and seeps. These vesicomyid clams don't eat in the usual sense but get their nutrients from bacteria that live in their gills and metabolize sulfide from the vents. However, the clams surrounding the whale that Smith had just seen were some 200 kilometers from the nearest seep.

The explanation lay in the decomposing bones, decided Smith, who is at the University of Hawaii at Manoa. The bonanza of a whale at the ocean bottom can set off a microbial feeding frenzy that uses up all the oxygen in the area. Microbes that can survive without oxygen, such as those that metabolize sulfur compounds, take over. Deep-sea vents spew sulfur compounds that power such communities, but Smith's team had discovered a distinct deep-sea ecosystem as unexpected as the vent communities were a decade before.

Since finding that initial whale-assisted community, Smith and other researchers have sampled some 20 whale carcasses on the seafloor, each supporting a biological abundance. Because whale cadavers are hard to find on the ocean's vast bottom, scientists haven't been relying on luck alone for coming up with study sites. They've been sinking already-dead whales.

The studies so far have revealed that the communities arising at whale falls, as aficionados call the sunken carcasses, display underwater versions of the classic stages of succession and change seen in terrestrial ecosystems. Instead of grass giving way to shrubs that yield to the trees of forests, whale falls first nourish such scavengers as hagfish, then bone-eating zombie worms, and eventually the clams that Smith's team recognized.

Although some whale-fall species also live on vents, researchers propose that some two dozen of the species identified so far are exclusively whale eaters.

WHALE IN A HAYSTACK Serendipity provided Smith with that first whale fall. He found another after a tip from a Navy officer in 1993. Hunting for a missile that had gone missing, the U.S. military had happened upon sunken whales near San Nicolas Island off the California coast.

Rather than wait for such flukes, Smith and other whale-fall researchers put out requests for any dead whales found in shallow water or on the shore. Smith's crew will tow the body out to sea, weigh it down with scrap metal such as old railroad wheels, and sink it where the researchers can revisit it.

If necessary, the researchers put on scuba gear to wrap a net around a decomposing carcass before towing it. That's "not a pleasant job," says marine biologist Amy Baco-Taylor of Woods Hole (Mass.) Oceanographic Institution. There's the risk of disturbing dining sharks. And the clothes Baco-Taylor wore on the towboat after helping net a whale carcass picked up such a strong and persistent odor that she had to throw them away.

Until recently, all the sunken whale carcasses were off the Pacific coast of North America, but a research crew in 2002 sank 12 stranded whales off the coast of Japan, and another team has sunk two in the past year in the Atlantic off the coast of Sweden.

The towed carcasses provide researchers with the chance to watch a whale-fall community unfold. The Swedish scientists sank one whale in water shallow enough for divers to reach. However, researchers need to use a submersible to visit the deeper sites.

Baco-Taylor says that descending in a submersible "is cool, but there are certain things that people on land don't think about, such as that there's no bathroom and it gets really cold down there."

AS THE WHALE TURNS From the time Smith first realized that whale falls are lively spots on the ocean floor, he predicted that different assemblages of creatures would appear at each site in turn. In the late 1990s, Baco-Taylor began visiting whale falls of different ages to document under water stages of succession.

To see the first stage, the submersible Alvin carried her down to visit two recently deposited whales. One whale, observed just 6 weeks after it had settled to the bottom, was still largely intact, but it had hundreds of hagfish writhing over it. These eel-shaped fish, about 40 centimeters long, use their rasping teeth to scrape bits of meat off carcasses.

Baco-Taylor says that she's seen a hagfish grip a whale with its mouth, tie itself in a knot, and use its body to knock loose a chunk of whale meat. But she was dubious that the hagfish could have made the big gouges that she saw. "While we were taking sediment samples," she says, "I looked up, out the pilot window, and there was a huge shark."

Thus, she discovered that the Pacific sleeper shark, a deep-water species that people hardly ever see, visits whale falls. "It grabs on to the whale flesh and twists its whole body back and forth, back and forth," she says. "It seems to take forever until it finally gets a piece off."

Baco-Taylor and Smith call this period the mobile-scavenger stage. They've seen some 38 species descend to whale falls for the opening feast. None of these creatures, including the sharks and hagfish, appears to eat only whale. Nevertheless, the scavengers do a good job.

In one of the researcher-sunk whales, the scavengers cleaned off the bulk of whale meat in less than 18 months. Soft tissue makes up around 90 percent of a whale's weight, and this whale weighed about 30 metric tons.

When the large scavengers finished, says Baco-Taylor, she found that a lot of smaller animals were "picking up leftovers." The species that show up during this second stage are known as enrichment opportunists.

Baco-Taylor and other scientists have reported an abundance of snails, little amphipods that look like shrimp, and segmented worms. A survey at one whale fall that had been on the ocean bottom for almost 2 years recorded that, close to the whale, each square meter of sediment hosted up to 45,000 individuals, not counting microbes.

Sometimes, Beggiotoa bacteria start coating the bones at this stage. The huge cells line up in long filaments, and so researchers don't need microscopes to see the pale bacterial mat. "It looked like it had snowed," says Baco-Taylor.

Worm specialist Adrian Glover of the Natural History Museum in London also evokes the snow image. Among notable species that he's seen on whale falls are segmented worms (Bathykurile guaymasensis) that leave trails as they eat their way through the snowlike bacterial mat. Glover calls them snowboarding worms.

Many other segmented worms, called polychaetes, also show up at second-stage whale falls. "They're related to earthworms but are much more diverse and in many ways are much more interesting," says Glover.

Many of the animals that appear during the second stage are exclusive to whale falls, the researchers suspect. They've found several polychaetes and a snail, for example, in great numbers on whales but in no other habitat. For example, what Smith calls bone-eating zombie worms, in the genus Osedax, were first described in the July 30, 2004 Science. They get their nutrition by sending into the bone a tangle of green, rootlike coils containing rod-shaped bacteria that break down the skeleton's complex organic compounds (SN: 7/31/04,p. 68).

Since then, at least five more whale-dwelling zombie worm species have turned up, including one from Swedish waters, Smith said in February in Washington, D.C., at the annual meeting of the American Association for the Advancement of Science. He says that he expects scientists to find zombie worms in whale-fall communities in many parts of the world.

A LATER WHALE When the hordes of little creatures have nibbled the whale fall down to bones, a third successional stage begins. The bacterial mats remain, and life around the whale takes on its strongest resemblance to that at a deep-ocean vent. This stage has so far been observed only in the natural whale falls.

Baco-Taylor calls it the chemoautotrophic phase. Many of the larger animals that are present depend on chemoautotrophs, microbes that get energy directly from such compounds as the sulfides that swirl from hot-water vents and deteriorating whale bones.

This is the era of the vesicomyid clams that intrigued Smith at the first whale fall his team discovered. There are also other mollusks that carry sulfide-metabolizing bacteria. For example, more than 10,000 mussels of the species Idas washingtonia can amass on the remains of a single whale.

A newly discovered species of the polychaete genus Vigtorniella also forms dense colonies "like lawns of orange grass around the whale skeleton," says Smith. Researchers described the worms in the December 2004 Deep-Sea Research.

Baco-Taylor calls the fourth and final fate of a sunken whale "the reef stage." The multitudes of creatures have at last exhausted the nutritional bonanza, and the makeup of the community shifts to undersea animals that thrive on craggy structures. At this point, she says, "the bones are acting like a rock."

So far, researchers haven't figured out how long a skeleton takes to become rocky, nutrientfree rubble. They've dated some of the natural whale falls to 70 to 80 years old, but these still bristle with chemoautotrophs.

WHALE MATTERS Of course, other food windfalls drift to the ocean bottom. As Thomas Dahlgren of Goteborg University in Sweden puts it, "There are shark falls, squid falls, and fish falls. There are wood falls."

Sunken whales are special, though, says Smith, because they're big and rich in oily bones, and they last for decades. He says that a whale settling to the depths deposits as much food there as would be delivered by the regular rain of detritus in 2,000 years.

Smith contends that whales make such a reliable food source that some species have evolved to specialize in them. So far, he lists 27 species that researchers have collected from whale skeletons but not from other undersea habitats. Several more species grow riotously on whales but hardly appear anywhere else.

But whale sites matter to many animals that live elsewhere, such as at hydrothermal vents, Smith suggests. There's a lot of ocean out there, with big gaps between friendly habitats. Whale falls may offer stepping-stones or alternative habitats for vent species that stray from home.

Or at least that's the way deep-sea habitats may have worked for millennia. "It doesn't take a rocket scientist, or a benthic oceanographer, to figure out that the reduction of live whale falls will reduce the abundance of habitat" for creatures that feast on whales, Smith says.

A genetic analysis recently suggested that over the past 150 years or so, the North Atlantic has lost 75 percent of its whale population to the commercial catch. Smith has used various mathematical models to work out the consequences. One of the simpler approaches predicts that such a loss of whales will wipe out 30 to 40 percent of the whale-fall species.

Smith proposes a way to test for losses of whale-fall biodiversity. The world's oceans have had very different histories of whaling, and Smith proposes sinking bones in various locales and then comparing the diversity of the communities that arise.

Baco-Taylor and Smith are now also pushing the study of sunken worlds into new dimensions. To see how well communities are tailored to a whale fall or other sunken bonanzas, the researchers went to Home Depot. They purchased two-by-fours of untreated wood, made up standardized bundles, and sank them off the California coast. She also sent down some batches of kelp. Like whale carcasses, both wood and kelp invite colonizers.

"So far," says Smith, "I'm surprised at how different they [all] are."