A Whale of a Tale
by Robin Meadows

Life can be found in the most extreme environments, from hot springs to frigid glaciers to salt crystals. One of the strangest forms of life was recently found on a whale carcass in the deep sea. On a routine survey of a marine canyon off California, scientists discovered two closely related species of tubeworms that live only on whale bones at the bottom of the ocean. These worms have a unique way of feeding: They grow "roots" into the bones, and these roots contain bacteria that break down the oils in the bone marrow and so provide the worms with nutrients. Bone-eating worms are the first kind of animal known to have symbiotic bacteria that live on oils. They also have a unique way of developing: Only the females grow roots into bones, while the males resemble larvae all their lives and are essentially tiny sperm-producing machines that live inside the females' tubes.

Osedax frankpressi
A female Osedax frankpressi whale worm. (Greg Rouse)

"Everything we looked at was a surprise," says Robert Vrijenhoek of the Monterey Bay Aquarium Research Institute (MBARI) in Moss Landing, California, who led the team that found the bone-eating worms in 2002. "Every time we find something new like this, it opens a window on what forms of life are possible," he adds, noting that the idea of life on other planets was made far more plausible by the 1977 discovery of life at deep-sea hydrothermal vents. These hot-spring habitats are crowded with tubeworms and other extreme forms of life that get their energy from sulfides rather than sunlight.

Whale carcasses that sink to the bottoms of oceans around the world are another source of concentrated nutrients in the otherwise nutrient-poor deep sea. Like hydrothermal vents, these "whale falls" are almost completely covered with tens of thousands of living creatures. Besides being fascinating in their own right, whale falls may help explain mysteries of deep-sea ecology and evolution, such as how some animals reached remote hydrothermal vents in the first place. Learning more about the deep-sea floor is critical to protecting its remarkable biodiversity, which may be comparable to that of tropical rainforests.

Deep-sea Basics
The deep sea starts at about 3,300 feet below sea level and goes all the way down to about 36,000 feet at its deepest point, the Mariana Trench, in the Pacific Ocean near Guam. The depth of the Mariana Trench is greater than the height of Mount Everest, which is the tallest mountain in the world at 29,035 feet above sea level.

In addition to being remote, the deep sea is vast. "It's the largest habitat on Earth and may harbor a substantial part of [the Earth's] biodiversity," says whale-fall expert Craig Smith of the University of Hawaii. The deep-sea floor alone covers about 60 percent of the Earth's surface and about 116 million square miles, making it one of the most extensive ecosystems in the world. Its sheer size and inaccessibility also make it one of the least-known ecosystems.

But what we do know makes us want to learn more. One of the biggest mysteries is why so many species inhabit the deep sea. "By some estimates, there may be as many as ten million animal species in deep-sea sediments, rivaling the diversity of tropical rainforests," says Smith. Intuitively, it seems that the opposite would be true. The deep-sea floor is a tough place to live—it's completely dark, is under enormous pressure, and for the most part, is near freezing and contains few nutrients. Even so, there are thought to be many more bottom-dwelling species in the deep sea than in shallower waters.

While biodiversity is high on the deep-sea floor, animals there are typically much smaller and less abundant than those in shallower waters. This is not surprising because animals in most of the deep sea live on "marine snow": plankton and other organic debris that fall from surface waters to the bottom of the ocean.

There are exceptions, however. Some deep-sea floor habitats are crammed with animals that may be gigantic compared to their shallow-water relatives. The most famous of these habitats are the hydrothermal vents on submarine mountain ridges, which are packed with foot-long clams, nine-foot-long tubeworms with red plumes, and other fantastical creatures.

The reason there is so much life at hydrothermal vents is that they spew out sulfides and other energy-rich minerals. Most ecosystems are based on photosynthesis: Plants, algae, and some bacteria use the energy in sunlight to turn carbon dioxide into the organic compounds that form the basis of most known life. However, hydrothermal vent ecosystems are based on chemosynthesis: Bacteria use the energy in sulfides and other minerals to make organic compounds. Some of these bacteria live in seawater and form dense mats, while others live symbiotically within the tissues of animals and provide their hosts with food. Giant tubeworms, for example, have no mouths or guts, but instead have a large organ full of symbiotic bacteria that produce nutrients for them. Similarly, the gills of hydrothermal vent clams and mussels are also full of symbiotic bacteria.

Whale-fall Basics
Whale carcasses are another deep-sea habitat that is crammed with life. Whale falls can provide as much organic material as a thousand years of marine snow, and a single skeleton can support more than 40,000 individual animals including shellfish, amphipods, and worms.

In 1987, a decade after hydrothermal vents were first discovered off the Galapagos Islands, biologists learned that whale falls also support animals that get their food from symbiotic bacteria. Led by the University of Hawaii's Smith, a team of scientists made this discovery on a blue whale (Balaenoptera musculus) skeleton they found at about 4,000 feet deep in the Santa Catalina Basin off the coast of southern California. The scientists found the bones were covered with clams and mussels containing symbiotic bacteria that live on sulfides. While the sulfides at hydrothermal vents are in the water that spews from beneath the sea floor, the sulfides at whale falls are produced by bacteria that decompose oils inside whale bones.

A whale fall in the deep sea
MBARI scientists found this whale fall in Monterey Canyon near California. Osedax worms and sea cucumbers live on it. (MBARI)

Animals with symbiotic bacteria have inhabited whale falls for ages. In the Pacific Ocean, 30-million-year-old whale fossils have been found with mussels attached to their bones, and these mussels presumably had symbiotic bacteria because all of their close relatives do today. Intriguingly, animals with symbiotic bacteria may also have lived on skeletons in the deep sea well before the time of whales, which first appeared about 40 million years ago. Mollusk fossils have been found near 200-million-year-old fossils of large marine reptiles, including ichthyosaurs and plesiosaurs.

Whale skeletons support so much life in the deep sea because they contain an enormous amount of oil. Large whale bones can be more than 60 percent oil by weight, and the skeleton of a 90-ton whale, for example, is estimated to contain five tons of oil. Depending on the size of the whale, its bones can contain enough oil to support sulfur-loving species for as long as 80 years.

So far, 407 species have been found on whale falls. But there are probably a lot more, because most of what we know about whale falls comes from only 20-odd specimens—either skeletons found by chance on the sea floor, or skulls and other parts that were trawled up from the depths. In addition, while whale falls have been found scattered around the world, most of those that have been studied are in California waters. Just as the species at hydrothermal vents vary in different parts of the world, Smith expects that whale fall species will vary around the world. In keeping with his expectation, museum specimens of animals found on whale bones off New Zealand are different from those found on whale bones off California.

The fact that so many whale-fall species are known from so few specimens suggests that whale falls have more species than hydrothermal vents. While vents have more known species right now—600 worldwide—they have also been more intensively studied than whale falls. As we learn more about whale falls, the numbers of known species at whale falls could surpass those at hydrothermal vents.

Likewise, the number of species unique to whale falls is likely to rise above the 30 that are known today. The existence of these whale-fall specialists raises an interesting question: Because whale skeletons are isolated habitats that support life for a limited time, how do the species that depend on them get from one whale fall to another?

Smith thinks that whale falls are close enough together to form habitat "archipelagos." Whale carcasses are likely to be concentrated along migration routes and in feeding and calving grounds, which means they are probably close enough together for marine larvae to traverse them. For example, Smith estimates that the deep-sea carcasses of gray whales (Eschrichtius robustus) off the west coast of North America are roughly four to ten miles apart, which is well within range of marine larvae dispersal. Even greater distances could also be within their range: Some marine larvae can survive as long as nine months and so may be able to disperse more than 500 miles.

The existence of species that are unique to whale falls raises another question: How did commercial whaling affect them? Massive commercial whaling began in the 1800s and continued into the 1900s. Despite the 1982 International Whaling Commission's moratorium on commercial whaling, today many whale populations are estimated to be at only ten to 25 percent of their historical levels. Fewer whales means fewer whale falls, which in turn means less habitat for whale-fall species. Habitat loss can make species more vulnerable to dying out, and Smith believes that intensive commercial whaling has already driven some whale-fall specialists to extinction. "It's likely that the first extinctions were due to the onset of whaling," says Smith, adding that "extinctions of whale fall specialists are probably ongoing."

Extreme Forms of Life
Learning more about species unique to whale falls may also teach us more about the extremes of life, which increases our understanding of the range and limits of life on Earth—and possibly on other planets. The bone-eating worms that live on deep-sea whale skeletons are a prime example.

Named Osedax, which is Latin for "bone-eater," these worms were found by a team of MBARI scientists on a gray whale carcass at a depth of nearly 9,500 feet, in the waters of Monterey Canyon off California. The whale bones were covered with short tubeworms that turned out to be two new species: Osedax rubiplumus, which is up to two-and-a-half inches long and has red plumes, and Osedax frankpressi, which is up to an inch long and has red plumes with white stripes. The plumes are thought to act as gills, and neither species has eyes.

Albeit on a much smaller scale, bone-eating worms resemble the giant tubeworms at hydrothermal vents, and it turns out they are related. Both types of worms are members of the family Siboglinidae, and they lack mouths and guts and depend on symbiotic bacteria for nourishment. Here the similarities end, however. Vent tubeworms have a large internal organ called a trophosome that is full of bacteria that live on sulfides. In contrast, MBARI researcher Shana Goffredi found that bone-eating worms have a large external organ full of bacteria that live on oils. This organ grows "roots" into whale bones, so the bacteria can feed on oils in the bone marrow and in turn supply nutrients to their worm hosts.

Unlike vent tubeworms, bone-eating worms all appear to be female at first glance. However, when worm specialist Greg Rouse of the South Australia Museum took a closer look at the new worms through a microscope, he saw that there were dwarf males inside the females' tubes. Large females can have more than 100 males attached to their bodies with tiny hooks.

Females with attached males are nothing new in the deep sea. A famous example is the female angler fish—in this species, dwarf parasitic males bite females and hold on, eventually fusing with their mates' bodies. Bone-eating worms go to an even further extreme than angler fish in the game of attachment. "The males are essentially embryos with sperm," says Vrijenhoek. "They're pushing sexual maturity as far back as possible."

Clump of O. frankpressi
A clump of whale worms on a bone. (MBARI)

In hopes of learning more about how bone-eating worms reproduce and develop, Vrijenhoek and his team sank a beached 56-foot blue whale in nearly 3,000-foot-deep water in October 2004. The scientists are waiting to see if bone-eating worms will also colonize a whale fall in shallower water, where they would be easier and cheaper to study. This approach has worked before—worms in the same family have been found on whale carcasses that Smith sank in relatively shallow waters off California and Sweden.

The MBARI team is full of questions about the bone-eating worms. For example, do larvae that settle on bones become females, while larvae that land on female worm become males? There is a precedent for this. Sex is environmentally determined in some other marine worms, and crowding usually leads to males. Alternatively, it is possible that males are the sons of the females they are attached to. "Anything goes here, we just don't know what to expect," says Vrijenhoek.

The scientists do know that the bone-eating worms are very successful. Analyses of their genetic variation indicate that, depending on the species, between 500,000 and a million female bone-eating worms contributed to the pool of larvae that colonized the Monterey whale fall. This is similar to population estimates for other deep-sea worms, suggesting that whale-fall habitats may be more abundant than previously believed, says Vrijenhoek.

Clues to Deep-sea Ecology and Evolution
Whale-fall species not only offer insights into the extremes of life—they are also helping scientists learn more about the ecology and evolution of life in the deep sea. For example, some species may use whale falls as ecological "stepping stones" to reach hydrothermal vents. The University of Hawaii's Smith and his colleagues have so far found that there are 11 species known to live at both whale falls and vents.

Some species may also use whale falls as ecological stepping stones to get from one vent system to another. This could explain why vents in different areas of the world have some species in common. Notably, there is an overlap of about ten species at the vents on the Juan de Fuca Ridge off Washington and British Columbia, and those in the East Pacific Rise off Baja California, Mexico. These vent systems are about 1,500 miles apart but could be connected by the carcasses of gray whales, which migrate from their winter feeding grounds in the Bering Sea to their summer breeding grounds in the Gulf of Mexico. In support of this theory, at least one of the species that lives at both of these vent systems (a clam) also lives on whale falls. Scientists may find other such examples as they study more whale falls around the world.

Similarly, some species may have used whale falls as evolutionary stepping stones from shallow waters to hydrothermal vents. This makes sense, because whale falls lie at intermediate depths between these two habitats. This theory could also explain why a species of mussel that is related to mussels in salt marshes and other shallow waters also lives near some vents: Smith and his colleagues found that whale falls have a mussel that is intermediate between the species at the other two habitats. DNA analyses suggest that the deep-sea mussel split from the shallow-water mussel roughly 30 million years ago, about the time that large whales evolved.

Why We Need to Understand the Deep Sea
Any insights that whale falls can give us into the deep sea are important because we know so little about this ecosystem. And understanding the deep sea is critical because, although remote, it is still intimately connected to the rest of the world. "It's the biggest sink for carbon dioxide, and understanding the global carbon balance is important for figuring out what to do about climate change," says Vrijenhoek. Carbon dioxide is the major "greenhouse gas" produced by people, and is linked to global warming.

Carbon dioxide is absorbed by the oceans' surface waters, where it is then taken up by photosynthetic plankton. Some people suggest we take advantage of this process to reduce global warming. The idea is to fertilize the plankton with iron, thereby increasing the plankton and so decreasing the atmospheric carbon dioxide. However, this plan could also decrease the amount of oxygen in the deep sea, which would cause problems. "If iron fertilization was on a large enough scale to decrease the carbon dioxide, it would probably create major anoxic [oxygen-deficient] areas where virtually all the deep-sea animals would die," says Smith.

If the deep sea became too oxygen-depleted, it might not be able to provide one of its key ecosystem services: nutrient recycling. Over the course of centuries to thousands of years, nutrients that fall into the deep sea as marine snow and other organic debris are recycled back to the surface. Animals and bacteria that live in deep-sea sediments return these nutrients to the sea water, and the cycle begins anew. This process yields upwellings rich in nitrogen, phosphorus, and other nutrients that support algae growing in the ocean's surface.

In contrast, the fate of carbon that falls to the deep sea floor is largely a mystery. "We don't know how much of it comes back up," says Vrijenhoek. Carbon does get spread around by animals in the deep sea, partly facilitated by whale falls, and he speculates that bone-eating worms and other abundant deep-sea species may play a significant role in the global carbon cycle.

Whale falls are likely to keep surprising and delighting us with new species like bone-eating worms, and increasing our understanding of the connections within the deep sea and maybe even between the deep sea and the rest of the world. These extraordinary habitats at the bottom of the ocean also remind us that there's still a lot we don't know about what goes on down there. And while the deep sea is vast enough that it can probably take a lot of use or even abuse, we still need to be careful about what we do to it. The deep sea is one case where out of sight should not mean out of mind.

—Robin Meadows is a contributing editor of ZooGoer. She wrote about California's island fox in the July/August 2004 issue of the magazine.

link toSidebar—Vent Crabs: Shallow Opportunists

ZooGoer 34(2) 2005. Copyright 2005 Friends of the National Zoo.
All rights reserved.



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