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Science  06 Feb 1998:
Vol. 279, Issue 5352, pp. 803

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    Pushing Back the Origins of Animals

    1. Richard A. Kerr


    The origins of the tremendous diversity of animals alive today—from sponges, tapeworms, snails, and spiders to sharks, bullfrogs, and humans—are hidden in the mists of time. If the fossil record is to be believed, these and other phyla—in fact, all the basic types of multicellular animals known today—burst on the scene in an evolutionary frenzy called the Cambrian explosion about 540 million years ago. Even paleontologists knew that that can't be the full story, however, for the Cambrian animals presumably had predecessors. But older rocks held few, if any, familiar-looking animals, and many researchers had lately resigned themselves to never finding any fossils of these small, squishy ancestors.

    Not for the bathtub.

    This submillimeter sponge with needlelike spicules is 570 million years old.

    LI ET AL.

    That left the question of when complex animal life arose and what it looked like to biologists, who in a flurry of recent work have been using the genes and embryos of living organisms to peer into the distant past (Science, 4 July 1997, p. 34). But with a pair of new findings, paleontologists have reentered the game. Their findings reveal a fossil history of animals stretching back tens of millions of years before the Cambrian explosion, opening up the dawn of animals to paleontological exploration.

    In this issue of Science (p. 879) and in this week's Nature, two groups report that they have found microscopic fossils of animals and embryos exquisitely preserved in 570-million-year-old phosphorite rocks in south-central China. The new finds include submillimeter-sized marine sponges—the oldest known representatives of a living group of organisms—as well as ancient embryos that represent more advanced, bilateral animals. By showing that phosphate can fossilize tiny, fragile organisms from such ancient times, the finds have “really opened up a new way of looking for an older record of animals,” says paleontologist Andrew Knoll of Harvard University, one of the discoverers. “As paleontologists, we don't have to just sit in our armchairs and watch the debate.”

    These first glimpses of that record suggest that the ancestors of today's kinds of animals were diverse and abundant well before the Cambrian explosion. The complexity of the fossils suggests that they must themselves have had even earlier, unknown ancestors and implies that the conservative dates once favored by some paleontologists for the origin of multicellular life—less than 600 million years ago—are too recent. The discoveries even raise hopes that fossils may one day help the molecular evolutionists settle their disputes about the dates of the first animals, which one camp now puts at a whopping 1.2 billion years ago and another at 670 million years.

    Both new reports of early animals spring from the same source—a mine bored into the Doushantuo formation in central Guizhou province for its phosphate-rich rock used as fertilizer. Dated by correlation with deposits of known age to about 570 million years, give or take 20 million years, the Doushantuo had yielded remarkably well-preserved algae, according to published reports, but no animals. Last year, however, paleontologists Stefan Bengtson, of the Swedish Museum of Natural History in Stockholm, and Yue Zhao, of the Chinese Academy of Geological Sciences in Beijing, reported finding microscopic embryos in 530-million-year-old phosphate-rich rocks from China and Siberia (Science, 12 September 1997, p. 1645). That suggested that even older phosphate deposits might yield submillimeter-sized animals and embryos.

    With that in mind, both groups independently realized that some of the “algae” from Doushantuo were actually animals and embryos. As they report in this issue, the team of cell biologists Chia-Wei Li and Tzu-En Hua of the National Tsing Hua University in Taiwan, and paleontologist Jun-Yuan Chen of the Nanjing Institute of Geology and Palaeontology in Nanjing, China, examined 150- to 750-micrometer spheroids and recognized sponges, among the most primitive of living multicellular animals. “I usually regard myself as a skeptic,” says Bengtson, but he finds the sponge argument “very convincing.” Not only are there abundant spicules—a sponge's siliceous, needlelike structural elements—but some spicules are still attached to the fossilized cells that produced them. These are the oldest known representatives of a living phylum, says Li, whose group also reports identifying sponge embryos and—tantalizingly—“many different metazoan taxa other than sponges.”

    The other group, consisting of paleontologists Shuhai Xiao of Harvard, Yun Zhang of Beijing University, and Knoll, also reports a range of microscopic embryos in the Nature paper. Bengtson finds their interpretation of these roughly 500-micrometer spheroidal bodies as embryos containing one, two, four, eight, and more cells “very reasonable,” because the fossils are the same size no matter how many cells they contain. That's just the way early-stage embryos behave as their constant volume is divided and redivided; in contrast, algal cells tend to be similar in size, so the girth of a clump of algae would depend on the number of cells in the cluster. The team reports that in four-cell embryos, the cells are arranged in a strict tetrahedron—a hallmark of animals that have bilateral symmetry and are therefore much more advanced than sponges.

    Paleontologists had hardly dared hope to find embryos in the fossil record, as that requires exquisite preservation of soft tissue. These Doushantuo fossils “yet again show the potential of phosphatization as a means of preserving incredible detail,” says paleontologist Simon Conway Morris of Cambridge University. Just how phosphate manages to freeze even the tiniest details of soft tissues is unclear, says Knoll. When the Doushantuo formed, large amounts of dissolved phosphate were apparently delivered to a shallow sea floor covered by low-oxygen waters, a place where small creatures could be preserved within days of their deaths. Similar conditions have prevailed in a range of times and places throughout the geologic record, and that is raising hopes that this glimpse of Precambrian animals will soon turn into a panorama. “Both the Nature and Science papers show we can map out early animal evolution,” says Bengtson. “There are other phosphorites that we should go back to and look at with our new eyes. It's a new world waiting.”

    “The big question,” says Conway Morris, “is how much farther back this will go.” It might go quite a ways. Developmental biologist Eric Davidson of the California Institute of Technology in Pasadena and his colleagues have suggested that life might have spent many tens, even hundreds, of millions of years as tiny, simple assemblages of cells—“squishy little larvalike things”—that were more sophisticated than sponges but were prevented from evolving into the larger forms preserved at the Cambrian explosion by a developmental barrier (Science, 24 November 1995, p. 1300). Davidson's team suggested that paleontologists would therefore miss all the early action, but the new fossils raise the possibility that such tiny life-forms may be in the record after all, says Knoll. Davidson agrees that this is the most direct fossil evidence yet for an extended history for his larvalike animals.

    Meanwhile, other biologists have also been theorizing about the origins of animals, and some have been pushing for very early dates for these life-forms. In 1996, for example, molecular evolutionist Gregory Wray and colleagues at the State University of New York, Stony Brook, analyzed the sequences and evolution of eight genes across the living animal phyla (Science, 25 October 1996, p. 568). Assuming that mutation rates were constant, they used the amount of gene-sequence difference among various organisms to calculate how long ago the groups split. They concluded that a deep division among these animals—between the mollusks, annelid worms, and arthropods (called the protostomes) on one hand and the echinoderms and chordates (called the deuterostomes) on the other—happened a whopping 1.2 billion years ago. The split between bilaterally symmetric animals (like people) and radially symmetric ones (like jellyfish) would have been even earlier.

    But other molecular evolutionists aren't convinced. In the 25 January issue of the Proceedings of the National Academy of Sciences, Francisco Ayala of Pennsylvania State University (PSU) in University Park, statistical analyst Andrey Rzhetsky of Columbia University, and Ayala's father—evolutionary biologist Francisco José Ayala of the University of California, Irvine—reanalyze the gene data used by Wray and his colleagues. They use rates for 12 additional genes and throw out data from genes whose rates of evolution appeared to change over time. Their result: The protostome/deuterostome split occurred 670 million years ago, give or take 60 million years (see diagram).

    Looking back.

    The latest molecular study dates a key branch point in the tree of life to about 670 million years ago.


    That's at least drawing closer to dates from the fossil record, says evolutionary biologist Charles Marshall of the University of California, Los Angeles. “Seven hundred million years is a pretty long way out” for life to have existed without leaving a trace, he says. “But [at least] it's not a billion.” The numbers from genetic studies may eventually converge, for more studies from more genes are on the way. But for now, their estimates for the protostome/deuterostome split range from 670 million to 1500 million years, according to a limited survey by Science. As molecular evolutionist Xun Gu of PSU notes, with some understatement, “This problem needs more data.”

    The new paleontological findings show that the additional data won't be coming from genes alone. Knoll predicts that “over the next few years, you are going to see people finding comparable fossils in yet older rocks.” And finding whole animals—perhaps even the common ancestor of vertebrates and invertebrates at the root of the animal family tree—is a real possibility. Paleontologists may be able to test some of biologists' ideas on what the ancestral animal looked like, says Doug Erwin of the National Museum of Natural History in Washington, D.C., and “that's pretty exciting.”


    Proving a Link Between Logic and Origami

    1. Barry Cipra

    Baltimore—If you have ever tried to fold an origami boat or swan, you know it's not as easy as the step-by-step instructions suggest. But try doing it with just an unfolded square of paper and nothing but the crease lines. Even the most dedicated amateur origamist might give up in frustration when faced with the challenge of making the folds in the proper order. Predicting the properties of the finished origami model is still more daunting: It involves solving a problem that's as hard as anything known to computer scientists.

    A pair of computer scientists has now shown that a well-known origami problem called the flat-folding problem belongs to a class of tasks that mathematicians call NP-complete: problems so difficult that each contains the key to solving—or being unable to solve—all the rest. (The initials “NP” stand for “nondeterministic polynomial time,” which is computer science jargon for “may take an awfully long time unless you make a lucky guess.”) The problem, predicting whether an origami model can be folded flat between the pages of a book without creating any new creases or otherwise damaging the model, has long tantalized the small community that studies the mathematics underlying origami. Now Barry Hayes, a computer scientist at the Mountain View, California, software firm Placeware Inc., and Marshall Bern of Xerox's Palo Alto Research Center have shown that this question is equivalent to a famous “hard” problem in computer science known as not-all-true 3-SAT.

    The proof, which Hayes presented at a meeting here* in a session devoted to mathematical aspects of origami, is “a capstone of the type of research that has been emerging in origami mathematics,” says Thomas Hull, a mathematician at Merrimack College in Andover, Massachusetts, who organized the session. Even though Hayes and Bern's proof is of purely theoretical interest, Hull says he is “delighted by the result,” because the glimpse of a connection between paper sculpture and a much-studied problem in computer science may help bring other researchers into the fold.

    The computer-science problem, not-all-true 3-SAT, involves determining whether a given logical expression, created by stringing together simple, three-term clauses, can be satisfied. “Satisfied” means, in this case, that the expression can be made true by assigning each term—which may appear in multiple clauses—a single value, True or False, throughout the expression. The constraint, as the “not-all-true” sobriquet suggests, is that you're not allowed to assign the value True to all three variables in any clause. For example, the two-clause expression “(A or B or C) and (A or C or D)” can be satisfied under the constraint by letting A, B, and D be true and C be false.

    Simple though this example sounds, longer examples, where the same term occurs many times in different contexts, are much harder to satisfy. It's easy to show that a given example is satisfiable if you happen to know the proper True/False values, but there seems to be no way to find a solution short of trying all possible combinations. That's what makes the 3-SAT problem NP-complete. “Complete,” in this context, means that every other NP problem, from factoring products of large primes to the famous Traveling Salesman problem, can be translated into a not-all-true 3-SAT problem.

    By translating 3-SAT expressions into crease patterns, Hayes and Bern were able to prove that flat-folding, too, is NP-complete. The key ingredient in their proof is a crease pattern consisting of an equilateral triangle with strips radiating from its three sides—a pattern well known to origamists as a “triangle twist.” The triangle twist can't be folded into a flat sheet of paper if all three strips are creased in the same way—for example, with an upward fold (what origamists call a mountain fold) on the left and a downward fold (a valley fold) on the right of each one as it enters the triangle. It is flat-foldable only if one strip is folded in the opposite way (see figure). This folding constraint suggests that the triangle twist can stand for one clause in a not-all-true 3-SAT expression. The strips represent the three variables participating in the clause, and the True/False value carried by each variable depends on which side of the strip is mountain- or valley-folded as it enters the triangle.

    How to fold a proof.

    In a folding pattern that mirrors a logic problem called not-all-true 3-SAT, the lines indicate strips formed by an upward and a downward fold; the up-fold is always on the right in the direction of the arrow. The strips converge in two “triangle twists” that correspond to clauses in which only two of the three variables carry the same true or false value.

    The key to showing that origami folding is the equivalent of a 3-SAT problem is to fold a bunch of these triangle twists, each one representing a clause, connected by strip-folds that carry variables from triangle to triangle. Hayes and Bern showed that the entire pattern can be folded flat only if the strips carry the same “value” each time they enter a triangle. The pattern, then, is flat-foldable only if the 3-SAT expression is satisfiable.

    The proof means that if origami experts could find an efficient way to answer their flat-folding question, the result would apply across the board to a vast range of computational problems, including those whose difficulty provides the security for modern cryptographic systems. But origami enthusiasts are no more likely to solve the flat-folding problem than computer scientists are to solve such NP-hard chestnuts as the Traveling Salesman problem. Says Hayes: “This has no practical applications to [either] origami or computer science; I will be really surprised if one turns up.”

    Still, Hull is confident that origami will soon be producing something more than beautiful models for problems in other fields. “There are lots of places where you see things being folded up in nature,” from insect wings and flower buds to the crumpled aftermath of a car crash, he says. Using paper to study what nature does with a range of materials, Hull thinks, “might be the next revolution in origami.”

    • * Annual meetings of the American Mathematical Society and the Mathematical Association of America, 7–10 January.


    Algorigami, Anyone?

    1. Barry Cipra

    Predicting whether any given origami design can be flat-folded—pressed flat between the pages of a book without damage—is about as hard as a problem can get (see main text). It's easier to start with the flat-foldable criterion and create designs that meet it, as Robert Lang, a physicist at SDL Inc. in San Jose, California, and a renowned origami expert, has shown. At the mathematics meetings, he described a way to create arbitrarily complex patterns that are easy to fold flat. More important—at least to origamists—the method also provides a way to sculpt in paper essentially any object whose general shape can be suggested by a stick figure.

    By the numbers.

    An origami sculpture folded with the help of a new algorithm.


    The stick figure specifies the numbers and lengths of various body parts—six legs for an insect, say, plus mandibles if it's a beetle. These in turn constrain how close together various vertices can be in the crease pattern. Within those constraints, Lang's algorithm works out a crease pattern that puts flesh—the flat-foldable kind—on this framework. The basic shape can then be decorated using familiar origami techniques to produce details such as feet and joints.

    The algorithm also aims at producing the largest possible sculpture from a given square of paper. Lang notes that this challenge is closely related to what mathematicians call the circle-packing problem: determining how large a square you need to enclose N nonoverlapping circles of radius 1. In the origami context, it's only necessary to enclose the centers of the circles, which correspond to the tips of the stick figure's extremities and thus can lie at the edge of the paper. Lang's algorithm can tell you, for example, that a three-pointed star with 1-centimeter spokes can be folded from a square with sides approximately 1.93 centimeters in length.

    But for more complex shapes, there's no guarantee that the algorithm will make the most efficient use of paper. The circle-packing problem, like other mathematics related to origami, is a longtime puzzler. The state of the art, Lang notes, is such that no one knows how small a square can be used for stars with more than 20 points.


    A Deep Root for Iceland?

    1. Richard A. Kerr

    The island of Iceland, where fiery lava erupts to melt glacial ice, is perched atop a mantle plume—a column of hot rock rising slowly from Earth's interior. Similar plumes feed long-lived volcanic centers around the globe, such as Hawaii and the Galápagos. For decades, researchers have debated whether these plumes rise from the bottom of Earth's lower mantle, 2900 kilometers down, or are rooted only a few hundred kilometers down in the upper mantle (Science, 23 May 1997, p. 1198). The answer would determine whether the bulk of Earth's rocky mass is forever sealed off in the lower mantle or can mix into the upper mantle and so shape the surface. Now seismologists tracing the origin of Iceland's fires present the strongest support yet for deep plumes.

    By studying earthquake waves that probed the mantle deep below Iceland, seismologist Yang Shen of the Woods Hole Oceanographic Institution in Massachusetts and his colleagues detected signs of a narrow, hot plume at the traditional boundary between upper and lower mantle, about 660 kilometers down. “I think it's pretty strong,” geophysicist Donald Forsyth of Brown University says of the evidence, which Shen and his colleagues reported at the annual fall meeting of the American Geophysical Union in December. “It indicates [that] something with higher temperatures continues down to the lower mantle; I don't know any way to get around it with an upper mantle source” for the Iceland volcanic hot spot.

    Seismic waves slow down as they pass through hot rock. By plotting wave speeds from distant earthquakes, seismologists had already created CT scan-like images of at least a shallow plume beneath Iceland. In these so-called tomographic images, a column of hot rock—perhaps a couple of hundred degrees hotter than its surroundings—extends from just beneath Iceland to about 400 kilometers down. It shows no sign of petering out with depth, but the tomographic image fades at that point because it depends on the paths of many seismic waves crossing within the plume. Seismic stations on Iceland itself can't see wave paths cross much below 400 kilometers, and distant stations have trouble resolving a narrow plume.

    To get around this problem, Shen and his colleagues didn't image the plume itself but instead measured its effect on the depth of the upper mantle-lower mantle boundary. At the boundary, the crystal structure of a key mineral changes to the denser phase found in the lower mantle; when the temperature is unusually high, the transition happens at shallower depths. To gauge the boundary's depth, Shen used two kinds of waves: acoustic-like compressional seismic waves created by distant earthquakes, and shear waves, side-to-side vibrations touched off when compressional waves hit the boundary. Both kinds leave the boundary together, but they have different velocities, so the difference in their arrival times at the surface can be used as a measure of the precise distance to the boundary.

    Combining 1500 pairs of waves, Shen found that the transition is 20 kilometers shallower than normal across a 300-kilometer region beneath Iceland. “I think it's convincing evidence for a plume from the lower mantle,” says Shen. A narrow column of rock about 125 degrees Celsius hotter than its surroundings would have just this effect, he says. But the broad, flat base of a plume originating just above the boundary would affect the transition depth over a much wider area. “It's a big step in the direction” of proving a lower mantle origin, acknowledges seismologist Richard Allen of Yale University, but, he adds, “I don't know if I'm thoroughly convinced.”

    Allen and others would still like to see some sort of seismic indication of the plume in the 2200 kilometers of mantle below the mineralogical transition. Skeptics say that this transition may not truly mark the upper mantle boundary, which some have pushed closer to 1000 kilometers. A prime target for more seismic probing may be the zone of partially molten (and therefore more easily imaged) rock recently identified at the base of the mantle below Iceland (Science, 31 January 1997, p. 614). This could be the ultimate source of Iceland's fires.


    That Winking, Blinking Sun

    1. Andrew Watson
    1. Andrew Watson is a science writer in Norwich, U.K.

    New observations from the Solar and Heliospheric Observatory (SOHO) satellite show that the sun is covered in tiny hot spots. These short-lived bursts of energy could shed light on a big puzzle in solar science: What heats the sun's atmosphere to fantastically high temperatures and powers the stream of charged particles that flows into space as the solar wind?

    Solar physicist Richard Harrison of the Rutherford Appleton Laboratory, near Oxford, U.K., discovered these so-called blinkers while studying the surface of the sun in extreme ultraviolet light. Viewed in the ultraviolet, the sun looks dimpled like an orange. The pattern results from the convection of hot, ionized gases, which well up, cool, and sink back below the surface. As the charged particles in the gases move, they generate magnetic fields, which also influence their motion. As Harrison watched these features, he spotted something unusual.

    All over the sun, spots about the size of Earth briefly flare to temperatures of up to a million degrees Celsius, far above the average solar surface temperature of about 5500 degrees. Because the blinkers are concentrated at the fringes of the convecting gas patches, Harrison believes that the magnetic field lines squeeze and heat the gas. The spots “seem to be occurring because these magnetic fields are getting rammed into one another,” he says.

    At any moment, about 3000 blinkers dot the sun. “This work is very exciting because it can help us to understand the heating mechanism for the solar atmosphere,” says Helen Mason of Cambridge University. It's not clear, though, whether the blinkers pack enough punch to heat the entire atmosphere to million-degree temperatures. “The energy we see at the moment is insufficient,” Harrison admits. However, visible blinkers might represent only a part of the total energy converted from tortured magnetic fields into heat, he argues.


    Coral Reefs Dominate Integrative Biology Meeting

    1. Elizabeth Pennisi

    Boston—In addition to the normal contingent of biologists from many disciplines, this year's annual meeting of the Society for Integrative and Comparative Biology, which was held here from 3 to 7 January, attracted hundreds of coral reef scientists. Some highlights follow.

    Coral Partners May Enhance Reef Survival, Versatility

    Many visitors to coral reefs are so taken by the beauty and diversity of the colorful fish and other reef inhabitants that they never notice one of the reef's most important components: microscopic algae called zooxanthellae that color reefs greenish gold. But the absence of these algae, which inhabit the tissue of the tiny coral animals and provide the nourishment that enables corals to form large colonies, is impossible to overlook. In the past decade, they have sometimes disappeared from large expanses of reefs throughout the world, leaving them bleached a ghostly white—and apparently dead (Science, 25 July 1997, p. 491). As the reefs went white, their departed brown guests caught marine biologists' attention.

    Symbiont shuffle.

    Both hard (top) and soft (bottom) corals mix and match algal partners.

    No one knows what causes coral bleaching, although biologists have fingered everything from global warming to disease. But the scrutiny the zooxanthellae are now attracting is putting their symbiotic relationship with corals in a new light—and suggesting that the outlook for bleached corals may not be as grim as it had seemed.

    Data presented at the meeting indicate, for example, that this symbiosis undergoes seasonal fluctuations in which about three-quarters of the zooxanthellae can be lost from a reef without harming it. Moreover, corals may still retain some of these algae in deep reserve even when they look dead white. And while it was once assumed that each species of coral associates with a particular alga, researchers now find that corals can take in different zooxanthellae depending on circumstances—a hint that when one kind of algae leaves, another might come to the rescue. “There's potential for [corals] to be fairly malleable systems,” says Rob Rowan, a marine biologist at the University of Guam.

    Signs that zooxanthellae come and go with the seasons emerged in studies of coral reefs off Florida and the Bahamas that marine biologist Bill Fitt of the University of Georgia, Athens, and his colleagues began 3 years ago. The researchers expected that zooxanthellae densities and the corals' reserves of proteins, carbohydrates, and lipids would be highest in the summer, when light is most plentiful. But instead, “the highest densities [are] in the winter, in the coolest part of the year,” says Fitt. Their quarterly measurements indicated that by late summer the algal density often plunges to one-fourth or less of peak levels.

    This suggested that the high-light, high-temperature conditions of summer somehow disrupt the algae's photosynthetic pathways. Mark Warner of the University of Georgia, working with Georgia botanist Gregory Schmidt and Fitt, has confirmed that idea, showing that a light-sensitive protein, called D1, which helps convert sunlight to chemical energy, breaks down in high water temperatures—above 30 degrees Celsius. As a result, photosynthesis declines and the algae seem to die and be expelled from the coral, perhaps because they are no longer useful. “All reef-building corals bleach every single year even when we don't see it,” says Fitt. Only when algal density drops below a million algae per square centimeter, as it does in particularly hot summers with little cloud cover, does the coral begin to pale, and even then it usually recovers.

    Indeed, even coral that appears dead may have a secret reserve of algae, Cynthia Hunter, a coral-reef biologist at the University of Hawaii, Honolulu, reported at the meeting. She has studied the ability of corals to withstand sudden immersion in fresh water, a threat to corals that live in estuarine areas where rainfall can cause bursts of freshwater runoff. One branching coral, Porites compressa, seems to die in fresh water, as it bleaches and loses all signs of soft tissue. But when Hunter examined the remaining coral skeleton, she found live tissue, including zooxanthellae, underneath. That tissue enables the coral to come back to life eventually.

    Another factor may also help bleached corals bounce back: their ability to host a range of different algal guests. Evidence that they can do so first came last year when Rowan's team found that a single coral colony could have a different algal symbiont, depending on whether the coral face was in the sun or shaded. They also found that three closely related corals varied in which of the three recognized groups of algae (designated A, B, and C) they carried, depending on the depth at which the corals lived.

    Other researchers are now finding the same type of algal diversity in other types of corals. Coral reef biologist Andrew Baker of the University of Miami in Florida, for example, compared DNA in zooxanthellae collected from a variety of hard corals in locations ranging from the Bahamas and eastern Panama to Australia and western Panama. He too finds that a particular coral species can associate with more than one type of zooxanthellae. Mary Alice Coffroth and Tamar Goulet at the State University of New York at Buffalo have seen similar patterns in soft corals such as sea fans. “Coral can be seen as a landscape in which different populations of zooxanthellae are competing,” Baker told the meeting participants.

    That diversity may help explain why one coral bleaches while another just a few yards away does not. Different zooxanthellae in those corals may respond differently to the stress that leads to bleaching, Rowan explains. Bleaching may even help the coral switch to an alga better suited to new conditions. Yet he and others caution that they still have much to learn about the ongoing conversation between the algae and the coral. “It's only beginning to come out how complex it is,” says Goulet.

    Farm-Fresh Corals

    Fish and pearls now come from farms, so why not corals? At the meeting, reef scientists reported techniques that may allow aquaculturists to grow coral commercially for sale to tourists or aquarium enthusiasts, reducing the harvesting of natural reefs. The cultivated corals might also be used to reseed small swathes of reef damaged by ships, fishing, or development, says one of the researchers, Robert Richmond of the University of Guam Marine Laboratory in Mangilao.

    The idea of growing corals is not new, but with these methods, “the goal is to make the [aquaculture] system simple so that it can be used by the island communities,” says Richmond, whose university has been developing the system based on the discoveries he and others have made about coral reproduction.

    The culture systems are catching the eye of conservationists as well as entrepreneurs. “It's dangerous to think we will grow back reefs on the kilometers scale,” comments reef scientist Howard Lasker of the State University of New York, Buffalo. “But reseeding efforts [with cultivated corals] will be important in specialized cases.”

    Richmond's initial interest was not in reef restoration or aquaculture but in producing the many dozens of coral specimens he needed to test the toxicity of various chemicals to reefs. Before the corals could be cultured, however, his team first studied them in the wild to determine when the tiny polyp-shaped animals that form coral colonies release their gametes. This turned out to be within a week after the summer full moons.

    This cycle sets the timetable for coral culturing. The researchers collect adult pieces of reefs just before the full moon and place them in tanks with running seawater. When the gametes are ready, the team siphons off the eggs and sperm released by the corals and mixes those gametes in new containers where the fertilized eggs transform into swimming larvae. After 2 days, the larvae begin to settle on glass plates at the bottom of the containers. At that point, the researchers place a larger coral colony in with the settled larvae to provide a source of the algae that the new corals need to take in if they are to survive. The corals then begin forming calcified nodules—reefs in microcosm.

    Thus far, the team in Guam has cultivated 10 species with this technique. Most are branching corals, although others grow into large, rounded colonies. The researchers have learned that because the closely spaced young corals in the containers quickly fuse into a single, larger colony, cultivated corals can reach souvenir and aquarium size—about 10 centimeters around—in just 5 months rather than the year it takes in nature.

    Next summer, Richmond's team plans to scale up their operations to demonstrate whether mass-production of corals is possible. If all goes well, they expect to hold a workshop by fall to teach potential coral farmers these techniques, but they have already started transferring the technology to Palau, Richmond's colleague Sandra Romano reported at the meeting.

    Researchers interested in reconstituting damaged coral reefs are studying the cultured corals to see if they can be used in transplants instead of natural corals. “Transplanting coral is viable, but you always get some mortality,” Richmond explains.

    In one experiment, Laurie Raymundo, a coral reef biologist at Silliman University in the Philippines, and her colleagues showed that cultured coral colonies can survive when transplanted to natural reefs, provided the transplants are big enough. When they grafted colonies they had cultured using an approach similar to Richmond's onto a healthy reef off Negros Island in the central Philippines, the researchers found that only about 10% of corals with diameters smaller than 6 millimeters survived. But nearly 70% of those with diameters of 10 millimeters or more lived. The team is now monitoring the transplanted corals to see whether they will continue to thrive and to grow.

    Throat Pumps for Better Breathing, Longer Run

    For years, researchers have argued about whether lizards can run and breathe at the same time. Their anatomy suggests that they can't, at least not well. But when the wide-ranging kind of lizards called monitors run on a treadmill, their blood remains rich in oxygen—suggesting that these animals breathe just fine as they run. “It's been a fairly contentious argument for over a decade,” says David Carrier, a functional morphologist at the University of Utah, Salt Lake City. Now it may be over.

    Breathe deeply.

    X-rays reveal the monitor's expanding and contracting throat pouch (arrow).


    New data presented at the meeting by physiologist Elizabeth Brainerd of the University of Massachusetts, Amherst, and her colleagues suggest that monitors are a special case. They have found that the large throat pouches found in these lizards serve as accessory air pumps, forcing air into their lungs and overcoming the anatomical limitations of other lizards. The finding “seems to have resolved the conflict,” comments Jaap Hillenius, a physiologist at the College of Charleston in South Carolina. “Some lizards can breathe and some lizards cannot.”

    Mammals use a specialized muscle—the diaphragm—for breathing, freeing the other muscles for locomotion. But in lizards, the same rib muscles that cause the lungs to expand and contract also make the lizard's body stay upright and wiggle from side to side as it runs. As a result, these animals generally can't breathe hard when they need to most and “would have had a problem with sustained locomotion,” says Carrier.

    Brainerd got her first clue that monitors might be an exception when she made an x-ray video of a monitor lizard in motion. It revealed that the expandable gular region of the throat was filled with air and seemed to be expanding and contracting.

    Others had previously noted that when monitors breathe, they exhale all at once, but they seem to inhale in a series of small breaths. Brainerd found that those breaths feed air to the gular pouch, which acts as a pump. With each inhalation, she found, the gular region would pump several times, pushing air down into the lungs. Another sign that the pouch aids breathing is that its movements correlate with the lizard's degree of activity. “The faster they run, the more they pump; the longer they run, the more they pump,” Brainerd says.

    And when she, Tomasz Owerkowicz of Harvard University, and Colleen Farmer and James Hicks of the University of California, Irvine, prevented the pouch from pumping by propping the lizards' mouths open, the animals couldn't take in oxygen as well as before. When they ran on the treadmill at 1 kilometer per hour, their oxygen intake dropped 22%; at 2 kilometers per hour the decrease was 37%. “The faster they go, the more constrained they get,” she adds, just as predicted for lizards who can't breathe and run.

    These results help explain why monitor lizards can chase down their prey while many of their reptilian cousins sit and wait to snag a meal that comes along. They also show how evolution can solve a single problem in different ways. They suggest that the lizardlike early tetrapods, thought to be the evolutionary ancestors of both mammals and modern lizards, could run only in short, quick bursts before they used up the available oxygen and needed to stop and take a breath, so to speak. “Unless there was a change in the basic body design, you couldn't have animals with high stamina,” says Carrier. Mammals solved the problem by evolving a diaphragm muscle, and monitor lizards came to have gular pumps.


    Overfishing Disrupts Entire Ecosystems

    1. Nigel Williams

    In the face of declining fish stocks, the managers of many of the world's fisheries have been forced to take often drastic measures to prevent total collapse. These include, for example, a complete ban on fishing the Grand Banks off Newfoundland and quotas that limit takes, such as those now imposed on fishing vessels in European Union waters. But a new analysis of global fish catches over the past 45 years, which appears on page 860, suggests that even more drastic action is urgently needed.

    Bouncing back.

    Fish stocks recovered 2 years after a small reserve was set up off St. Lucia.


    The study—conducted by Daniel Pauly and Johanne Dalsgaard of the University of British Columbia in Vancouver and colleagues at the International Center for Living Aquatic Resources Management in Makati, the Philippines—concludes that humans are inexorably fishing down marine food webs as larger and more commercially valuable species disappear, creating impoverished, less valuable ecosystems. Complete fishing bans currently apply to less than 1% of the world's fishing grounds, but fisheries experts say the findings of this new study indicate that more such protected areas must be created if there is to be any chance of salvaging vanishing ecosystems. “Most researchers work at the fishery or species level, but this study looks at the global picture and reveals just how unsustainable our exploitation of marine resources is. It's a wake-up call,” says marine researcher Elliott Norse, president of the Marine Conservation Biology Institute in Redmond, Washington. (See Research Commentary on p. 821.)

    To come to this conclusion, Pauly, Dalsgaard, and their colleagues first used an analysis of the diet of 220 key species to assign to each species of catch a trophic level, a rating describing its location in the food chain. Trophic level 1 comprises the primary photosynthetic plankton, while a top predator, such as the snappers inhabiting the continental shelf off Mexico's Yucatán Peninsula, gets a rating of 4.6.

    Then, the team analyzed data collected by the United Nations Food and Agriculture Organization on catches in the world's major fisheries from 1950 to 1994 to determine whether the trophic levels had changed with time. This showed that there had been a gradual shift from long-lived, high-trophic-level fish (such as cod and haddock) to low-trophic-level invertebrates and plankton-feeding fish (such as anchovy). Overall, the researchers found a steady mean decline of about 0.1 trophic levels per decade in the worldwide catches. What's more, Pauly says, “this is probably an underestimate, as catch measurements from the tropics are poorly recorded.”

    The results also indicate that the quantities, as well as the quality, of the catches are decreasing. At first, skimming off the top of the food chain and then moving down to lower trophic levels can lead to increased catch sizes, because top predators require a large reservoir of prey to sustain them. But the new research shows that, in most instances, when the top predators are removed, catches stagnated or declined, apparently because the populations of the predators' competitors for food expand. “The Black Sea provides a good example,” Pauly says. “There's been a huge increase in jellyfish as their economically valuable competitors have been removed.”

    As a result of this overfishing, the number of main fisheries in the Black Sea has fallen from 26 in the 1970s to five now, says Norse. “Present fishing policy is unsustainable. The food-web structure is changing,” says Pauly. “At least 60% of the world's 200 most commercially valuable species are overfished or fished to the limit,” says Claude Martin, director-general of the World Wide Fund for Nature.

    Pauly argues that there is an urgent need to create protected areas, where fishing is not allowed. Although other measures, such as quotas, limiting fishing time at sea, changing fishing gear, and controlling pollution are crucial, they are difficult to implement quickly and control, he says. And there is growing evidence that protected areas can be highly effective in restoring and maintaining marine ecosystems. Such areas on the Georges Bank off Massachusetts were created only in 1994, but researchers are already finding an increase in the size and spawning populations of key fish species, as well as a rapid increase in the bottom-dwelling scallop population, says a spokesperson for the National Marine Fisheries Service in Woods Hole, Massachusetts.

    Even tiny protected areas can be very effective in some regions. Callum Roberts of the University of York in the United Kingdom says reserves of just a few hectares on tropical coral reefs have boosted fish stocks and helped maintain long-lived large predators.

    The fishing industry is also now beginning to back this policy. In the United Kingdom, the industry now backs plans for no-fishing areas as a key way to develop the European Union's fishing policy in the face of declining stocks, says Roberts. “At the very least, they can offer quick and simple protection while the complexity of long-term sustainable fishing policies are developed,” says Norse.

    But Pauly's results have set a clock ticking on the development of such policies. “In 30 to 40 years, our fisheries could have moved down another 0.5 of a trophic level in overall catch, which is an enormous change,” he says. “If things go unchecked, we might end up with a marine junkyard dominated by plankton.”

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