REPORTS ON RESEARCH FROM WOODS HOLE OCEANOGRAPHIC INSTITUTIO* Contents Discovering Life and Sustaining Habitats — Laurence Madin 4 The Undiscovered Ocean 6 12 17 20 24 Coral Gardens in the Dark Depths Scientists seek to learn more about these fragile, threat- ened communities— Lauren Mullineaux and Susan Mills Little Things Matter A Lot Once overlooked, cyanobacteria are among Earth's most important organisms— John Waterbury The Deeps of Time in the Depths of the Ocean Discoveries of unusual marine microbes are radically changing our views about the evolution of life —Andreas Teske and Katrina Edwards Life in the Arctic Ocean Distinctive species and environmental factors combine to create a unique, complex food web—Carin Ashjian Shedding Light on Light in the Ocean New researcli is illuminating an optically complex environment— Sonke Johnsen and Heidi Sosik COVER: Bright yellow stony corals (Enallopsammia) stand like bare trees, 1,500 meters (4,500 feet) deep on the basalt flank of Manning Seamount, an extinct undersea volcano that is part of the New England Seamounts chain off the east coast of the United States. Nearby a lower-growing, pale pink soft coral (Camlidella) is covered with darker pink brittle stars feeding on the coral polyps. (Photo taken with the ROV Hercules, courtesy of the "Mountains in the Sea" scientific party, NOAA, and the Institute for Exploration.) Ocean Ecosystems and Resources T Q Whither the North Atlantic Right Whale? Scientists explore many facets of whales' lives to help a species on the edge of extinction — Michael Moore ~)A Scientists Muster to Help Right Whales With time running out, an ambitious research plan is launched for an endangered species— Laurence Madin 36 39 42 45 48 The Secret Lives of Fish Scientists learn to read the 'diary' recorded in the ear bones of fish— Simon Thorrold and Anne Cohen In Tiny Ear Bones, the Life Story of Giant Bluefin Tuna — Anne Cohen and Graham Layne Ar> Tracking Fish to Save Them The Reef Fish Connectivity and Conservation Initiative — Simon Thorrold Do Marine Protected Areas Really Work? Georges Bank experiment provides clues to longstanding questions about closing areas to fishing —Michael Fogarty and Steven Murawski Can We Catch More Fish and Preserve the Stock? Mathematical analyses offer new insights into age-old controversies on fishing restrictions — Michael Neubert Voyages into the Antarctic Winter Cruises into the pack ice of the Southern Ocean reveal secrets of its fertile ecosystem — Peter Wiebe 2 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Dear Reader, This issue, devoted to the WHOI Ocean Life Institute, concludes our series on research by the WHOI Ocean Institutes. Starting in June, you will see a redesigned Oceanus, featuring articles and images that reflect the breadth of research at the Institution. Oceanus is now published continually online at oceanusmag.whoi.edu. Reading Oceanus online is free and you may sign up to receive E-mail alerts when new articles are published. 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Phone _ Expiration Date_ E-mail Signature v43n2 m New Technologies 54 57 59 64 68 72 Run Deep, But Not Silent A new tagging device lets scientists 'go along for the ride' into the underwater world of whales — Peter Tyack Playing Tag with Whales Engineers overcome nightmarish specifications to create a dream instrument— Mark Johnson How to See What Whales Hear Biomedical imaging reveals new insights into marine mammal ears — Darlene Ketten Revealing the Ocean's Invisible Abundance Scientists develop new instruments to study microbes at the center of the ocean food web — Rebecca Cast Sensors to Make Sense of the Sea An expanding variety of sensors is changing the way we monitor dynamic ocean systems — Scoff Gallager Down to the Sea on (Gene) Chips The genomics revolution is transforming the way scientists can study life in the oceans — Mark Hahn 1930 EDITOR: Kate Madin OCEAN INSTITUTE SERIES EDITOR: Lonny Lippsett CONTRIBUTING EDITOR: Michael Carlowicz DESIGNER: Jim Canavan, WHOI Graphic Services CONTRIBUTING DESIGNERS: Katherine Joyce and Jeannine Pires WHOI PRESIDENT AND DIRECTOR: Robert B. 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N v- - The Ocean Life Institute Discovering Life and Sustaining Habitats The oceans cover 70 percent of the planet's surface and constitute 99 percent of its living space, and every drop of ocean water holds living things. Without its oceans, Earth would be a rock in space, and life may never have appeared on our planet. The sea is the great experimental labo- ratory of evolution. In three billion years of Earth history, its waters have nurtured nearly every form ot life that has ever ex- isted, including probably the first entities that were truly alive. The ocean is home to the greatest part of Earths biodiversity, containing 90 percent of the major groups of living things. They range from immense to minute and live everywhere, from gey- sers on the seafloor to the lips of lobsters. In the 20th century, new technology enhanced traditional collecting meth- ods to locate organisms and characterize their habitats. Satellite pictures of light reflected from chlorophyll in the ocean revealed broad patterns of phytoplankton abundance, and satellite maps of ocean temperatures helped us understand the distribution of pelagic animals. Submers- ibles, manned and robotic, explored parts of the deep ocean never before visited, retrieving images and specimens of crea- tures new to human knowledge. Even surface waters yielded new discoveries of ubiquitous microbes, including photo- synthetic bacteria responsible for half the primary production in the ocean. Revo- lutionary biotechnology concepts and methods, applied to life in the sea, helped us discover new organisms, untangle evo- lutionary relationships, explain adapta- tions, and reveal fundamental mecha- nisms of life. Entering the 21st century, ocean biolo- gy faces tremendous challenges — not only to understand the complex ecosystems of the sea, but to learn how to maintain the integrity, productivity, and resources of the ocean for the future. The sea and its biology is crucial for us and our planet— for balancing oxygen and carbon dioxide, for maintaining genetic diversity, and for producing food. Human civilization is putting increas- ing pressure on ocean life, from overfish- ing, nutrient pollution, waste dumping, and climate change due to greenhouse effects. These are large and complex prob- lems; understanding and alleviating them is essential. But the promise is also great. We know the major problems and largely how they came about. We now understand better how fish populations respond to fish- ing pressure, how toxins affect marine animals, how nutrients stimulate phy- toplankton blooms, how whales react to noise, or how species diversity maintains stable ecosystems. Much of the information and technol- ogy for defining problems and identify- ing solutions is within our grasp, or will be soon. That knowledge and capability give us the basis for action to understand, sustain, and restore the ocean's ecosys- tems. Public awareness, funding, regula- tory action, and economic adjustments are also needed, but with continued research, we can ensure that the necessary scientific knowledge will be at the ready. The Ocean Life Institute (OLI) fosters research in ocean biology under three broad charges: Discover Life, Sustain Eco- systems, and Develop Tools. The goal for the OLI is to support pioneering basic sci- ence, both for its own value and to help solve important ecological and societal problems of the ocean. Discover Life This theme broadly includes explora- tion, discovery, and characterization of ocean organisms. The OLI has funded studies on new deep-sea microbes, fossil corals, and magnetic bacteria. Discovery may mean new information about where organisms live, how they evolved, and how their particular traits fit into the tapestry of marine communities. Often discovery happens when we look in familiar places with new tools and techniques. 4 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu N •• t \ , Sustain Ecosystems Organisms together create commu- nities that then provide stable habitats. These ecosystems, whether as small as a single coral head or as large as the Sar- gasso Sea, are maintained by the interac- tion of the particular organisms in the ecosystems with environmental forces, such as temperature, currents, nutrients, and sunlight. Changes in the abundance and diversity of key species (perhaps due to fishing or toxicity) or in the physical or chemical environment (from climate change or excess nutrients) can upset an ecosystems equilibrium and lead to dramatic shifts that could decimate re- sources or imperil species survival. The OLI sponsors studies on toxicity of cop- per mine waste to seaweeds and industrial chemicals to fish, on responses of whales to stress, and on mathematical models to help manage fisheries and save threatened albatross populations. Develop Tools Even as it makes ocean life possible, water impedes research, and we need special equipment and techniques to ex- tract specimens and information from the depths. New electronics, optics, computers, and molecular biology add a huge range of possibilities for tools to explore ocean life. Such tools, including biological and chemi- cal sensors, can be deployed in many ways. Whether lowered from ships, borne on submarine vehicles, or mounted on moored or mobile observatories, these new sen- sors yield information on organisms both at small scales and over large distances and long time periods. New tools developed with OLI support include imaging systems for phytoplankton cells, heartbeat moni- tors for whales, and molecular probes to sample and identify microbes. Stewardship ot the future rests on today's knowledge. Important deci- sions must be made soon about how to conserve, restore, or manage ocean envi- ronments and resources. Such efforts have often tailed, lacking accurate information about biology and ecology. The vision for the WHOI Ocean Insti- tutes includes furnishing knowledge and awareness to those who need to use solid scientific information to benefit society and the environment. With this goal, the Laurence Madin, Ocean Life Institute director Photo by lain Kerf, Ocean Alliance OLI has launched two research initiatives: First, to provide focused scientific infor- mation to help conserve the highly en- dangered North Atlantic right whale; and second, to provide life-history data needed for effective policies to regulate fishing on coral reefs and enable the rejuvena- tion of important reef species. People breathe - the oceans oxy- o I gen, eat its fish, and § marvel at the beau- ty of its inhabitants. But we also over- reach in our harvest, pour our wastes into ocean waters, and damage the framework ot many habitats. Achieving a new balance with the ocean will prove a challenge for the burgeoning human population, but one that can be met if we inform our ac- tions with scientific knowledge. — Laurence Madin Laurence Madin, a transplanted fourth -generation Californian, makes his home in Massachusetts studying gelatinous animals such as medusae, siphonophores, ctenophores, and pelagic tuni- cates. Growing up in the San Francisco Bay area, he developed an appreciation for the natural world and the sea. He received an A.B. degree from the University of California, Berkeley, and a Ph.D. in zoology from UC Davis, having spent some ot graduate school on a Bahamian island, helping pio- neer the use of scuba diving to study plankton. Since coming to WHOI in 1974, he has also used submersibles and remotely operated vehicles to explore strange jelly creatures in deep water. Cur- rent projects include dynamics of salp blooms in the Atlantic and Antarctica; predation on larval fishes on Georges Bank; biogeography ot plankton and fishes in the open ocean and deep sea; and developing new gizmos for sampling and exploration. Formerly chair of the Biology Department, Madin is the current director of the Ocean Life Institute, which has broadened his interests into tropical ecology, endangered whales, conservation biology, and policy. He still enjoys diving (even in Antarctica), photographing, and playing with plankton. Woods Hole Oceanographic Institution 5 Coral Gardens in the Dark Depths Scientists seek to learn more about these abundant, fragile, and now-threatened communities By Lauren S. Mullineaux, Senior Scientist and Susan W. Mills, Research Associate Biology Department Woods Hole Oceanographic Institution The words "coral reefs" conjure up im- ages of a tropical paradise: shallow, warm, aquamarine waters, bright sun- light, white sand, and colorful, darting fish. But corals also live deep in the sea, in regions where the sun doesn't pene- trate and water temperatures remain just above freezing. Until recently, deep-sea corals were relatively unknown. But as scientists have explored further and farther, they have found corals living in deep places throughout the world's oceans. Like their tropical cousins, deep-sea corals can be brightly colored and harbor a rich diver- sity of underwater life, including abun- dant commercially valuable tish. Fishermen have discovered these deep- sea coral communities, too. Unfortunate- ly, commercial trawling on seamounts has caused declines in the fish populations and serious damage to coral communities. Like ancient, solitary, old-growth for- ests on land, these deep-sea coral com- munities may be easily disrupted and slow to recover. Once lost, they may dis- appear, along with the diverse, complex ecosystems they have sustained over long reaches of time. Oases in a deep-sea desert Scientists have learned that deep-sea corals tend to live in areas with rocky to- pography: on oceanic mountain ranges, the continental slope, and underwater volcanoes, or seamounts, whose slopes and canyon walls provide the two things corals need most: a hard surface to an- TOUCHED BY A COLD HAND — A colonial soft coral (octocoral) pulls in its small, whitish polyps upon contact by the manipulator hand of the remotely operated vehicle Hercules. This coral (ParagorgiaJ is called "bubblegum coral" because of its color and bulbous branch ends. It is common on the New England Seamounts. Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.ed chor to and access to food. Corals cannot live on muddy or sandy bottoms. They must find something hard to attach to, such as rock or another coral skeleton. Topographic features in the deep sea create islands of habitat, sur- rounded by fine sediments that are inhos- pitable for corals. Though corals may look like plants, they actually are colonies of animals, re- lated to sea anemones. Each individual, or "polyp," is connected by tissue to oth- ers, and they live together, usually within a skeleton that they secrete for support. Food and shelter Deep corals differ from shallow-liv- ing, reef-building corals in several ways. 1 hey live in high and mid-latitudes, not just in the tropics. They need no sunlight, because they do not rely on the symbiotic relationship with photosynthetic algae, which provide food to shallow-living cor- als in exchange for a place to live. Instead, deep corals feed entirely on small plank- ton and organic particles — stirred up and brought to them by ocean currents that in- tensify when they hit undersea mountains. These currents also feed a rich variety of other small animals that seek refuge from predators in the large, immobile cor- als, whose structures are as complex as the trunks and branches of a forest. Inverte- brates such as brittle stars, sea stars, and feathery crinoids live directly on the coral colonies, and smaller animals burrow into the skeletons. In the North Pacific, deep coral com- munities are inhabited by an abundance of fish, crabs, and other commercially impor- tant species. Dense schools offish are asso- ciated with deep coral mounds oft Norway and with a kind of coral called octocorals on seamounts off New Zealand. All in all, the corals live in a quiet, stable neighborhood. In deep waters, temperatures and salinity levels are con- stant. In the depths, the communities are not exposed to hurricanes or buried by a tailing rain of sediments, and natural dis- turbances are uncommon. VENERABLE INVERTEBRATES— Deep-sea stony corals can attain great ages, and the hard skeletons of dead ones sometimes form mounds, tens of meters long and high, which support living colonies. This yellow stony coral has soft corals, feather stars, and brittle stars as neighbors. HOT COLOR IN THE COLD DEPTHS— A pink bushy black coral, a white tree-like soft coral behind it, and a bright yellow sponge share a rocky seamount slope far below the reach of sunlight. CLEAN SLATES — Researchers placed blocks of basalt on a seamount's rocky surface to investigate whether larvae from other communities will settle near these two colonies of corals (ParagorgiaJ. The blocks, next to a numbered marker and attached to yellow lines for retrieval, have been in place for a year. Woods Hole Oceanographic Institution 7 A HARD-ROCK FOUNDATION — Corals need a hard surface to grow on, like this circular outcrop of basalt. A red crab roams over sand and rock. Stony, soft, or black Though they may be found in the same habitats, three different types of corals live in the deep sea. Stony coral skeletons are dense and rocky, often persisting long alter coral colonies have died. The stony corals are related to shallow tropical reef-building species (sderactinians). They can form extensive mounds, reaching 12 kilometers in length and protruding as far as 30 me- ters above the seafloor. Soft corals (or octocorals) often look like colorful undersea gardens of pink, red, and white. They grow in many dif- ferent forms, including branching sea fans and sea pens. From a distance they look like bushes or trees, sometimes reaching two meters tall. An octocoral's flexible skeleton is formed by small NO VISIBLE MEANS OF S PPORT — Black corals have many forms and colors. This unbranched "black whip coral," attached to the bottom, is supported only by the water. spines (spicules) embedded in a firm or- ganic substance. The third type, black corals (antipath- arians), are usually orange to tan, but se- crete hard black proteinaceous skeletons. They have varied growth forms, includ- ing branching and unbranched shapes. Scientists who have studied deep-sea coral species suggest that corals can live for hundreds of years. By measuring ra- dioactive isotopes (with known half-lives) in their skeletons, scientists have calcu- lated that some large colonies of the soft corals Paragorgia and Primnoa appear to be at least 500 years old. Reefs of stony corals Lophelia and Oculina are estimated to be more than 1,000 years old. Radio- metric dating also indicates that the cor- als grow very slowly. Two ways to reproduce We still have very little information about how deep coral species reproduce, but we assume that it is similar to shallow species. Shallow-water corals reproduce sexually, or asexually, and some do both. Asexual reproduction occurs through the production of buds that grow on the 8 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu colony, or by fragments that break off and settle near the parent colony. In fact, some researchers think that even very large mounds of stony coral (Lophcliii) are formed by fragmentation, and that in- dividual colonies are genetic clones of the first coral larvae that settled there. Sexual reproduction produces micro- scopic larvae that disperse through the water — sometimes traveling far before they attach to a hard surface and grow. So far, scientists have rarely observed any sites with young deep-sea corals, indicat- ing that these organisms do not disperse and colonize frequently or easily. Their slow growth rates, longevity, and infre- quent colonization may make deep-sea coral communities more vulnerable to extinction when they are disturbed. Endangered communities? Fishermen once avoided areas with deep-sea corals because they damaged their nets. Now, redesigned trawls and new techniques tor removing corals en- able fishermen to take advantage of these highly productive locales with less risk of losing gear. Recent damage to deep- sea coral ecosystems and declines in fish stocks have led conservation groups to call for fishing bans in areas with deep corals and the creation of marine protect- ed areas in these places. (See "Do Marine Protected Areas Really Work?" page 42.") To understand and predict how deep- sea coral communities will respond to and recover from disturbances, we need to know how often and where new colo- nies are established. Some communi- ties might frequently receive incoming coral larvae from other coral colonies and therefore be resilient to disturbances. Others may be colonized rarely, making them less likely to recover from a distur- bance and more vulnerable to extinction. A second critical factor is where new colonists come from. If they arrive as lar- vae from remote populations, new settlers enhance the chances that a community will recover in the wake of a local catas- trophe. But if new colonies form through A CORAL LINE — A line of deep-sea corals recedes into darkness. From bottom left to top right: white, bushy soft corals, a bright orange black coral, a branched soft coral like a bare tree, and white, twisted, branchless bamboo corals. Sharing center stage in front are (from left to right) a dark, bottlebrush-shaped black coral, a red soft coral, and purple crinoids (relatives of sea stars). fragmentation or budding from estab- lished colonies, then the source ot new colonists expires when the parent colo- nies are destroyed. Counting the newcomers We use several methods to investigate how deep coral colonies recruit new set- tlers. First, we monitor and count coral communities for the appearance of new individuals. Second, we can measure settlement directly. On top of a seamount, we set out clean blocks of basalt, similar to the natural hard surface of the sea- mount. This provides new, uncolonized habitat tor any corals to settle on. After a time, we recover the blocks and count the number of polyps that settled on them. Some new corals appear to prefer to settle directly onto dead coral skeletons. To test this, we can also make experimen- tal settlement surfaces out of biologically produced (biogenic) calcium carbonate that mimics coral skeletons. In our first short-term colonization studies on Pacific seamounts, few larvae FRAGILE OASES — Rising abruptly from the seafloor, seamounts are home to fragile ecosystems often dominated by corals. They are vulnerable to damage by fishing gear and are believed to be slow to recover. Many scientists recommend making them protected areas. The New England Seamount chain stretches from the New England coast toward the middle of the North Atlantic. Woods Hole Oceanographic Institution 5 settled on our blocks. In a longer-term study on the New England Seamounts in the North Atlantic Ocean, we placed 20 blocks at two sites and re- covered them after 10 months. No corals had settled in that time, though other in- vertebrates (anemones and snails) had. Because of the slow settling, we left the remaining blocks in place for an even longer time, and also placed blocks in different habitats at geographically separate sites. i Coral demographics V To gain insights into when colonies formed, we determine the ages of cor- als and map their locations within the communities. For instance, if we see a continuous range of ages in a community, including very young colonies, we can infer that colonization is still occurring, and at a fairly constant rate. If instead we see only very old individuals, we infer that V' I V . ; |p ; ||f;|;§:: CALCULATING CORAL AGES— By measuring the amount of a naturally occurring lead isotope (with a known half-life) in this section of a Paragorgia trunk (actual size), scientists can determine how old the coral is. a past colonization event established the community, but that new recruits are no longer arriving. We also map the positions of corals in a community to determine the sequence in which the community was settled. If corals are reproducing by fragmenta- tion, we expect the youngest colonies to be located near older colonies. But if _ colonists arrive as larvae from remote g populations, we might not expect to ' .•' = s see clusters of the same species. For community-scale mapping, we examine images taken from cameras on the submersible Alvin. But to survey larger areas, we need ve- hicles with greater range and versatility. To search for new coral communities, a towed camera system is relatively inex- pensive to operate and can be used from a ship during night hours when a hu- man-occupied submersible is recharging batteries. Autonomous and remotely op- MIDNId • A deep coral community grows on volcanic rock in the New England Seamount chain. It includes an abundance of invertebrate animals, including pink, white, and orange soft corals, red-orange sea stars, and a multitude of light-colored sponges. 10 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu BLACK BUT ORANGE — Black corals can have several growth forms and external tissue colors. This one, bright orange and feathery, is nearly six feet tall. Their hard black internal skeletons are prized for jewelry. crated underwater vehicles are also im- portant tools, providing high-resolution topographic maps and seafloor images. Genetic investigations We are also using molecular genetic techniques to investigate where new cor- als come from, working with Scott France of the College of Charleston. By com- paring the genetic composition of newly settled corals to those of established colonies, we can decipher whether more recent colonists come from a nearby or faraway source. If the new colonies started from frag- ments or budding of locally established adults, they will be genetically identical to them. In contrast, corals from remote populations will have a different genetic makeup. It the new coral differs geneti- cally from older colonies, and we know the genetic composition of other popula- tions, then we may eventually be able to identify exactly where the new coral dis- persed from. Old-growth gardens Because of deep-sea corals' impressive ages, slow and infrequent replacement, and role as habitat for diverse communities, they invite comparison with old-growth forests. However, they are quite different from terrestrial systems, and succession, change, and restoration in these commu- nities may not follow any pattern we see on land. Only by carefully measuring the scaleYspeed, and sources of new recruits to deep coral communities will we be able to predict how and whether they can recover from the kinds of damage they now face. Lauren Mullineaux is a biological oceanographer at Woods Hole Ocean- ographic Institution and faculty member of the MIT/WHOI Joint Program in Oceanography. She grew up in Colorado and started studying desert plant communities, but got hooked on oceanography after sail- ing on a research cruise in college. Currently, she studies the larval stages of marine invertebrates in order to understand how species disperse and colonize remote habitats. Much of her recent fieldwork has focused on the ecology of deep-sea communities, particularly on seamounts and at hydro- thermal vents. Susan Mills came to Woods Hole in 1975, after finishing her bachelor's degree at Brown University. Working first at the Marine Biological Labo- ratory and then at WHOI, she has participated in projects including studies ot population genetics of polychaete worms, identification of hydrothermal vent invertebrates in plankton samples, measurement of trace element con- centrations in bivalve shells, and coral colonization at seamounts. Her work takes her to salt marshes in Massachusetts and deep-sea sites in the Atlantic and tropical Pacific— far too often, in the opinion of her husband. In her "spare time," she enjoys working on her lab's Web site, studying Spanish, and spending time with her family — especially traveling to South America with her two children to visit the countries where they were born. Woods Hole Oceanographic Institution 11 Little Things Matter A Lot Overlooked in the ocean until the 1970s, cyanobacteria are among Earth's most important organisms By John Waterbury, Associate Scientist Biology Department Woods Hole Oceanographic Institution When people think of bacteria, they usually think of germs— dis- ease-causing agents that threaten human health. In reality, bacteria make life on Earth possible. One group — the cyanobacteria — has completely transformed Earth's environ- ment through their long history. Three billion years ago, ancestors of cyanobac- teria infused Earth's ancient atmosphere with the byproduct of their photosyn- thesis—oxygen—changing the chemis- try of the planet and setting the stage for entirely new oxygen-breathing life forms to evolve. Without the cyanobacteria, the life we see around us, including humans, simply wouldn't be here. Before 1970, cyanobacteria were known to occur widely in tresh water and terrestrial habitats, but they were thought to be relatively unimportant in the mod- ern oceans. This perception changed dramatically in the late 1970s and 1980s with the discovery of photosynthetic pi- coplankton by scientists at Woods Hole Oceanographic Institution and the Mas- sachusetts Institute of Technology. Tiny members of this group of newly discovered cyanobacteria, Synechococcus and Prochlorococcus, turn out to be the most abundant organisms on the planet today. They are at the base of the ocean's food chain, making air, light, and water into food for other life. Today, exploiting new biotechnological techniques, we are exploring their genes and uncovering the secrets of these extraordinary organisms. 12 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.ee An unexpected glow In 1977, I was on Atlantis //in the Arabian Sea with WHOI microbiolo- gist Stanley Watson, measuring bacterial abundance and biomass. We were using a new technique employing epi fluorescence microscopy: fluorescent dyes that labeled nucleic acids, making bacterial cells fluo- resce green when excited with blue light. But, to our great surprise, some sam- ples contained cells that glowed a brilliant orange— before any dye was added. The color was produced by the natural fluo- rescence of phycoerythrin, the primary light-harvesting pigment in many cyano- bacteria. This was our first introduction to Synechococcus. To examine this new cyanobacte- rium, we attempted to culture it on that cruise, using media developed during my Ph.D. studies. But the cells died within 24 hours. It would take almost a year to develop media in which Synechococcus could successfully be isolated and grown in the laboratory. We knew right away that Synechococ- cus was important by the impressive numbers ot them that we found in seawa- ter samples. Since 1977, they have been tound everywhere in the world's oceans when the water temperature is warmer than 5°C (41°F) at concentrations from a few cells to more than 500,000 cells per milliliter (about 1/5 of a teaspoon), depending on the season and nutrients. This amazing abundance makes them a source of food tor microscopic proto- zoans, the next organisms up in a food chain that ends in fish and mammals. Cycles of life Bacteria take up the elements essen- tial to life — especially carbon and nitro- gen— and incorporate them into mol- ecules that higher bacteria-consuming organisms use for growth. Bacteria also can reverse the transformation, return- ing elements to the environment, com- pleting sequences of reactions known as nutrient cycles. Without the continuous cycling of these elements, all biochemical BARBELL BACTERIA — Cyanobacteria have mechanisms that allow two antagonistic physiological processes to coexist in the same organism: oxygen-producing photosynthesis and dinitrogen fixation, which is inhibited by oxygen. In Richelia (above), the two processes are separated by space: Dinitrogen fixation occurs only in the bulbous, specialized cells (heterocysts) at the end of a 60-micrometer-long, filamentous cyanobacterium. life processes would lead to a dead end. Cyanobacteria are vital to two pri- mary nutrient cycles in the ocean. In the carbon cycle, they photosynthetically "fix" carbon from air into organic mat- ter at the base of the food chain, simulta- neously releasing oxygen. Many are also important in the nitrogen cycle— a com- plex series of reactions and transforma- tions, including one known as nitrogen fixation, which converts nitrogen from the air and incorporates it into cellular compounds. The key is cyanobacteria's ability to use molecular nitrogen (N2, or dinitrogen) as a source of nitrogen for their cells. Cyanobacteria live anywhere there is light and moisture: in the open oceans, in pristine or polluted lakes and streams, in soils, hot and cold deserts, hot springs, brine pools, and salt ponds. In symbiotic relationships with algae and plants, they provide nitrogen to their hosts in ex- change for a site to live on. In many instances, Cyanobacteria are visible to the naked eye. Their name is derived from one of their major light-har- vesting pigments (phycocyanin), which has a characteristic blue-green color. In coastal oceans, Cyanobacteria form dark blue-green mats covering rocks and mol- lusk shells in tidal pools. Along upper limestone shores, they form black crusts that erode rocks. In salt marshes throughout the world, several types of Cyanobacteria play a key ecological role in binding sediments by forming dense layered mats. In the tropics, these mats, called stromatolites, become thick; Cyanobacteria inside them look almost indistinguishable from those in three-billion-year-old fossil stromatolites. This is evidence that Cyanobacteria inhab- ited the seas when Earth was still young. How oxygen got in the atmosphere Three billion years ago, Earth's atmo- sphere contained little oxygen. But ances- tral Cyanobacteria thriving in the early oxygen-free oceans evolved a biochemi- Woods Hole Oceanographic Institution 13 The "red" in the Red Sea The cyanobacterium Trichodesmium erythraeum forms filaments (left) made up of many cylindrical cells, each about 9 micrometers (10~6 meters) wide. Hundreds of filaments form a raft-shaped colony of Trichodesmium erythraeum several millimeters (70~4 meters) long (above). The raft is red because the cyanobacteria contain the red light-harvesting pigment, phycoerythrin. In calm weather, buoyant colonies rise to the surface in massive blooms that can cover thousands of square kilometers. These blooms gave the Red Sea its name. cal mechanism for photosynthesis, which used light to generate cellular energy by splitting water molecules, and producing oxygen in the process. For a billion years, growing and mul- tiplying in the sea, they slowly raised the oxygen level in the atmosphere to 20 percent, the level that supports oxygen- breathing life. Cyanobacteria alone, di- rectly or indirectly, are responsible for all of the oxygen in our air. In every case, the green plants we are most familiar with, from unicellular algae to trees, owe their photosynthetic abilities to small chlorophyll-contain- ing bodies within their cells known as chloroplasts— which look a lot like cya- nobacteria. In fact, most microbiologists believe that chloroplasts are derived from , teria — or, more precise- ly, that ancestra :yanobacteria entered larger cell • symbiotic in them, giving tr ie ability to photo- synthesize, aiu reating plants. An ancient process Both plants and cyanobacteria use carbon dioxide in air to synthesize cell carbon. But only bacteria can fix dini- trogen as a sole source of nitrogen in cells. Microbiologists believe this ancient process evolved very early, while Earth's atmosphere was still without oxygen, be- cause the necessary enzyme, nitrogenase, is inactivated by oxygen. Cyanobacteria have mechanisms that allow oxygen-producing photosynthesis and dinitrogen fixation — two antagonis- tic physiological processes — to coexist in the same organism. In some, the two pro- cesses are separated by time: Photosyn- thesis happens during daylight and dini- trogen fixation at night. In more complex species, the two processes are separated by space, with dinitrogen fixation occur- ring only in specialized cells (heterocysts) within filaments. Trichodesmium, a filamentous cyano- bacterium, plays an important ecological role by replenishing nitrogen in the cen- tral oceanic gyres — areas of widely circu- lating currents in the middle of oceans — where nutrients like nitrogen, required by other marine microorganisms for growth, would otherwise be low. In calm weather, their buoyant red-colored colonies rise to the surface, resulting in massive blooms that can cover thousands of square kilo- meters. These blooms gave the Red Sea its name. Cultural breakthroughs Trichodesmium quickly disintegrates when collected at sea and has been noto- riously difficult to culture in the labo- ratory. In 1990, my lab at WHOI estab- lished conditions that made culturing routine and reliable by using very rigor- ous cleanliness. It turns out that instead of failing to add something these cyano- bacteria required, we were inadvertently poisoning them with trace contaminants in our chemicals and on our glassware. We can now grow four of the five species of Trichodesmium in the lab and use molecular genetic methods to study them. (See "The Deeps of Time in the Depths ot the Ocean," page 17.) In col- laboration with the U.S. Department of Energy's Joint Genome Institute, we have sequenced the entire genome of one Trichodesmium species. These advances give scientists at WHOI and elsewhere the ability to uncover the genetic reasons for Trichodesmium's success. We can also culture Syneclwcoccus, and using molecular methods, scien- tists have found 12 distinct groupings, or clades, of marine Syneclwcoccus, each ap- proximately equal to a species. Scientists at the DOE's Joint Genome Institute have already sequenced the genome of one type, and others will soon follow. Scientists are examining the factors that control Synechococcus's growth and distribution to understand more about their role in the ocean, especially in the food chain. Others are examining how Synechococcus coexists with a diverse and abundant group of cyanophages. 14 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Microbial libraries Kven as we studied Synechococcus, new surprises awaited. In 1985 Robert Olson of WHOI and Sallie Chisholm of MIT discovered a second group of even smaller photosynthetic picoplankton in the Sargasso Sea, in the central North Atlantic Ocean. Olson took to sea, for the first time, an instrument that could count bacterial cells using fluorescence: the Flow Cytometer. The instrument led to the discovery of cyanobacteria ranging in size from 0.7 to 1.0 micrometers called Prochlorococcus. It is our great fortune that these cya- nobacteria can also be cultured in the lab. Scientists at MIT have assembled a col- lection of strains (cell lines) for Prochlo- rococcus collected from various places, while \VHOI maintains collections for Synechococcus, Trichodesmium, and Cro- cosphaera, another recently discovered cyanobacterium. As a sort of lending library of cells, these two sites provide cultures for microbiologists all over the world to study. Oceanographers measuring Prochlo- THE INSIDE STORY — Richelia are cyanobacteria that live symbolically inside single-celled marine plants called diatoms. The cyanobacteria have specialized dinitrogen-fixing cells that provide nitrogen to their hosts. Above is a light micrograph of the diatom Hemiaulus sp. Below is an epifluorescence light micrograph of the same cells, showing the red chloroplasts of the diatom and the orange fluorescence of the barbell-shaped endosymbiotic Richelia. Telltale fluorescence Many biological compounds, including photosynthetic pigments such as chlo- rophylls and phycobiliproteins, fluoresce naturally when excited with light. This natural fluorescence played a key role in the discovery of marine photosynthetic picoplankton. In 1977, we were using epifluorescence light microscopy to count bacteria in sea- water, aided by fluorescent dyes that stained bacterial nucleic acids. Synechococcus was discovered when, quite by chance, we examined unstained samples and were immediately struck by the numerous small cells that fluoresced bright orange (be- low). The brilliant orange color results from the natural fluorescence of phycoery- thrin, one of the phycobiliproteins abundant in cyanobacteria. In 1985, WHOI scientist Rob Olson was the first to take a new instrument, the Flow Cytometer, to sea. It exploits fluorescence to study individual cells. With it, he and Sallie Chisholm of MIT detected very small cells with natural fluorescence of their chloro- phylls. This unique "signature" led 1 1 to the discovery of Prochlorococcus, \ i which turn out to be among the most abundant organisms of Earth. WHOI scientists Rob Olson and Heidi Sosik prepare to test a new-generation Flow Cytometer. dl tion Woods Hole Oceanographic Institution 15 Eureka moments and cul-de-sacs In 1975, Ralph I .-.' m Scripps Institution of Oa\>;. ..-•.•jphy found something sen-! .T knew ex- isted— Pro* .'• : mbiotic cya- nobacterium living in sea squirts in Palau. it was a legitimate "Eureka mo- ment," signifying the discovery of a previously unknown kind of organism known as prochlorophytes. But it also offered the tantalizing possibility of an even more momentous, heart-thump- ing discovery: how the first plant on Earth evolved. Cyanobacteria inhabited the Earth billions of years ago, and scientists believe that ancestral cyanobacteria started symbiotic relationships with larger cells and provided them with the ability to photosynthesize. Eventu- ally, these cyanobacteria evolved into chloroplasts, the photosynthetic facto- ries inside all plant cells. Prochlorophytes, like other cya- nobacteria, contain chlorophyll a, a Transmission electron micrograph of a thin section of Prochlorococcus sp. pigment important in photosynthesis. But unlike other cyanobacteria, which contain phycobiliproteins to absorb solar energy for photosynthesis, pro- chlorophytes contain chlorophyll b as their light-harvesting pigment. So do all green plants. Microbiologists speculated excit- edly that prochlorophytes were on the same evolutionary pathway that led directly to chloroplasts in modern green plants. But the theory didn't hold. Phylo- genetic studies showed that the three known prochlorophytes (Prochloron, Prochlorothrix, and Prochlorococcus) evolved separately from within the cyanobacteria, and none was on the same line of descent leading to higher- plant chloroplasts. Although chloro- plasts also arose from cyanobacteria, their modern cyanobacterial relatives have yet to be found. The study of cyanobacteria demonstrates the strength of sci- entific inquiry. Scientists follow paths that lead sometimes to unex- pected discoveries and sometimes to nowhere. But every line of inves- tigation adds to our knowledge. rococcus at sea have found staggering abundances in central oceanic gyres, where it can reach concentrations in excess of 100,000 cells in a milliliter of seawater. It may represent fully half the total photosynthetic production in these waters. Rough calculations, based on the surface area of the oceans and the abun- dance and distribution of Synechococcus and Prochlorococcus, suggest that these are the two most abundant organisms on Earth. Cyanobacteria continue to surprise Discoveries about cyanobacteria con- tinue. We recently isolated Crocosphncra, a new genus of dinitrogen-fixing cya- nobacteria, from the tropical Atlantic and Pacific Oceans. Surprisingly, these two-to-four-micrometer cells, which might otherwise occur in vast areas of the ocean, are relegated to the tropics by a quirk in their physiology: They cannot grow below 24°C(75°F). Scientists have also found Richelia, cyanobacteria with specialized cells for fixing dinitrogen that live inside single- celled marine plants, including some diatoms. (See "Revealing the Ocean's Invisible Abundance," page 64.) With Riclielia fixing dinitrogen for them, the diatoms form extensive blooms. Such symbiotic relationships between phyto- plankton and dinitrogen-fixing cyano- bacteria, once they can be successfully cultured, may be shown to play a sig- nificant role in the carbon and nitrogen cycles of the oceans. Clearly, cyanobacteria, which have been so central to life on Earth, will con- tinue to provide many new surprises, as scientists learn more about them. "ohn Waterbury grew up outside ot New York City and I spent summers sailing in Wellfleet, Mass. After graduat- ing from the University of Vermont with a degree in zoology, he faced the option of a tour ot duty in Vietnam or an otter to work with Stanley Watson at WHOI. The choice was both obvious and fortuitous. He spent four years working on nitri- fying bacteria before Watson persuaded Roger Stanier at the University of California, Berkeley, to take him on as a gradu- ate student. There he was drawn to cyanobacteria, a group that has remained the focus of his research ever since. Along the way, Stanier and his wife, a Parisian, moved to the Pasteur Institute in Paris. Waterbury tagged along, having finished his course work at Berkeley, to do his research in Paris. After three formative years there, with Ph.D. in hand, he headed back to Woods Hole, where he has been ever since. 16 Oceanus Magazine • Vol. 43, No. 2 • 2005 The Deeps of Time in the Depths of the Ocean Discoveries of unusual marine microbes are radically changing our views about the evolution of life BACTERIA Cyanobacteria Other bacteria By Andreas Teske, Associate Professor University of North Carolina at Chapel Hill and Katrina Edwards, Associate Scientist Marine Chemistry & Geochemistry Dept. Woods Hole Oceanographic Institution At the helm of the Endeavor, James Cook set sail from England in 1768. He rounded Cape Horn in January 1769, entering the vast, unexplored Pacific and Southern Oceans and opening up an entirely new vista on the world. Cook "added a hemisphere" to the body of European knowledge, said the naturalist Charles Dar- win. He discovered new Pacific islands and Aus- tralia. He found never- seen-before animal species and more than 1,000 exotic spe- cies of plants. In the 1830s, Darwin him- self sailed aboard the Beagle to the Galapagos Islands. The observations he made there of animal life spurred his theory of natural selection, which revolution- ized our understanding of the origin and evolution of species. Centuries after these classical voyages, we are making discoveries that are simi- larly shaking and expanding prevailing ideas about life on our planet. Once again we have embarked on voyages to explore remote, unknown areas of our planet — this time in, rather than on, the oceans. Wherever we have looked in the oceans, we have found previously un- known microorganisms. We have often found them living in conditions once thought to be incompatible with life, us- ing unfamiliar physiologic and metabolic adaptations. These discoveries have radically changed our think- Animate ing about where and how life EUKARYOTES Fungi Primitive ancestral cells A COMPLEX TREE OF LIFE— Microbes are living archives of Earth's evolutionary history. The discovery of a great variety of deep-sea microorganisms (using diverse metabolic strategies to live in diverse habitats) indicates that they evolved along different evolution- ary pathways. Using genetic analyses, scien- tists can trace these pathways to reconstruct when various microbial biochemical and metabolic machinery developed, diverged, or intermingled in the three major domains of life: bacteria, archaea, and eukaryotes. may have originated and evolved on this planet, and where it might exist on others. The seafloor and the rocky regions be- low it offer boundless new potential habi- tats to explore. With research submers- ibles, robotic vehicles, and new sampling tools and techniques, marine microbiologists are making discoveries at an unprece- dented rate. We are open- ing a wide window onto the immense, unexplored realm of the smallest, least- known, but most impor- tant life forms. We have entered the classical age of microbiology. Recent discoveries Without microorgan- isms, there would be no other life on Earth. Un- seen, ubiquitous, and uni- cellular, microorganisms nevertheless keep the planet running. Photosynthesizing plankton form the base of the marine food chain and keep the biosphere well oxygenated. At the other end of the cycle, other microbes decompose organic molecules for reuse. It was not until 1977 that we discov- ered cyanobacteria in the open ocean, which turn out to be among the most abundant and important bacteria on Earth. These bacteria were the photosyn- thetic pioneers responsible three billion years ago for infusing our planet's atmo- sphere with oxygen. (See "Little Things Matter A Lot," page 12.) Woods Hole Oceanographic Institution l. MICROBES IN MANY COLORS — Scientists have found a multitude of deep-sea microorganisms using a variety of chemical compounds to live. Yellow bacterial mats atop sediments in the Guaymas Basin in the Sea of California (left) are evidence of microbes that oxidize sulfide; the sediments underneath harbor methane-oxidizing archaea. The orange mats at right are made by microbes that live off iron in seafloor rocks near Hawaii. As recently as the mid-1970s, scientists believed there were only two domains of life on Earth: prokaryotes (single-celled bacteria, without nuclei or complex cellu- lar structures) and eukaryotes (organisms made of cells with nuclei, ranging from single-celled amoebae to all multicellu- lar life, including tungi, plants, reptiles, and mammals). Then in 1977, Carl Woese of the University ot Illinois identified a wholly new domain of single-celled life forms, called archaea, which are as genet- ically different from bacteria as bacteria are from trees and people. Archaea, or "ancient ones," have ex- isted for billions of years on Earth. Many are extremophiles that thrive in hot, cold, salty, acidic, oxygen-depleted, or other extreme environments. Such conditions prevailed on an adolescent Earth, before cyanobacteria evolved and fundamentally changed Earth's atmosphere. Life in unexpected places In the late 1970s, we also discovered microbial communities in the dark and high-pressure depths of the seafloor— living on superheated, acidic, sulfide-rich fluids emanating from hydrothermal vents. Since then, we have found microbes that thrive in polar ice, on ocean floor lava, buried beneath seafloor sediments, and in the rocky nooks beneath the sea- floor. They exploit a wide range of chemi- cal reactions, using hydrogen sulfide, iron compounds, nitrites, methane, and other chemical compounds to obtain energy and resources to grow. (See "Revealing the Ocean's Invisible Abundance," page 64.) This great variety of habitats and meta- bolic strategies indicates that microbes have taken a diversity of evolutionary pathways in the past. Ancient microbial lineages, which had their origin (and pos- sible heyday) when different biogeochemi- cal conditions prevailed on Earth, can survive today in diverse habitats that still exist in the mostly unknown deep subsur- face of oceans. These microbes are living archives of Earth's evolutionary history. The novel microbial lineages we are finding on Earth are also expanding and guiding our search tor lite that may ex- ist in the extreme environments on other planetary bodies. With our eyes opened wider to more possibilities, we can look for life in previously unsuspected places: in the iron-rich rocks of the red planet, Mars; beneath the ice-covered surface of Jupiter's volcanic moon, Europa; or on Titan, Sat- urn's moon, which now shows evidence of having liquid-methane lakes to go along with its methane-rich atmosphere. Portals into microspace Like Cook and Darwin, today's scien- tists collect specimens in remote places, but studying microorganisms pres- ents a new set of challenges. To study microbes, scientists need to keep them alive, but it is often hard to reproduce undersea conditions in the laboratory, and only some microbial species have been successfully cultured. Instead, microbiologists have exploit- ed modern genetic techniques to search for, identify, and study newly found microbes. They examine samples from deep-sea environments containing un- known species of microbes, locate gene sequences within them, and compare these sequences with those of known, cultured microbial species. An unknown organism in the wild can be identified — on the basis of how similar gene sequences are to those of known microbes— without scientists ever having to grow it in the laboratory. Fully half of the bacterial branches known to- day have never been cultured and have been identified only by gene sequences. Genomic investigations Gene sequences also allow scientists to trace microorganisms' evolutionary history. All microorganisms share some common genetic equipment, includ- ing certain genes, known as "conserved genes," which are the blueprints for basic biochemical functions. Mutations that change gene sequences accumulate in genes over evolutionary time, but this process occurs at a far slower rate in con- served genes than in other genes. Thus, conserved genes are similar in closely 18 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu related organisms and less similar in dis- tantly related ones. The greater the differ- ences in conserved genes shared by two organisms, the further back in time they diverged in evolutionary history. By analyzing the DNA of conserved genes, scientists can place microorgan- isms in evolutionary trees that encom- pass deep evolutionary time and chron- icle when various microbial biochemical and metabolic machinery developed and diverged. Surveying samples from marine environments, microbiologists are finding novel gene sequences from unknown organisms and accumulating libraries of gene sequences to reference newer discoveries. Little microbes that could At the same time, microbiologists are also extracting nucleic acids from mi- crobes to determine what protein prod- ucts the nucleic acids code for. By these means, we can find out something about what compounds and biochemical mech- anisms the microorganisms use to obtain energy and carbon to live and grow. In addition, microbiologists are ana- lyzing isotopes of elements incorporated into microbes during their metabolic pro- cesses. These not only provide more clues to learn about the microbes' biochemical machinery, they also reveal how the mi- crobes affect the rocks they live in, seawa- ter chemistry, and even the atmosphere. In 2000, for example, we tound'new species of microbes that live directly off minerals in seafloor rock. They oxidize iron in the rocks to obtain energy and convert carbon dioxide in seawater into organic matter to grow. If these previously unknown bacteria turn out to be as abundant as they seem to be, they may play a longstanding, im- portant role in Earth's climate by extract- ing huge amounts of the greenhouse gas carbon dioxide from seawater and keep- ing it out of the atmosphere (while pro- ducing up to a million tons of biomass). They may have changed the geology of the seafloor by changing the chemical composition of seafloor rocks. They may have been evolutionary pioneers on an iron-rich, oxygen-poor early Earth, or in- habitants of iron-rich, oxygen-poor plan- ets today, such as Mars. No oxygen, no problem Over the past tew years we have sampled and analyzed sediments in the Guaymas Basin in the Gulf of California, where hundreds of meters of sediments have piled on top of hydrothermal vents. We had expected to find the molecular signs of archaea adapted to high heat (hy- perthermophiles), which are well known at hydrothermal vents. But instead we found something com- pletely different — a major new type of ar- chaea, related to known methane-produc- ing archaea, or methanogens. We believe that the high geothermal heat emanating from the hydrothermal vent site is break- ing down organic matter in the sediments into short-chain fatty acids, ammonia, and more methane. Some of these compounds perco- late upward and are released from the sediments into the ocean — but not all ot them. In the sediments we also found isotopic and gene sequence signatures that reveal archaeal populations that use methane to grow in oxygen-free environ- ments, such as those beneath the Guay- mas sediments. The discovery of these anaerobic methanotrophs fills a large gap in our knowledge of Earth's microbial and geo- chemical cycles. Microbes that generate methane, and others that consume it, play crucial roles in minimizing how much methane— a greenhouse gas more potent than carbon dioxide— is released from the ocean to the atmosphere. These microorganisms complete a subsurface methane cycle that allows life to flourish at the seafloor, not only in the microbial oases of hydrothermal vent sites, but also in deep marine sediments and the subsurface biosphere. We are now exploring deep marine sediments in the Pacific to investigate whether this phe- nomenon is global. Though the pace of microbial discov- eries has increased, history warns us that we haven't seen everything yet. The book on microbial life, on Earth and elsewhere in the universe, is far from written. A . ' Scattering - ' • •-'•' I \ •' • J- ' :'2: 7 •"''.:..' '" '"'' Water Molecules —:jv Vy Panicles Light hitting a substance can scatter in all directions. Woods Hole Oceanographic Institution .• Adaptations to light, from surface to depths The dark backs and light undersides of these near-surface fish help them match their environment in the open ocean. To a predator looking from above, their dark backs seem to blend into the dark depths. From theside, their lighter sides blend with the sunlit water. Many open ocean animals use invisibility to hide in plain view. Adapted to limitless, featureless blue surroundings, this plankton ic ctenophore, Cestum, lives near the ocean surface. The complete transparency of its body makes it almost impossible to see against the open ocean waters. The hatchet fish is well prepared for the midwater ocean's light levels. Bright silver sides reflect whatever light surrounds it. Long, tubular eyes capture and detect low light levels. Living at depths from 200 to 1000 meters, it has ventral (underside) light organs that can produce bioluminescence to match light coming from above, making it less visible from below. With enormous upward-looking eyes that fill half its otherwise transparent body, the deep-living shrimplike amphipod Cystisoma is well-suited to its dim world. It needs such large eyes to detect the little light available in its midwater environment (800 meters). At that depth, red eyes appear black — and invisible. Atolla is a jellyfish common from midwater, about 500 meters deep — where there is still a small amount of sunlight, to depths of 4,500 meters — far below the limit of sunlight's penetration. Where there is light, its red color looks black, making it hard to see. It also produces brilliant bioluminescence, possibly to frighten predators. in the ocean. If water were not relatively transparent to this light, aquatic photosynthesis would not be possible, and the ocean would be largely a dead zone. In addition, if coastal waters be- come less clear because of human activi- ties, photosynthesis by phytoplankton may decrease. Phytoplankton form the base of the prolific marine food chain, which ulti- mately also helps feed people and other terrestrial life. Throughout Earth's his- tory, phytoplankton have also played an important role in regulating Earth's climate. They remove huge amounts of the greenhouse gas carbon dioxide from the atmosphere, turning it into organic matter via photosynthesis. Much of this organic carbon is consumed by animals in upper ocean waters. Some fails to the seafloor, as dead organisms or fecal pel- lets, where it is consumed or converted over time into oil and gas deposits. The threat of UV radiation Marine photosynthesis is confined to the tiny fraction ot ocean where sunlight penetrates — at most, the upper 200 me- ters. UV light also penetrates this region, which may have increasingly profound consequences. UV radiation can cause damage to organisms on both land and sea. Recently, scientists have discovered that ultraviolet radiation can harm or- ganisms deeper than previously thought. Decreasing ozone levels in the atmo- sphere, including the ozone hole over Antarctica, may exacerbate the problem, because ozone blocks UV radiation from reaching Earth. Higher levels of UV can kill phytoplankton, slow their growth, or disrupt the delicate balance of species that interact in ocean ecosystems. Marine organisms have evolved ways to protect themselves from UV. These in- clude UV-absorbing pigments, the ability to repair UV-damaged DNA, and devel- oping behavior to avoid UV by staying in deeper water. However, the recent ozone changes may be occurring too fast for organisms to adapt. Given the tundamen- 26 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu tal role of phytoplankton in Earth's biolo- gy, chemistry, and climate, these changes may affect us all. Into the darker depths As our diver continues to descend a tew more meters, she begins to go from day to night. She can see blue light to her sides, and white light above, but below her the view is dark. As she moves down- ward, the UV, green, and violet wave- lengths disappear, and the light becomes an intense, almost laser-like, pure blue. At 200 meters deep, the diver would cross from the surface realm (called the epipelagic zone), where there is enough sunlight tor photosynthesis, to the twi- light realm (called the mesopelagic zone), where enough sunlight penetrates for vi- sion, but not tor photosynthesis. By now, our descending diver would notice nearly continuous blue flashes around her — bioluminescent light pro- duced by animals in the midwater zone, in response to the disturbance in the water that she caused. Below 850 meters, though, the diver would no longer be able to see anything, even looking up. Human eyes aren't sensitive enough to detect the minute amounts of sunlight that haven't been absorbed by the water. At 1,000 meters, even the most visually sensitive deep-sea animals can no lon- ger see the sun. The region below this is known as the aphotic (no-light) zone, but this is only true for sunlight, as bio- luminescence is common. Predators — using light to hunt Not surprisingly, aquatic animals possess visual systems that are specially adapted to the nature and properties of light underwater. Animals living near well-lit surface regions have eyes similar to terrestrial species. They have color vision, since light near the surface still has color. Many also have UV vision, which ad- vantageously extends their range of vi- sion. Many animals contain compounds in their tissues that protect them against UV radiation by scattering, reflecting, or absorbing UV light. This makes the animals appear dark and silhouetted against an otherwise bright background of UV light. With UV vision, animals can see animals that are transparent in visible light. Some ocean animals, such as shrimp and squid, can even see the polarization of underwater light — due to a special geo- metric arrangement of their retinas. With this ability, they can actually navigate by the skylight polarization pattern, or detect otherwise transparent, or silvery- scaled prey by seeing its effect on the po- larization of light. In deeper, mesopelagic regions with less light, the animals often have bizarre adaptations to increase their visual sensi- tivity. They see in extremely low light lev- els, though at the expense of acuity, with a reduced ability to detect rapid move- ments. Long, tubular, telescope eyes in fish, or enormous crustacean eyes that till the animal's entire head capture as much light as possible. Prey — using light to camouflage But seeing is only part of the equation. Ocean organisms' visual adaptations are matched by clever strategies to avoid being seen in an open ocean where it is difficult to hide. Some color themselves to match the background water. Others have mirrored sides, because a mirror in the ocean only reflects more of the ocean, and so is invisible. Still others camouflage themselves with light, hiding their silhouettes with light-producing organs on their down- ward-facing surfaces that mimic the sur- rounding illumination. Many are simply transparent, matching their background in all situations. Finally, some use light and dark for The advantage ofUV vision shows in reef views in visible (left) and ultraviolet (right) light. In UV light, the fish are in much higher contrast to the background. Prey species such as the copepod Labidocera are nearly transparent in visible light (left), but they are brightly visible when photographed in polarized light (right), or to a predator that can see polarization of light. Woods Hole Oceanographic Institution 27 disguise. They hide in the depths during the day, rising to feed at night, or they stay near the surface, hiding in the glit- tering background of the lensing waves. Instruments to measure light To study light in the sea, scientists use a wide range of instruments — sub- merged in the depths and sent into space. Submersible radiometers, or light meters, measure ultraviolet and visible light and detect extremely low light levels in the deep sea. They numerically describe the shape of the light field in the ocean and measure how light is absorbed and scat- tered in water over small spatial scales. They can be lowered from ships, placed on submersible vehicles, or even carried by scuba divers to investigate the optical environment of specific areas or depths. One of the most exciting advances in oceanography has been the developing ability to measure changing color over wide swaths of the ocean, using Earth-orbiting satellites that carry spectral radiometers that measure light reflected from the surface of the ocean. These color changes indicate changes in the global distribution of phytoplank- ton. For the first time, oceanographers can see how phytoplankton populations bloom, collapse, and change over time in any area, and these satellite views have revolutionized how we think about the upper ocean. A bright future Despite continually improving satel- lite data, optical oceanographers still have too few observations. Satellites view only the upper few meters of the water. With underwater instruments, we can sample only relatively few specific places and times in the ocean. What's lacking is a way to visualize the entire ocean — sur- face to depths and across the globe. Computer models otter a way to ap- proach this deficit. Combining available observations with new, accurate comput- er model :hat simulate how light behaves and propagates through the ocean has led DIVING INTO DIFFERENT WORLDS — Open ocean water (left) contains few particles and absorbs warm colors, so blue light penetrates far into the clear distance. Near the coast, high nutrient levels allow dense growth of phytoplankton (center), making the water appear green and darker (right). Forests appear dark and green for the same reason — plant pigments absorb red and blue wavelengths of light and reflect remaining green light. to insights on satellite-based ocean color measurements, global phytoplankton productivity, and how marine animals use light and camouflage. The door is now open to answering questions about the operation of light in the ocean, and its role in the lives ot ma- rine phytoplankton and animals. We are gaining new understanding of this hereto- fore shadowy — but not lightless — realm. Sonke Johnsen entered biology with backgrounds in math, phys- ics, and art and has since used all three fields to investigate the visual ecology of oceanic zooplankton. After a frustrating graduate career, in which he studied the vision and behavior of animals with neither eyes nor brains, he completed postdoctoral fellowships at Harbor Branch Oceanographic Institution and WHOI. After a year l« as an assistant scientist at WHOI, he accepted a position in the Bi- ology Department at Duke University. He is interested in all aspects of vision in oceanic species, with a particular emphasis on strategies for camouflage. The camouflage research has involved investigations into UV vision, whole-body transparency, cryptic coloration, and counterillumi- nation using techniques ranging from blue-water diving to protein biochemistry to Monte Carlo modeling of photon trajectories. He gives numerous talks to the general public and his work has been featured in newspapers, magazines, and a John Updike poem. Heidi Sosik received bachelor and master of science degrees in i i Civil and Environmental Engineering from MIT in 1988 and a doctorate in oceanography from Scripps Institution of Oceanography in 1993. She joined the Woods Hole Oceanographic Institution as a postdoctoral scholar in 1993 and is now an asso- ciate scientist in the Biology Department. Her research interests focus on phytoplankton ecology and factors that influence light in the marine environment. She received a Presidential Early Ca- reer Award for Scientists and Engineers in 1996 and is currently a joint Fellow of WHOI's Ocean Life Institute and Coastal Ocean Institute. "Never a dull moment" is an apt description of life for Heidi, whose family— one husband, three kids, two dogs, and a cat— keep her keel even and her sails full through the ups and downs ot a career as an oceanographer. 28 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Whither the North Atlantic Right Whale? Researchers explore many facets of whales' lives to help a species on the edge of extinction Michael Moore, Research Specialist Biology Department Woods Hole Oceanographic Institution For millions of years, the North At- lantic Ocean has been home to right whales. In winter, they gave birth to calves off the shores of West Africa in the eastern Atlantic and oft Florida and Georgia in the western Atlantic. In the spring, they migrated north along the coasts as far as the Gulf of St. Lawrence and the seas north of Iceland to feed in plankton-rich northern waters in sum- mer and fall. In 1150 King Sancho the Wise granted privileges to Navarre, a Basque province in northern Spain, to charge a duty on whalebone. So began centuries of whale hunting in which tens of thousands of right whales on both sides of the Atlantic were killed. Today only a remnant of the popula- tion survives, no more than 350 whales clustered in calving and feeding grounds along the eastern seaboard of North America. Only occasional right whale sightings in the Gulf of St. Lawrence or in the waters between Iceland, Greenland, and Norway give echoes of their once substantially greater range. To help a vulnerable population Since whaling ceased in the 1930s, related and similarly decimated species, such as the Southern Ocean right whale, have demonstrated spectacular recover- ies. However, the North Atlantic right whale population has not rebounded. Too few are being born. Too many are dying — often in accidents induced by hu- man activities such as shipping and fish- ing. In 1999, a study by Hal Caswell of Woods Hole Oceanographic Institution, Solange Brault of the University of Mas- sachusetts, and then-MIT/WHOI gradu- ate student Masami Fujiwara warned that unless this dire trend is reversed, the spe- cies is headed toward extinction. But to know how to help this dwin- dling population, we need to know much more about the factors preventing its recovery. We need to learn much more about the lives of whales, whose vast watery domain has made them far more difficult and inaccessible to study than terrestrial animals. Slaughtered over centuries Right whales dwell along coastlines, which has always made them convenient and vulnerable to whalers. The Basques were granted the right to levy a tax on whale products and began hunting them in 1150. They continued for nearly 600 years. By the 1500s, Basque whalers had exterminated the right whale population on th eastern side of the North Atlantic Ocean, and too few whales remained for worth- while hunting. In the latter part of the 16th century, they expanded their hunting grounds westward, particularly to the waters off southern Labrador. Then New England shore-based whalers took over, seeking oil and baleen for en- ergy and commercial products. Their catches peaked in the early 1700s, but high-sea Yankee whalers continued to pursue this species whenever opportunity afforded. Even into the 20th century, right whales were hunted near Iceland and Scotland. The last animals to be taken intentionally were a mother and calf off Madiera in 1967, although they had been protected from hunting since 1935. Woods Hole Oceanographic Institution Lower Bay of Fundy Summer/Fall North Atlantic right w Cape Cod and Massachusetts Bays irfaisry routes winter/spring , Southwestern / Scotian Shelf Great South Summer/Fall Channel Spring/Summer , Calving Grounds Now researchers are working to- gether, using a variety of new techniques and instruments, to study the whales' habitats, health, physiology, endocrinol- ogy, and genetics; their mating, feeding, and diving behaviors; their migration patterns and routes; their response to sounds, and their population changes over time. This basic knowledge can provide the foundation to devise ef- ficient and effective management and conservation strategies that can enhance the species' chances of survival. Too many deaths A critical factor in the North Atlan- tic right whale's decline is human-in- duced mortality, caused by collisions with ships and by entanglement in fish- ing gea nl ike the recovering South- ern Oce jht whale population, which >s populated and trafficked w North Atlantic right whales are exposed to gauntlets. The right whales' north-south mi- gration between calving and feeding grounds sets up a dangerous intersection with intensive east-west shipping traf- fic through many of the world's busiest ports on the North American East Coast. Resulting collisions cause fatal trauma to whales, including propeller lacerations and fractured jaws, brain cases, ribs, and vertebrae. Ship collisions kill an average of two North Atlantic right whales per year, though more undocumented fatali- ties probably occur. East Coast waters are also prime fish- ing grounds. Right whales run into fixed lobster, crab, and other trap fishery gear, and anchored gill nets. They get fish- ing lines around their tails, flippers, or in the worst-case scenario, through their baleen plates as they filter water for long periods with their mouths open. As they struggle, the whales' flippers, bodies, and tail stocks can get wrapped in ever tighter circles. Many right whales can tree them- selves from less severe entanglements, but others can't. They may die rapidly, or swim for months with the gear attached, only to die several months later. Swimming in traffic Reducing collisions between ships and whales is enormously difficult. At times, right whales appear to be unable to de- tect, or at least to avoid, large ships. We don't know as much as we need to about the physiology of whales' ears and what they can hear. At WHOI, scientists Darlene Ketten and Susan Parks have done seminal re- search on right whale hearing. (See "How to See What Whales Hear," page 59.) To investigate the behavior of right whales in response to noise, WHOI biologist Peter Tyack and his colleagues have developed sophisticated digital, suction-cupped tags that can be placed temporarily and harm- lessly on the whales. (See "Run Deep, But Not Silent," page 54, and "Playing Tag with Whales," page 57.) The tags record the whales' diving, surfacing, and swim- ming movements in response to ships, natural noises, and alarm stimuli — the latter in the hope that some system to warn whales of approaching ships could be developed. Are the whales so habituated to ubiq- uitous ship noise that they don't distin- guish ships? Do ships exert hydrody- namic forces as they travel through water, which the whales are unable to evade? More research must be done to answer these fundamental questions. There has been one significant re- cent advance in the effort to reduce ship strikes. Moira Brown of the New Eng- land Aquarium (NEAq) in Boston, and a group of collaborators from industry, science, and government in Canada, have made it possible to relocate a major ship- ping lane away from a prime right whale habitat in the Bay of Fundy. In addition, efforts have begun to educate interna- tional maritime professionals to the risk 30 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edi of whale-ship strikes, and ships traveling in right whale habitats in U.S. waters are now required to report whenever they are transiting such waters. Lethal entanglements There are only two ways to mitigate the fishing gear problem: reduce the number of whales entangled or disentan- gle animals seen trailing fishing gear. Disentanglement efforts, led by the Provincetown Center for Coastal Studies (PCCS), have at times been spectacular but will never be a solution. Numerous animals have been successfully disentan- gled, using modified small-boat whaling methods to slow down the animals and make strategic cuts in entangling gear. But despite heroic efforts and the devel- opment of physical and chemical restraint systems, a significant number of cases have been intractable: The whales were impossible to free, and they died. Even the best disentanglement tech- nique will never remove the ongoing flow of new cases. Many of these are only evident in new rope scars on previously unscarred individuals. Avoiding entan- glement is the true solution and a critical current research focus. Researchers in academia, govern- ment, and industry are all seeking modi- fications to fishing gear that attempt to decrease or eliminate entanglement. These include developing weak links in fixed fishing gear so that lines break rather than obstruct a colliding whale, and changing the buoyancy of lines to reduce their exposure in areas where whales dive. Other potential modifica- tions include gear with less friction to re- duce abrasion and laceration with whale flesh, and with better visibility, so that whales have a better chance of avoiding them. Some seasonal fishing regulations have also been established with the aim of minimizing encounters between right whales and fixed fishing gear. None of these efforts has yet decreased the mortality rate. Most are controversial because commercial fishermen question Scientists distinguish individual right whales by black horny protuberances on their heads, called callosities, which are highlighted by intensely colored whale lice. Distinguishing a "face" in a crowd We know how many North Atlantic right whales exist, where they go, and even the life histories of individuals in the population because of four decades of research. This has included extensive efforts to photograph the population in boats and airplanes, and painstak- ing record-keeping. WHOI biologists Bill Schevill and Bill Watkins launched modern-day studies of the North Atlantic right whale popu- lation in the 1960s with aerial surveys of whales in Vineyard Sound, Cape Cod Bay, and the Great South Channel off Nan- tucket. They and other whale research pioneers began to dis- tinguish individuals by using distinctive, black horny protuber- ances, called callosities, on the whales' heads. The callosities are highlighted by intensely colored whale lice. Photographs of callosity patterns and other distinctive body scars allow us to recognize individuals. Over the past 25 years, colleagues at the New Eng- land Aquarium and the University of Rhode Island, led by Scott Kraus and Bob Kenney, have catalogued right whale sightings from a broad consor- tium of institutions and individuals to build uniquely detailed databases that include individual histories for the majority of whales in the remain- ing population. These databases include infor- mation on individual whale sight- ings, feeding, calving, toxic chemical exposure, genetics, and deaths. This shared database provides researchers with essential, fundamental informa- tion that undergirds most ongoing North Atlantic right whale research. Like fingerprints, callosity patterns (in drawing above and real life below) give researchers the ability to identify and keep track of the life histories and movements of individual whales. Woods Hole Oceanographic Institution 31 the value of required changes and the se- lection of restricted fishing areas. Too few births Part of the shortfall of North Atlan- tic right whale population growth is a reproductive failure: Not enough calves are born. Over recent decades, researchers have observed several disturbing trends: Ma- ture females are having a declining num- ber of calves. About 25 percent of mature females have never been sighted with calves. The age at which females have their first calt appears to be increasing. Inter- vals between pregnancies have increased. Overall, the species' calving rate is about one-third what it should be, which is all the more distressing in an already small population subjected to other stresses. Once again, the inherent difficulties of tracking, monitoring, and sampling such large animals over a vast, remote region has limited our ability to understand why the North Atlantic right whale reproduc- tion is so inconsistent. Suspected, and probably interrelated, causes include dis- ease, pollutants, and poor food supplies. Only recently, Rosalind Rolland at NEAq and colleagues have developed pio- neering techniques to analyze whale fecal samples to obtain previously unobtain- able biomedical data on whales. These are providing a novel, non-invasive window to reveal the whales' genetic makeup and their levels of contaminants and hor- mones (both reproductive and stress). These biomedical data, along with other studies of whale body conditions and nutrition, will help assess the myriad factors that may be compromising right whales' health and ability to reproduce. Recent studies by my colleague Carolyn Miller and me, for example, indicate that Southern Ocean right whales may have higher birth rates than their northern cousins because they have better food re- sources and higher body fat reserves. Protecting feeding grounds The issue of nutrition leads directly to questions ot whale food supplies: Where are they and how might they be protected? Much of the research and manage- ment of North Atlantic right whales in U.S. waters today is driven by the federal Endangered Species Act and the Marine Mammal Protection Act. Independent, federal, and state agencies currently carry out large-scale annual surveys to count right whales and find where they go in which season. The surveys show year-to-year varia- tion in the whales' travel patterns, which scientists think are governed by differ- ences in food availability. Whales, like other animals, follow their food. They teed on dense patches of zooplankton, especially small crustaceans called co- pepods. They strain mouthfuls of water through a fibrous filter in their mouths, known as baleen, which retains copepods that the whales swallow. Right whales today feed in the Great South Channel, Cape Cod Bay, the Bay of Fundy, and the banks south ot Nova Sco- tia. But there must also be other important feeding areas of which we are unaware. Stormy Mayo of PCCS has demon- strated a critical need for conserving hab- itats where copepod patches are dense, such as in Cape Cod Bay in the winter and early spring. The location of these patches is probably determined by myriad factors: local phytoplankton productiv- ity, the presence of other copepod preda- tors, local oceanographic features, such as water temperatures and fronts separating different water masses — all of which may, in turn, be affected by climate changes II jj «• $ •5 £ S 1 « 818 4j C ~ LIBERATING LEVI -A rescue team from the Provincetown Center for Coastal Studies attempts to free a right whale with fishing lines wrapped around it. Fishing gear entanglements kill a significant number of North Atlantic right whales. "la 32 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu GENERATIONS NOT FORTHCOMING — Fewer new North Atlantic right whale calves are being born, threatening the species' ability to survive. Scientists seek to understand the reasons for their low and inconsistent birth rate, which may be linked to pollution or declining food supplies. from year to year, or over decades. WHOI biologist Mark Baumgartner and colleagues have begun to explore the factors that govern where, when, and why whale prey aggregates. Using tags and sensors, they have been collecting and correlating data on copepod abundances, oceanographic conditions, and whale feeding and diving behaviors. This fun- damental knowledge on whale habitats is an essential first step to devise strategies to manage and protect them. "Whale-safe" consumer products Current and planned research at WHOI and elsewhere is aimed at several research fronts. (See "Scientists Muster to Help Right Whales," page 34.) Seek- ing ways to reduce human-caused deaths, researchers are analyzing the factors that prevent right whales from avoiding ships, and they are working to develop whale- friendly fixed fishing gear. They are gain- ing better understanding of the role of nutrition, chemical exposure, and infec- tious agents in reproductive success. And they are using computer models of right whale demographics to pinpoint the most critical factors, among many, that threat- en the species' survival. This information. in turn, helps identify the most effective conservation strategies. Will all this effort result in saving the North Atlantic right whale? Possibly. It depends largely upon our society's will to do what it takes to reduce human-in- duced whale deaths. This will involve very hard decisions. Major maritime in- dustries will have to alter their practices in a way that our consumer-driven soci- ety is loath to allow. An important and successful model to follow is that of the tuna fishery in the eastern tropical Pacific in recent de- cades. Tuna fishers used to target tuna by setting their nets around groups of dolphins. Overwhelming public opin- ion against this practice made the cost of "dolphin-safe" tuna acceptable. If we can develop the same willingness to pay for right-whale-safe shipping and fishing practices, then the North Atlantic- right whale has a chance to survive. The job facing the science and engineering community is to develop the tools and knowledge necessary to enable a "whale- safe" stamp on all lobster claw bands and other fishing products and on products shipped in containers and tankers to North Atlantic ports. It's a Herculean task, and it could lead to much higher consumer costs. But the alternative is acceptance that humans exterminated a great species that plays powerful roles in human history and the natural history of the ocean. Michael Moore grew up in England, where he trained as a veteri- narian. He began his career as a marine mammalogist, concur- rently in Newfoundland and the Caribbean. Moore then pursued his wife-to-be, Hannah, back to her New England home. He spent two years acquiring U.S. veterinary licenses, before gravitating to Woods Hole in 1985, where he was first at the Marine Biological Laboratory and then at WHOI. As a WHOI/MIT Joint Program student in the laboratory of John Stegeman in the Biology Department, his research first focused on tumors in flatfish exposed to Boston Harbor sewage. His interest therein endures, but since becoming a research specialist at WHOI, it has expanded to encompass other man-made impacts on marine vertebrates such as right whales and other marine mammals. He is also the vet- erinarian for the Cape Cod Stranding Network, which responds to single and mass strandings of marine mammals on Cape Cod. Woods Hole Oceanographic Institution .' Scientists Muster to Help Right Whales With time running out, an ambitious research plan is launched for an endangered species Laurence Madin, Director Ocean Life Institute Senior Scientist, Biology Department Woods Hole Oceanographic Institution It is a sad irony that we have cataloged individual photographs of the remain- ing North Atlantic right whales and given each of them unique numbers and some- times names, yet we still know too little about their physiology, behavior, and habitats to take effective steps toward en- suring their survival as a species. Rapaciously hunted by humans over centuries, the North Atlantic right whale has not recovered in the decades after whaling was outlawed. Living near heavily populated coasts, the whales are vulnerable to high levels of ship- ping, fishing, noise, and pollution. (See "Whither the North Atlantic Right Whale? page 29.) Today, right whales lie at a critical crossroads in their long history — pointed dangerously toward extinction by the end of the century. Now, an ambitious pro- gram of intensified research has begun finding ways to aid them. A species on the edge We now know that the mission is pos- sible. Using extensive right whale data collected by government agencies, re- searchers, and dedicated private groups, WHOI biologist Hal Caswell and col- leagues analyzed the factors contributing to the species' population decline. Saving just two females per year from untimely death, they concluded, can reverse the downward trend and put the population on a road to recovery. But despite years ot research on right whale habits and habitats, we still lack practical ways to reduce deaths or in- crease births. Learning the secrets of huge and uncooperative animals that can be studied only fleetingly at sea or dead on a beach is a daunting task. In November 2003, the WHOI Ocean Life Institute (OLI) convened a research forum in Woods Hole, gathering scien- tists and engineers from several institu- tions, along with representatives from government and industry, to assess the status of the North Atlantic right whale. Blending a diverse range of complemen- tary expertise, they devised a collabora- tive research plan to accelerate advances in our knowledge of right whales. The OLI Right Whale Research and Con- servation Initiative complements other government and academic programs, supplying essential pieces of the North Atlantic right whale puzzle they don't address. It will provide a necessary sci- entific foundation to guide effective con- servation efforts. A DIVE TO SURVIVE — A North Atlantic right whale dives in search of food near Grand Manan Island in the Bay ofFundy, Canada. 34 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edi HIT BY A SHIP— A necropsy of this 50-ton, 45-foot right whale, washed onto a beach in Wellfleet, Mass., in 7 999, showed a broken jaw, fractured vertebrae, and internal bleeding. The whale, known to researchers as Staccato, had given birth to many calves. Research has shown that saving just two mature females per year from untimely deaths could reverse the decline of the North Atlantic right whale population. Joining forces Over the next several years, scientists from WHOI, the New England Aquari- um in Boston, the Provincetown Center for Coastal Studies, Trent University in Canada, and other institutions will join in the OLI Right Whale Research and Conservation Initiative. They are plan- ning, launching, and seeking funds for a variety of studies aimed at: • reducing accidental whale deaths caused by ship collisions and fishing gear entanglement • understanding critical factors affect- ing right whale habitats, nutrition, re- production, and health • monitoring the North Atlantic right whale population to assess its size, present state, and future viability. Right Whale Initiative strategies in- clude pioneering studies of whale hearing, using CT scans to obtain physiological data on whale ears (See "How to See What Whales Hear," page 59), and field work to study whales' response to noise. Other scientists will use whale bone forensics to provide basic information on the speeds and masses of vessels that are unvolved in fatal ship-whale collisions. Another study will explore hydrodynamic forces, caused by ships moving through water, that lead to collisions. Scientists will also test new types of fishing gear designed to slip off more easily and break when entangled whales try to free themselves. A remote con- trol device is being developed to deliver sedatives and medications to entangled whales, to improve our ability to disen- tangle them. A multi-pronged research effort Over the long term, the critical threat to right whales is their low and incon- sistent birth rate, which could be linked to pollutants or to poor nutrition. The latter, in turn, may be caused by shifts in food supplies linked to changing oceano- graphic or climate conditions. The OLI Initiative includes research to: • analyze whale fecal samples to get pre- viously unobtainable data on whale genetics, and hormone and contami- nant levels • conduct detailed studies on the effects of chemical pollutants and nutrition on whale health and reproduction • develop new technology to monitor conditions in whale feeding grounds • learn why whale feeding grounds exist where they do and how they change with changing oceanographic and cli- matic conditions • deploy rapid-response expeditions to explore whale feeding and diving behavior. Tracking the population To monitor the whale population more effectively, the OLI Right Whale Initiative includes: • expeditions to recover and analyze whale bones left behind from 16th- century whaling to help determine the North Atlantic right whale population's pre-whaling size and genetic diversity • new aerial surveys using high-defini- tion camera systems that provide more detailed information on whale condi- tions and behaviors • development of comprehensive data- bases to share right whale information more widely and quickly • modeling studies to target critical fac- tors threatening the population and more effective conservation strategies. Time is running short for the North Atlantic right whale. Now is the time for scientists and supporters to work together to keep this magnificent mammal swim- ming off our shores. Woods Hole Oceanographic Institution 35 The Secret Lives of Fish Scientists learn to read the 'diary' recorded in the ear bones of fish By Simon Thorrold, Associate Scientist Biology Department, and Anne Cohen, Research Associate Geology & Geophysics Department Woods HoleOceanographic Institution The ocean's once-abundant fisheries — a resource that helps feed the world and drives multi-billion-dollar economies — are rapidly being depleted. Seventy percent ot the ocean's fish are being fished at or above catch limits that would sustain the fish stocks, according to a recent report by the National Research Council. This dismal situation has led to calls for Marine Protected Areas (MPAs) — ar- eas completely closed to fishing — as a means to protect both fish stocks and the environments they inhabit. Instead of trying to manage single species in isola- tion, the idea is to manage and preserve whole ecosystems. (See "Do Marine Pro- tected Areas Really Work?" page 42.) But which areas should we designate to protect fish stocks most effectively? To make these decisions, we need to know details about fish life cycles, movements, and migrations. Unfortunately, large gaps remain in our knowledge about the secret lives offish. Following fish in a vast ocean On land, the task is much easier. To learn about movements of terrestrial animals, researchers usually conduct tag-recapture studies. They place tags on a number ot animals, release them, and LAYERED LOOK — Simon Thorrold examines a magnified otolith (ear bone) of a weakfish. Dark and light lines are alternating layers of calcium carbonate and protein, secreted as layers, which can be detected as annual, or even daily, rings. 36 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu then keep track of where the tagged ani- mals were released and where they were found at later times. Such studies are difficult in marine environments. Larval fish, generally only 5 millimeters or less in size, are too small to tag. In addition, fish typically lay mil- lions ot eggs, ot which 99.9% do not sur- vive. Even it we could tag hatchlings, we would lose nearly all of our study subjects before they reached adulthood. Consequently, fisheries scientists have no way to know where an adult haddock caught on Georges Bank was spawned, or the location of the nursery area where it spent its adolescence, or the likelihood that it would return as an adult to spawn in the same place. Yet, this is exactly the information about fish species that we need to select and design MPAs that will effectively conserve and replenish fish populations. Their ears can tell tales Our recent research points to a prom- ising new way to reveal where and how fish live their lives. Within all fish are ear bones, called otoliths. They grow throughout each fish's life, adding annual rings, similar to the growth rings in trees. For more than a century, biologists have used otoliths to estimate fish's ages. But otoliths may be able to tell us far more. Otoliths consist of alternating layers of calcium carbonate and pro- tein, which are deposited in daily incre- ments. Through a complicated process, the chemical composition of the calcium carbonate is influenced by the chemi- cal composition and temperature of the water the fish inhabit. If a fish swims into waters with different chemical or physical properties, those differences will be re- corded chemically in its otoliths. In other words, the otoliths can tell us where the fish has been. And be- cause otolith layers remain unchanged once they are deposited, they can tell us when the fish was there. In addition, in some fish species, the width of each daily growth increment in the otoliths Peconic Returning home to spawn Delaware Bay Chesapea Bay Doboy Sound, Pamlico Sound, NC The weakfish,Cynosc\on regalis Scientists analyzed the chemical compositions of otoliths of spawning weakfish caught in five estuaries to determine the estuary where they hatched. The small graphs show the percentage offish caught in each estuary and where they hatched. The results indicate that most fish returned to their natal estuary to spawn. can be correlated with the growth rate of the fish. Keys to unlock the 'black box' In many ways, otoliths can be thought of as the fish-equivalent of an airplane's flight data recorder. They are continually logging information about the growth and health of the fish and about the water it swims in. Since otoliths begin to grow just before or after hatching, the entire lite history ot individual fish is available to be read, albeit in code. Unfortunately, accessing informa- tion from flight data recorders is sim- pler than retrieving it from the otolith "black box." Scientists can determine the chemical composition of samples taken from many calcium structures, such as coral skeletons or clamshells, bv using a mass spectrometer. This instrument sorts individual elements within a sample ac- cording to their mass and measures the amounts of each. But such analyses generally require fairly large amounts of material. Each day, fish deposit only an extremely thin layer of otolith — about 10 micrometers (0.0004 inches) in width. Most mass spec- trometers cannot be used on such small sampling scales. To determine the chemical composi- tion ot daily growth increments, scien- tists need to analyze thin (5- to 10-mi- crometer) sections of otoliths. To analyze these thin sections, they require special types of mass spectrometers that use mi- crobeams of ions or laser probes. Scientists are fortunate to have access to such state-of-the-art mass spectrom- Woods Hole Oceanographic Institution " Tiny otoliths (like this one from a snapper fish) provide large amounts of information about the life histories offish. eters, including the Northeast National Ion Microprobe Facility (NNIMF) and the Plasma Induced Multi-Collector Mass Spectrometer (PIMMS) facility, located at Woods Hole Oceanographic Institution. These provide precise measurements of minute quantities of trace elements and isotopes in thin sections of the otoliths. These measurements give us the ability to discern small differences in chemical composition that occur within time peri- ods as short as days. Cracking the chemical code Once collected, the data are still dif- ficult to interpret. When otoliths form, they are surrounded by the fish's internal fluids. These fluids are separated from the ambient water on the other side of the fish's scales. So the possibility has existed that otolith chemistry has no relationship to the chemistry of the ambient seawater outside the fish. Our research shows evidence, how- ever, that chemistry of the water the fish swims in does indeed influence the chemical composition of its otoliths. We demonstrated in the laboratory that for at least two elements, barium and stron- tium, there is a direct, linear relation- ship between concentrations of these elements in the ambient water and in the otoliths. This may hold true for other el- ements, too. If the properties of ambient water do influence the chemical composition of the otoliths on a daily basis, can we use the variations in composition as natural records of a fish's hatching location and subsequent travels? A treasure trove of fish data We have recently shown that we can do so with a natural, wild population of weakfish (Cynoscion regalis). Currently, these fish are managed as if they are a single population along the whole U.S. East Coast. That is because weakfish liv- ing from Florida to Maine show no genet- ic differences. Weakfish are an important commercial and recreational species that hatch in estuaries, spend their adulthood near the bottom in coastal waters, and re- turn to estuaries to spawn. Juvenile weaktish, however, hatch in each of five different East Coast estuar- ies. They are Doboy Sound, Ga.; Pamlico Sound, N.C., Chesapeake Bay, Va.; Dela- ware Bay, Del.; and Peconic Bay, near the end of Long Island, N.Y. We have found that otoliths offish born in each of the five natal estuaries had different, unique isotope and element com- positions, or "signatures." All their lives, these fish had carried a natural tag, encod- ing the location where they were hatched. We then analyzed otolith cores (the first portions deposited by hatchlings) from adult fish in those estuaries, and we found that most adult tish were returning to their birthplaces to reproduce — not randomly to any of the five possible na- tal estuaries. Knowing this means that protecting just one or two natal estuaries might not be sufficient to maintain the fish stocks. We now believe that fish otoliths are a rich source of demographic information for fisheries scientists all over the world. At least one million otoliths are sectioned in laboratories every year, primarily to determine the fish's ages. Now we know that annual and daily growth increments in otoliths contain significantly more information about the lives offish than simply their age. Chemical signatures in the otoliths offer the potential to reveal where and when a fish traveled through- out its life. The development of techniques for decoding this otolith archive gives us a powerful new tool to help manage fish- eries resources. If we know where fish hatch and travel, and where the spawning adults originate, fisheries managers will be better able to choose the most effec- tive locations to site MPAs and to restrict fishing— to protect the world's diminish- ing fish resources. Simon Thorrold (right) received a B.S. from the University of Auckland and Ph.D. from James Cook University, North Queensland, Australia. From o his birthplace in New Zealand, he has traveled far across the Pacific to the Caribbean Marine Research Center, Old Dominion University in Virginia, and to WHOI in 2001. Using geochemical markers, he traces dispersal, migration, and population dy- namics of marine invertebrates and fish, including clownfish. He has developed methods of cor- relating the chemical composition offish ear bones with the water fish live in and travel through. With much of his work in the South Pacific and Caribbean, Thorrold has been on many cruises, logging 1,000 hours of scuba diving and 800 hours in tropical environs. Growing up in coastal South Africa, Anne Cohen never knew snow, and spent time on the beach collecting shells. For her Ph.D. at the University of Cape Town, she studied shell composition and structure, using them to reconstruct the paleoceanography of west Africa's Ben- guela Current. She arrived in Woods Hole in winter, 1994, in T-shirt, jeans, and sandals, with a 6-foot coral core. At WHOI, she studied how corals record climate, and learned to scuba dive with sharks on a Pacific reef She has added sponges, deep corals, and fish otoliths to her list of interesting structures to study. Cohen and her husband, also a scientist, grow crystals and run after their young daughter on weekends. 38 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu In tiny ear bones, the life story of a giant bluef in tuna Chemical clues within the 2-centimeter-long ear bones of bluefin tuna are giving scientists the ability to track which waters the fish swam in «S^»T- and to reconstruct''^^ The Atlantic bluefin tuna, Thiin- nus tliynnus, is one of the fastest, most powerful and most beautiful of fish. It is also the most expensive. Highly prized by sushi connoisseurs, a single giant fish of 1,400 pounds may sell for $40,000. The tuna's high price has led the fishery to the brink of col- lapse. In 1981, in response to declining numbers of tuna, the International Commission for Conservation of Atlantic Tunas (ICCAT) introduced a strict management policy for Atlantic bluefin that rapidly developed into one of the most controver- sial and politically charged issues in fisheries management. The policy controversy, familiar to both commercial and recreational New England t^eir nfe histories. fishermen, centers on the as- sumption that there are two discrete and independent North Atlantic populations. The two populations are arbitrarily divided into eastern and western territories at the 45°W merid- ian. Each presumed stock is subject to different management restrictions, the most striking of which is the im- position of a strict, near-zero harvest quota for the western stock and the absence of country-specific quotas for the eastern stock. There is considerable debate con- cerning the appropriateness of the two- stock division because evidence is lack- ing to support its two key assumptions. The first is that eastern and western tuna populations reproduce separately in separate spawning grounds, with western fish spawning in the Gulf of Mexico and eastern fish in the Medi- terranean. The second is that the tuna populations do not migrate across the Atlantic and intermingle. A large research effort is currently underway to test these assumptions by tracking the movements of indi- vidual fish across the North Atlantic and studying their spawning behavior. Much of this effort — led by Barbara Block of Stanford University and Molly \ Lutcavage of the New England Aquar- ium— has involved the use of sophisti- cated pop-up satellite tags. Pop-up satellite tags presently have limited litespans, ranging perhaps from months to years. At Woods Hole Oceanographic Institution, we are investigating the feasibility of using chemical signatures in the otoliths, or ear bones, of giant fish to obtain infor- mation about trans-Atlantic migra- tions, stock mixing, and spawning hab- itats. The entire, detailed life history, from birth to death, of a giant 30-year- old bluefin is contained within a single otolith less than one inch long. Our approach is based on the prem- ise that differences in water chemistry and temperature experienced by fish during their travels will be recorded as distinct and predictable changes in the trace elements of aragonite, the mineral that makes up the otolith. This approach differs from most previous otolith studies in our use of microbeam technology to track chemical changes at weekly to daily resolution within a single ear bone. Using the micron-scale sampling capabilities of the Cameca 3f ion mi- croprobe and techniques developed to study coral skeletons, we have been able to analyze the chemi- cal composition of the primor- dium, a region of otolith just 20 microns in diameter. The primordium forms when the fish is still in the larval stage, s and its chemical composition i contains a record of where the * fish was born. o Our initial results are prom- c ising and show that we may be i; able to use chemical signatures 3 in the primordium to distin- guish different populations of bluetin tuna — in their first years of life when the primordium is being formed. With conventional bulk sample analy- ses, we are not able to distinguish between different stages (i.e. larval, juvenile, adult) of otolith formation. By contrast, our new approach gives us the ability to reconstruct the life history of the fish from birth to death. Because we can obtain a daily re- cord of the tuna's travels, rather than average, we may be able to tell when, during the tuna's long life, it swam in which waters. We can potentially dis- cern whether the tuna was born in the west and migrated east, or was born in the east and migrated west, instead of knowing only that it was in both areas sometime during its life. This will im- prove our ability to manage popula- tions of this magnificent fish. — Anne Cohen and Graliam Layne (Layne is a WHOI research specialist.) Woods Hole Oceanographic Institution 39 Tracking Fish to Save Them The Reef Fish Connectivity and Conservation Initiative By Simon Thorrold, Associate Scientist Biology Department, Woods Hole Oceanographic Institution For decades, the Nassau grouper (Epi- nephelus striatus) was one of the most sought-after fish species in the Caribbean and Gulf of Mexico, from the Bahamas to Central America. These large, deli- cious fish live among coral reefs and have a breeding behavior that makes them es- pecially vulnerable. They come together in aggregations ot thousands to spawn at specific times and places, making them easy to catch — and to overfish. Nassau grouper populations have been severely depleted by humans through- out most of their range. The environ- mental and economic ramifications are alarming, and regional governments are responding by restricting or prohibiting fishing for them. But several large spawning aggrega- tions of this species still exist in the west- ern part of its range near Belize, in the Meso-America Barrier Reef System. These aggregations may provide our last oppor- tunity to learn if and how fish populations are connected among isolated reef sites. This information will be critical if we are to save the Nassau grouper populations from local extinction, as has already oc- curred on some Caribbean islands. No fishing allowed Marine ecosystems in all the world's oceans are under considerable and in- creasing stress from human activities, precipitating urgent calls for new ways to counter the impacts of people. Resource managers are increasingly using Marine Protected Areas (MPAs) — areas com- pletely closed to fishing — as a means to maintain fisheries and biodiversity. But scientists, fishermen, environmen- talists, and governments continue to de- bate the effectiveness of MPAs. (See "Do Marine Protected Areas Really Work?" page 42, and "Can We Catch More Fish and Still Preserve the Stock?" page 45.) Monitoring mobile animals under water over long distances and times is difficult, if not impossible, so scientists use math- ematical models of population growth to predict the effectiveness of fishing clo- sures. Yet we don't know enough about one important component of such a mod- el— how fish move in and out of MPAs. To predict how well MPAs work, we will need models that accurately describe the move- ment of individuals between geographi- cally separated sites— what is termed population connectivity. A critical part of estimating connec- tivity among geographically separated groups offish is tracking the dispersal of larval fish. Until recently, there has been no way to tell if adult fish living in one reef habitat were spawned in a different location. We did not have the means to determine where fish were spawned, be- cause most fish larvae are too small to be tagged by conventional means. 40 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Revolutionary tagging technology But now, scientists at Woods Hole Oceanographic Institution have achieved a breakthrough that is poised to revolu- tionize the study of larval dispersal in marine tish. We have demonstrated that it is possible to introduce a unique chem- ical tag into the ear bones (otoliths) of fish embryos by injecting the female be- fore she spawns with a nontoxic isotope. The isotope is a variant of the ele- ments barium or strontium, which would normally be incorporated in small amounts (along with calcium) into the fish's ear bone as it grows. But the iso- tope has a slightly different mass than the common form of the element. The otolith grows as the fish grows, with layers that are laid down like tree rings during the fish's life. All the mate- rial in the otolith remains where it was originally deposited; it is not continually turned over, as happens in other bones. An isotope v/ith different mass "built into" the ear bone at the start of life will always be there, in minute amounts, at the center, or earliest, part of the otolith. This tag remains in the otolith through- out the fish's life, wherever it travels. Ear bones tell the tale When the fish is caught, we can remove the otolith, and use a mass spectrometer equipped with a laser system to detect the tag. (See "The Secret Lives of Fish," page 36.) A narrow laser beam from the instru- ment ablates, or vaporizes, selected parts of the otolith (in this case, the first-formed area, or core), and the isotopic composi- tion of the vaporized material is then au- tomatically analyzed to reveal whether the isotopic tag is present. Fish can be identi- fied as the offspring of a tagged parent if the otolith core contains significantly more of the rare isotope injected into the parent, as compared with control samples with natural isotopic compositions. Beginning in 2005, we will employ this new technique on large, long-lived species that aggregate to spawn at specific times and places and produce planktonic eggs, particularly the Nassau grouper, in coral reefs off Belize. It will give us the ability to learn for the first time whether Nassau groupers— tagged at spawning- disperse to other parts of their range during their larval lives. We will also be able to determine the extent to which fish hatched in an MPA return to their natal location, are dispersed from the MPA to areas open to fishing, or are recruited to other protected habitats. A conservation partnership Applying this innovative technology, the WHOI Ocean Life Institute (OLI) is launching the Reet Fish Connectivity and Conservation Initiative. The project is funded in large part by the Oak Founda- tion, a private philanthropy whose priori- ties include conservation ot the marine environment, and by OLI. The initiative will partner WHOI with a multinational large-scale study of coral reef fish and ecosystems called the Targeted Coral Reef Research Project, funded by the Global Environmental Facility (GEF) and imple- mented bv the World Bank. GEF is an independent organization that receives contributions from donor countries and funds projects that benefit and promote sustainable ecosystems in developing countries. The World Bank helps GEF implement projects in theme areas of crit- ical global interest, including biodiversity. Depletion of tish stocks in the tropi- cal coastal regions and coral reefs of the world is a large and growing problem. In many places in the Caribbean, the loss of 80 to 90 percent ot grouper populations to overfishing has meant significant losses to fishermen and local economies and se- vere degradation to ecosystems. Scientists, conservation groups, private foundations, and governments, along with financial and economic organizations such as the World Bank are concerned — and begin- ning to work together. With such support, new scientific approaches such as otolith tagging may provide information that resource managers and policy-makers can use to design and implement Marine Protected Areas that will protect marine populations vulnerable to human exploi- tation, including the Nassau grouper. Atlantic Ocean Geographic distribution of Nassau grouper DWINDLING FISH POPULATIONS— Fishermen have long sought Nassau groupers, which live among coral reefs in the Caribbean Sea, from Central America to the Bahamas and Bermuda. In recent decades, 80 to 90 percent of grouper populations have been lost to overfishing. Woods Hole Oceanographic Institution 41 Do Marine Protected Areas Really Work? Georges Bank experiment provides clues to longstanding questions about dosing areas to fishing By Michael ). Fogarty, Adj. Associate Scientist, Woods Hole Oceanographic Institution and NOAA Fisheries Service, Northeast Fisheries Science Center and Steven A. Murawski, Director, Office of Science and Technology, NOAA Fisheries Service, Silver Spring, MD Closing parts of the ocean to fishing to preserve fish stocks holds great intuitive appeal. Similar resource man- agement tools have been used as tar back as the Middle Ages, when European kings and princes controlled access to forests and streams, and the fish and wildlife in them. In Hawaii, chiefs established and maintained networks of no-fishing "kapu" zones, with violations punishable by death. Today, Marine Protected Areas, or MPAs— areas of the ocean temporarily or permanently closed to harvesting— are being proposed to restrict not only fish- ing, but also mineral and hydrocarbon extraction, and other activities. Some advocates of MPAs suggest that at least 20 percent of the coastal and open ocean should be set aside and permanently zoned to protect ecosystems, sustain fish FISHING ATTHE BORDERS — Georges Bank and surrounding areas with historically abundant fisheries have seen fish stock depletion and fishery collapses. To speed stock recovery, Marine Protected Areas (MPAs) closed to fishing have been established (blue polygons). Dots show fishing effort in 2003, based on satellite tracking of vessels moving at less than 3.5 knots and assumed to be towing fishing gear. Warmer colors (green to red) denote more intense activity. The highest intensity of fishing occurred right at MPA borders, indicating that fishers expected greater abundance there. stocks, and reduce conflicts between us- ers of the oceans. But the key question remains: Do MPAs really work? It is the modern incar- nation of a longstanding question: How can we best ensure sustainable fisheries? A Victorian model In the 19th century, scientists vigor- ously debated the effects ot fishing on fish populations and ecosystems. A major- ity of scientists accepted the paradigm that the oceans were unlimited. Thomas Henry Huxley, a preeminent Victorian naturalist, famously stated in 1884 that: "... the cod fishery, the herring fishery, the pilchard fishery, the mackerel fishery, and probably all the great sea-fisheries, are inex- haustible; that is to say that nothing we do seriously affects the number ojjish ... given our present mode oj fishing. And any attempt to regulate these fisheries consequently ... seems to be useless." The debate culminated in one of the first documented - experiments to determine J: the effects of fishing. In 1886, 1 one bay in Scotland remained ; open while another was 2 closed to fishing for 10 years. The focus of the experiment was plaice, a valuable com- mercial fish. Over the decade, plaice in the closed bay in- creased significantly com- pared to plaice in the open 42 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu THE DIFFERENCE A DREDGE MAKES — Dragging fishing gear over the oceam bottom causes severe damage to seafloor habitats and organisms. At left, a normal seafloor community on Georges Bank; at right, a similar area after dredges have been used to harvest scallops. bay. It was an early, instructive demon- stration that fishing does have impacts on fish populations, and that regulation is effective for conservation. SomeABCsofMPAs Since then, seasonal and longer-term closures have been an important fishery management tool, and they have protect- ed spawning fish and nursery areas, pre- served vulnerable habitats, and reduced fishing pressure. But by themselves, MPAs cannot at- tain all of today's fishery management objectives. And they can create unintend- ed consequences. Preventing harvesting in some areas, for example, inevitably results in people fishing in other, perhaps more vulnerable, locations. MPAs have now been established throughout the world ocean, from the tropics to the poles. Most are relatively small. Many are neither adequately en- forced nor monitored to determine their effectiveness. Of those that have been scientifically monitored, many are in tropical and sub- tropical areas. Fish in these regions live most of their lives in specific habitats, such as reef structures, and don't stray from them. Their fidelity to a small territory is an important part of the potential success of their marine reserve. Populations do increase in such reserves, and some studies suggest a spillover effect from the reserve that augments fisheries nearby. By contrast, in temperate, boreal, and subarctic systems — where most of the major world fisheries reside — many fish populations are wide-ranging and often exhibit extensive seasonal migrations. Can a reserve by itself be a successful fishery management tool for these fish? The Georges Bank 'experiment' In 1994, federal regulations established a number of year-round fishery closures on Georges Bank and adjacent areas. This shallow bank has sustained fisheries of legendary abundance for hundreds of years until the mid-20th century, when the heavily fished stocks declined steeply. The year-round closures evolved from seasonal closures established in the 1970s by the International Commission for Northwest Atlantic Fisheries to protect spawning groundfish, particularly had- dock. The current year-round closed areas — on Georges Bank and two nearby areas — encompass more than 20,000 square kilometers. It is one of the largest systems of closed fishing areas now in ef- fect. In addition, a mosaic of seasonally closed areas in the Gulf of Maine elimi- nates fishing in virtually all parts of the gulf at one time or another. At the same time, the National Oce- anic and Atmospheric Administration also restricted the number days at sea that fishermen could fish. Fishing by trawlers declined by more than 40 percent over the next five years, although fishing with stat- ic gear, such as lobster traps, gillnets and longlines, and limited scallop harvesting, is still allowed in the closed areas. These closures have given us a unique opportunity to examine a marine pro- tected area in a temperate system under a "macroscope"— to investigate how marine ecosystems are structured and how they function and recover. The long history of research on Georges Bank adds a founda- tion of scientific knowledge that makes the Georges Bank MPA ideal for testing the effects of year-round fishery closures and adds essential observations to test models. (See "Can We Catch More Fish and Still Preserve the Stocks?" page 45.) In the aftermath of closures We have several ways to assess the Georges Bank and nearby MPAs. We have monitored fish and shellfish populations to get detailed comparisons of abun- dances and sizes of animals within and outside the closures, both before and after the establishment of the MPAs. Together with information from the commercial fishery and from scientific studies, the results let us see the impacts of the closed areas on seafloor organisms and com- munities, on the physical structure of the habitat, and on population levels offish and shellfish species. It is not easy to separate the effects of the closed areas on Georges Bank from other changes, such as fishing-days reduc- tions implemented at the same time. How- ids Hole Oceanographic Institution 43 ever, our studies show that the closures have played an important role in the over- all increase in abundance ot these stocks: • The biomass (total population weight) of a number of commercially important fish species on Georges Bank has sharply increased, due to both an increase in the average size of individuals and. for some species, an increase in the number of young surviving to harvestable size. • Some non-commercial species, such as longhorn sculpin, increased in biomass. . By 2001. haddock populations rebound- ed dramatically with a fivefold increase. . Yellowtail flounder populations have increased by more than 800 percent since the establishment of year-round closures. • Cod biomass increased by about 50 per- cent by 2001. • Scallop biomass increased 14-fold by 2001. an extra benefit of the establish- ment of closed areas primarily intended to protect groundtish. Eggs and larvae to seed the seas Despite increases in biomass, MPAs benefit a fishery only it fish eggs and larvae are exported from closed areas to replenish open, harvested areas, and/or if some harvestable-size stock "spills over," moving from closed to open areas to be caught. But if fish at any age leave closed areas at high rates, it will prevent a build- up within the reserve and cancel out any positive effects from the MPA. Estimating the export of eggs and lar- vae is extremely difficult. But we can use the location of spawning aggregations and hydrodynamic models to estimate the magnitudes and directions of eggs and larvae dispersal. On Georges Bank, a key factor in lar- val dispersal is a well-established clock- wise circulation pattern, or gyre, result- ing from factors including local tidal forces and seafloor topography. The gyre creates a conduit that may allow eggs and larvae to self-seed closed areas, cross-seed other closed areas, and trans- port larvae to open areas. Our analyses for scallop larvae indicate that the closed areas on Georges Bank can be self-sus- taining and also contribute to recruit- ment into other areas. Spillover and trawling impacts Our initial findings on spillover amounts show that the MPAs have ben- efited fisheries for some species, but not all. Using information from the commer- cial fishing fleet, we found significant spillover for haddock and for yellowtail and winter flounders near some closed areas, but no spillover for other commer- cially important species. But the commercial fleet clearly ex- pects spillover from MPAs. Satellite tracking shows that large trawlers con- centrate fishing efforts on the borders of the closed areas, poised to pounce on any fish that stray over the boundaries. Scientists from the Northeast Fisher- ies Science Center, University of Rhode Island, and the U.S. Geological Survey have documented the impacts of mobile fishing gear, such as bottom trawls and dredges, on bottom-living (benthic) com- munities of organisms. Comparing de- tailed photographic images ot sites inside and outside the Georges Bank closed ar- eas, they have measured the damage done to the seafloor. The difference is striking: We can see the recovery of benthic organisms inside the closed areas and watch community structure re-emerge as a result of the MPA. Benefits beyond fisheries The large-scale management experi- ment on Georges Bank indicates that a combination of MPAs and other manage- ment measures, such as reduced fishing efforts, can allow some species to recover from overexploitation. And beyond pro- tecting fisheries, MPAs potentially offer other benefits. They can: • help preserve marine ecosystems and biodiversity of non-targeted fishery spe- cies by curtailing trawling damage or in- advertent catch • promote non-extractive uses ot marine areas, like eco-tourism • establish undisturbed locations tor sci- entific studies that can further improve resource management and conservation. To make the best use of MPAs, though, we have to clearly specify our objectives. We then must evaluate the ef- fectiveness and the social and economic impacts of MPAs and compare the utility of MPAs with other possible management tools to see if they are the best option for the situation. The Georges Bank experi- ence has proven very instructive in how to implement and evaluate marine pro- tected areas in temperate seas — and the experiment is still going strong. Michael Fogarty started life far from the ocean, in Fairbanks, Alaska. His parents, New England natives, eventually returned to Rhode Island, where he became fascinated with sea life and embarked on a career in marine biology. He received a doctorate from the University of Rhode Island and came to the Northeast Fisheries Science Center in 1980, where he studies changes in marine ecosystems in response to fishing. He has served on numerous national and international panels and committees, including the Scientific Steering Committee of the U.S. GLOBEC program, which he chaired from 1997 to 2002, and the Global Ocean Observation System (GOOS) Steering Committee. When not keeping the world safe for fish, he serves as a full-time chauffeur for his children, ages 9 and 12, who lead very busy lives. Steven Murawski spent his formative years in Kansas and Texas, before moving to New England as a teen. Interested in fisheries and the ocean since he was a lad, he obtained degrees at the University of Massachusetts- Amherst. Since coming to the Northeast Fisheries Science Center, he has been involved with determining how many fish ot various species are in the ocean, and how many should be caught— the process of stock assess- ment. Murawski will soon be the Director of the National Marine Fisheries Service's Office of Science and Technology. He lives in Massachusetts with his wife, daughters, and a golden retriever. 44 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Can We Catch More Fish and Still Preserve the Stock? Mathematical analyses offer new insights into age-old controversies on fishing restrictions Michael Neubert, Associate Scientist Biology Department Woods Hole Oceanographic Institution Near the town of Webster in southern Massachusetts there is a small lake with a long name: Lake Chargoggagogg- manchauggagoggchaubunagungamaugg. The correct translation, from the original Native American language, refers to Eng- lishmen fishing at a certain place, near a boundary. But a humorous translation in a 1916 newspaper article, now accepted the world over, is: "You fish on your side; I fish on my side; nobody fishes in the middle." People have always fished. But the history of fishing is also the history of overfishing. For hundreds of years, the establishment and enforcement of fish- ery management policies have generated controversy, as competing authorities have searched for a way to balance com- peting goals— to catch as many fish as possible while conserving the resource. To resolve this dilemma, we have applied mathematics— and we are finding that the ancient solution may still prove ef- fective in modern times. Conflicting policies and goals In May 2000, President Bill Clinton issued Executive Order 13158, expand- ing a 20-year-old fisheries management law, the Magnuson-Stevens Act. The SEARCHING FOR SOLUTIONS — Michael Neubert (left), WHOI mathematical ecologist and biologist, discusses equations with Alison Shaw, an undergraduate student in the WHOI Summer Student Fellowship Program. Mathematical models can yield information about population ecology that complements traditional monitoring methods. Woods Hole Oceanographic Institution "*-* order requires the National Oceanic and Atmospheric Administration (NOAA) and other federal agencies to establish new Marine Protected Areas (MPAs) and to expand the protection ot exist- ing MPAs. An MPA is defined as "any area of the marine environment that has been reserved by federal, state, territo- rial, tribal or local laws or regulations to provide lasting protection for part or all of the natural and cultural re- sources therein." MPA examples include National Marine Sanctuaries, Federal Threatened/Endangered Critical Habitat and Species Protected Area sites, and National Estuarine Research Reserve system sites. The language of this order clearly em- phasizes conservation. But NOAA has another mandate: to manage fisheries, "while achieving, on a continuing basis, the optimum yield from each fishery for the Unit- ed States tishing indus- try." Does the MPA ap- proach work tor the dual purpose ot increasing conservation and maxi- mizing yield? The growing weight of scientific opinion is that MPAs do protect endan- gered species and con- serve essential habitats. (See "Do Marine Protect- ed Areas Really Work? page 42.) In fact, in a sur- prising show of unanim- ity, more than 160 marine scientists signed a state- ment documenting their consensus that marine reserves have ecologi- cal benefits (http://www. nceas.ucsb.edu/Con- sensus/consensus.pdf). Inside such reserves, fish population sizes, bio- masses, organism sizes, and biological diversity are all typically higher than they are in ecologically similar but unprotected areas. "No-take marine re- serves"— a type of MPA within which tishing is prohibited — seem to be particu- larly effective. But what effects will expanding ma- rine reserves have on the fisheries? Many people, and not just fishermen, believe it is impossible to obtain the maximum yield from a fishery while simultaneously setting aside areas as marine reserves. A congressional critic of marine reserves re- vealed some of the intensity of the debate during congressional hearings in 2002 when he said that "the marine reserve movement seeks to exclude the Ameri- can public from a public resource without scientific justification tor doing so. . ." (http://resourcescommittee.house.gov/ archives/107cong/fisheries/2002may23/ peterson.htm). Lake Chargoggagoggmanchaug- gagoggchaubunagungamaugg V AHEAD OF THE TIMES — This lake in Webster, Mass., has a long name derived from the Native American Nipmuk language. The widely known (though incorrect) translation ("You fish on your side; I fish on my side; nobody fishes in the middle") may foretell how Marine Protected Areas can ensure the greatest fish abundance. A web of interrelated factors The essential questions are: Can NOAA simultaneously fulfill its conser- vation and fisheries management mis- sions, and can they do so using marine reserves? These are tough questions, because they are both complex and vague. Scien- tists prefer to try to answer simple, con- crete questions. Therefore, when I began to think about MPAs, I changed those two questions into these three: 1. Is it possible to maximize the sustain- able yield of a fishery using marine reserves? 2. If so, how big should they be? 3. Where should they be placed? These questions intrigued me, and so I set about trying to answer them using mathematics. At face value, it may not seem like my three questions are math- ematical questions at all. But like most scientific questions in ecology, they are — and here's why: The questions all in- volve optimally balancing various rates of change to achieve some goal. In this case, the goal is maximi- zation of yield. The rates are individual growth rates, population growth rates, harvesting rates, dispersal rates, distur- bance rates, and when economics is brought into the picture, interest rates. Many of these rates interact with each other in nonlinear ways. For example, as harvesting rates increase, population size tends to decrease. When that happens, fewer individual fish compete for food, individuals may grow taster, and as a re- sult, reproduce sooner. This web of interacting rates is quite complicated. WEBSTER •r s 46 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu There is no way to distill the consequences of the interactions of all of those rates, let alone figure out how to balance them in an optimal way, without using a math- ematical model, which is a set of equations describing how the properties of a system depend on and relate to each other. Models describe the behavior of a sys- tem in mathematical language — that is, equations. Models are powerful because they let us identity and separate critical factors (variables) affecting a changing system. By refining the equations, we can come closer and closer to describing the real system— and being able to predict it. Limiting fishing — or places to fish Fisheries biologists have a long tradi- tion of using mathematical models, so I was not surprised to find that people had already attempted to answer my first question. They used models ranging from simulations of very complicated comput- er models to "pencil and paper" manipu- lations of very simple models. For the most part, these analyses compared two types of fishing strate- gies. The first strategy seeks to find an ideal arrangement ot marine reserves that maximizes fish yield by varying the size and placement of one or several reserves. The second, more "traditional" strategy is to vary the level of tishing uniformly over an entire area to maximize the yield. The results ot these analyses, with few excep- tions, show that the best-distribut'ion-of- marine-reserves strategy and the more traditional fishing-limit strategy both produce the same yields. Both analyses have problems, however. Both strategies assume that a reserve pro- tects an unchanging fraction of the fish— those in the fixed area of the reserve. But in reality, as fish populations grow, a varying fraction of the stock will disperse out of the reserve area, so the remaining fish are also a varying fraction of the to- tal—and the analysis doesn't account for that variation. Only a so-called "spatially explicit" model, which takes the locations and movement of the fish into consid- eration, will account for the biophysical reality ot fish dispersal. Surprising initial results I set out to construct and analyze a spatially explicit fishery model and use it to determine the fishing strategy that produces the maximum possible yield — without assuming ahead of time that either of the usual strategies would be best. I kept the model simple enough that I could analyze it mathematically (which meant that 1 kept it very simple). In my model, all fish are identical, they live in a one-dimensional habitat of finite length, they move in a random fashion, and if they happen to leave the habitat, they die. The only limit I placed upon fishing effort was that it could not exceed some preset maximum level. I used techniques from a field of math- ematics called "optimal control theory" to figure out the best fishing strategy. This is the same theory that engineers use to figure out the most efficient way to control the motion and stability of airplanes, rock- ets, and submarines — hence the name. The results ot my analysis were sur- prising. The tishing strategy that maxi- mized yield always included at least one marine reserve, and fishing strategies that did not include reserves were all less than optimal. In other words, fishermen actually catch fewer fish when there are no areas closed to fishing. The optimal number of reserves de- pended upon the length of the habitat. If the habitat was large, the best arrange- ment of fishing took on a very intricate geometric structure— with infinitely many reserves alternating with areas of maximum fishing effort. Of course, such a complex distribution of fishing effort could never actually be used in the real world. But in every case — for every habi- tat length — I was able to find a strategy using only a few reserves that came very close to producing the maximum yield. Deeper into the complexities Are MPAs the best wav to maximize yield in real fisheries? Will fish and fish- eries both thrive if you fish on your side, I fish on my side, and nobody fishes in the middle? My results suggest that this is true. There are, however, many assumptions and simplifications in my model that are open to objections. Fisheries biologists might assert that it's essential to account for population size structure, uncer- tainty about the variables, and changing environmental properties. Conservation biologists might demand an optimization that includes what they term an "exis- tence value"— a non-consumptive value assigned to the fish's existence, whether or not anyone ever sees, or catches, the fish or its descendants. Biological ocean- ographers might object to the fact that my model ignores species interactions, or to the use of a one-dimensional model, or to the way that I described the movement offish, which disregards ocean currents. Economists might argue that the maxi- mization of sustainable profit, rather than the maximization of yield, should be the management objective. Including some of these modifications in the model could change my results; others might not. I am looking forward to exploring these issues further during my tenure as an Ocean Life Institute Fellow. Michael Neubert graduated from Brown University with a bachelor's degree in applied mathematics and biology and has been interested in the intersection between these two fields ever since. After receiving a Ph.D. in applied mathematics from the University of Washington in 1994, he came to the Woods Hole Oceanographic Institution as a postdoc- toral scholar, and is now an associate scientist in the Biology Department and Fellow of the Ocean Life Institute. Most of his research uses ecological models that include a spatial com- ponent. Using spatial models lets him address important questions in ecology and conserva- tion biology, such as: What determines how tast a population spreads through a habitat into which it is newly introduced? How much habitat does a population require to persist? How should one design a system of preserves to protect an endangered species? When not running ecological models, Neubert is usually running to the nearest coffee shop. Woods Hole Oceanographic Institution 47 Voyages into the Antarctic Winter Pioneering cruises into the pack ice of the Southern Ocean reveal secrets of its fertile ecosystem Peter H. Wiebe, Senior Scientist Biology Department Woods Hole Oceanographic Institution At the extreme end of the Earth, Ant- arctica is a vast, rocky continent, mostly ice-covered and barren. Sur- rounding Antarctica, the Southern Ocean is equally vast, cold, and ice-covered. But unlike the land, it teems with life, rang- ing from microscopic plankton to top predators: whales, seals, penguins, fish, and sea birds. The region's fecundity is fueled by 24- hour-a-day sunlight in summer, combined with ocean currents that bring essential nutrients. These provide the ingredients for rich blooms of microscopic marine plants and animals at the base of the food chain— phytoplankton and zooplankton— that are similar to those in many produc- tive regions of the world's oceans. But there is one big difference in the Antarctic ecosystem. The food moves swiftly to the very top of the chain through a crucial link: a shrimp-like crus- tacean called krill, which swarm in great pink oceanic patches that range from tens of square meters to tens of square kilo- meters. The krill connect the microscopic primary producers, which they eat, to the ICY RENDEZVOUS — Two National Science Foundation research vessels, the Nathaniel B. Palmer (left) and Laurence M. Gould, go bow to stern to exchange equipment, supplies, and personnel just west of Marguerite Bay during an unprecedented cruise into the winter pack ice off Antarctica. 48 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu top predators, which eat them. This unique and unusually short oceanic food chain is both strong and vulnerable. It efficiently supports large populations of big animals. But a small disruption in the chain could drastically affect the entire ecosystem. Adding urgency are recent indica- tions of changing conditions around Antarctica— particularly more frequent calving of massive icebergs from the con- tinental ice shelf. To manage and protect this unique environment, we need a more thorough understanding of the intricacies ot the ecosystem and the potential effects ot climate change on it. Krill are the glue that binds the Ant- arctic tood web, and 20th-century expe- ditions learned a great deal about their life stages, distribution, and abundance — but only during the warmer, sunlit, ice- free periods of the year. How do adult and larval krill survive the frigid, sunless winter — when photosynthesis diminishes essentially to zero and much of the ocean is covered with pack ice — to become an abundant food source for large animals the next spring? To pull back the veil on this critical and previously shrouded part ot the ecosystem, we undertook 11 cruises to the Southern Ocean, including four unprecedented voyages into the Antarctic winter ice pack. Destination: Marguerite Bay The cruises were part of the Global Ocean Ecosystem Dynamics Program (GLOBEC), a multiyear, multination, multidisciplinary series of investigations of several touchstone regions throughout the world's oceans where marine lite and fisheries historically thrive. Marshal- ling scientists across several disciplines, GLOBEC sought to define and measure the many factors— oceanic currents, cli- matic conditions, seafloor topography, biological processes, and others— that converge to create and maintain produc- tive ecosystems. GLOBEC also seeks to provide information on the vulnerability of ocean ecosystems to climate changes. GOING FOR THE KRILL— BIOMAPER-II is lifted aboard the icebreaker Palmer, which cleared a path in the ice to tow the vehicle behind it. BIOMAPER-II has an acoustic system to detect plankton andzooplankton, a video plankton recorder to take pictures of them, and sensors to measure water properties. ered mountains and seaward by huge ice shelves. It is dotted by numerous small islands and persistently covered by sea ice in winter. Below the sea surface, the bay is gouged by a trough that cuts di- Fieldwork for the Southern Ocean GLOBEC program, conducted between 2001 and early 2003, focused on a broad and relatively deep (300 to 400 meters) continental shelf region off the western Antarctic Peninsu- la, due south of the tip of South Amer- ica, from Adelaide Island to Charcot Island. In between lies Marguerite Bay, which supports a large, persistent stock of krill and large populations of top predators that depend on it for food. We sus- pect that this area may act as a reser- voir for maintain- ing krill stocks hundreds of miles away in the Scotia Sea, as far as South Georgia Island. Marguerite MARGUERITE BAY AND ENVIRONS, on the Western Antarctic Peninsula, Bay is surround- was the research site for four Southern Ocean GLOBEC cruises. Inset: ed landward by Antarctica and the southernmost tip of South America, where research high, snow-cov- vessels depart Punta Arenas, Chile, to cross to Antarctica. NBP0204-GLOBECIV NBP020 2 - GLOBEC III NBP0104-GLOBECII NBP010° -GLOBEC I Woods Hole Oceanographic Institution ' The Antarctic ecosystem Antarctic seas are extremely productive because phytoplankton grow abundantly during the extended daylight of summer and feed huge populations ofkrill. Krill are a key animal in this ecosystem, as food for are important predators of krill, copepods, and fish. top predators: whales, penguins, and seals. Winters have little light, no phytoplankton growth, and extremely cold temperatures, but a complex food web links a great variety of ocean animals. NGUINS consume krill as the dominant >art of their diets, but they also eat other animals, such as midwater fish and amphipods. WEDDELL SEALS and FUR SEALS are part of the Antarctic Ocean ecosystem, and krill are major parts of their diets. CRABEATER SEAI feed on krill and large prey such as penguins and seals. CTENOPHORES and other gelatinous, transpar plankton range from tiny to 30 centimeters. They eat crustaceans and small fish, from deep water to under the pack ice. PTEROPODS are planktonic snails. A 2-millimeter, transparent species is an abundant food source; a 2.5-centimeter, dark brown species is much less common. NILE KRILL aggregate er pack ice in winter, eating microscopic plankton and ice alga" *' grow in and on the ic \LS eat penguins eater seals. AMPHIPODS in the plankton are red and often are prey of penguins and fish. KRILL adults form large swarms and feed on phytoplankton, copepods, and other plankton. SQUID eat krill and fish, and in turn, are eaten by seals and whales. FISH live from midwater depths to under the ice and eat a variety of food from plankton to crustaceans such as krill and amphipods. _ WHALES and ot les strain vast am COPEPODS provide abundant food for krill, other invertebrates, and fish. In winter, they stay deeper in the water. agonally across the continental shell and ends in fjord-like features up to 1,600 meters deep in the interior of the bay. Our principal goal was to discern how these features, along with water proper- ties and currents in the region, conspire to allow krill to flourish and be retained in the area. Coping with the chill Working in the Antarctic fall and winter was challenging, and the scientists themselves had to learn to adapt. Tem- peratures during the fieldwork ranged from 0°C to -28.5°C (32°F to -19.5°F). As the late tall turned into winter, bitter cold and near perpetual night set in. The day was a brief, dim twilight. Sea ice covering the water made it very difficult to deploy and tow our instruments to sample ocean waters and marine life. Seizing this rare opportunity to con- duct research in these remote locations at these times, scientists had to coordinate a wide range of research spanning the spec- trum of the region's physics and biology. It was the first time so many scientists had gathered to study so many aspects of the Antarctic. To accommodate the amount and breadth of research, the scientists had to endure long cruises, 44 to 50 days, in trig- id conditions and had to use two National Science Foundation research ships at the same time. One was the 308-foot ice- breaker Nathaniel B. Palmer, which can operate in pack ice and clear a way. The other was the 230-foot, ice-strengthened research vessel Laurence M. Gould, which can come in contact with ice but not force its way through it. In the fall of 2001, we worked mostly in open water, free of sea ice. In these condi- tions, the two ships could work indepen- dently. For instance, scientists studying 50 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edi plankton and those studying penguins could travel to separate locations to do sampling needed by each group. But conditions were much colder when we returned to the region in the fall of 2002— in fact, the coldest in 20 years of measurements there. Sea ice formed al- most instantaneously, and we were often beset by icebergs that made it difficult or impossible to do our work, or even to get to sampling locations on a grid we had mapped out to ensure coverage of the bay. The ships had to remain together in con- voy to get to work sites, with the icebreak- er leading the way. Still, we persisted, huddling in our extreme-weather cloth- ing, with the ships casting beams of light into the darkness. Unprecedented observations The Southern Ocean GLOBEC cruises resulted in a number of "firsts." An im- portant accomplishment was to install arrays of long-term moorings in strategic locations across the continental shelf and inside Marguerite Bay. These moorings had sensors that measured water cur- rents, temperature, salinity, and bio-opti- cal properties (such as the clarity of the water) continuously over two years be- tween deployment in 2001 and retrieval in 2003. Such moorings never before had been deployed on the Antarctic continen- tal shell, and they provided the first-ever measurements of currents there. Current surveys based on instruments deployed from the ships revealed large circular eddies swirling on the continen- tal shelf, which may help keep krill in the bay, where conditions favor their survival. The surveys showed that water from the fast-moving Antarctic Circumpolar Cur- rent, circulating just beyond the conti- nental shelf, rides up onto the shelf, sup- plying warmer, more saline, nutrient-rich water into the Marguerite trough and bay. Such intrusions moderate winter condi- tions in the bay and enhance its fertility. Oceanographers also found a previ- ously unknown southward coastal cur- rent that flowed along Adelaide Island, into Marguerite Bay, and then south along Alexander Island. Our hypothesis is that deep and recirculating currents in the bay support krill reproduction, and the coastal current may move krill prog- eny along the coast to other areas. Scientists and engineers also moored pressure-protected instruments on the seafloor, both on and off the continen- tal shelf and in Marguerite Bay, to record marine mammal calls for a year at a time and open a previously inaccessible win- dow onto cetacean life in this region. Two automatic weather stations were installed on Kirkland and Faure Islands in the middle of Marguerite Bay. They continue to operate, providing the first continuous meteorological observations from this region of the Antarctic. Tools to catch elusive prey The aim of the biologists aboard the GLOBEC cruises was to survey krill and other plankton in the water and map where their populations are. To accom- plish this, we needed a combination of tools and instruments. Adult krill swim last and are notori- ous for avoiding capture by the relatively small nets traditionally used by ocean- ographers. To circumvent this, high-fre- quency acoustics has become biologists' tool of choice for surveying krill. A trans- ducer emits sound into the water. When sound waves, propagating at 1,500 meters per second, hit animals in the water, a portion of the energy is scattered back to the transducer. The acoustic signals give an indica- tion of how much animal life is pres- ent at different depths, but they cannot identity what species are present. So, de- spite the krill's agility, we still use nets to collect samples needed to interpret the acoustic returns. To map the distribution of krill and other plankton, we used a towed vehicle, the Bio-Optical Multifrequency Acousti- cal and Physical Environmental Recorder, or BIOMAPER-II. It is equipped with an acoustic system with five frequencies, a video plankton recorder system (VPR) to take pictures of the plankton, and sensors to measure water properties. UNDER THE ICE — Melanie Parker and Kerri Scolardi (University of South Florida) dive to collect juvenile krill that aggregate under pack ice to feed on microzooplankton and ice algae. Woods Hole Oceanographic Institution 51 A krill's life cycle • Euphausia ; superba TEgg Calyptopis Metanauplius * Nauplius Robots and divers under the ice We also towed a specialized net at different depths behind the ship to col- lect plankton that were later sorted and identified aboard ship. This net, the Multiple Opening/Closing Net and Environmental Sensing System (MOC- NESS), has a 1-square-meter mouth opening that can be signaled to open and close separate nets to capture plank- ton at different depths without combin- ing the samples. We equipped it with a strobe light to temporarily blind the krill so they could not see the net, thus reduc- ing their ability to avoid it. We used an even larger MOCNESS trawl to collect the larger mid-water animals, such as shrimp and fish. In winter, krill larvae and other plank- ton often are found living in or just under the bottom of pack ice. So we sent a small remotely operated vehicle (ROV) under the ice. It was tethered to the ship by a cable that transmitted power to the ROV and data from it. Operators could directly monitor and direct the vehicle, which was equipped with a VPR; water temperature, salinity, and depth sensors; and a track- ing device to signal its location. Finally, teams of divers conducted un- der-ice surveys of krill larvae and collect- Krill start life as eggs that sink and hatch in spring. They develop through larval stages as they swim to the surface, reaching the fourth (TurciliaJ stage by winter. Krill that hatch at the depth of the Antarctic shelf (300 to 400 meters) can swim back to surface waters before winter and find phytoplankton to eat before they use up their stored supplies. Furcilia that make it survive their first winter by feeding on algae and zooplankton on the undersurface of pack ice. But krill that hatch in water deeper than 500 meters may starve before they can swim back to the surface, and food. ed some of them for experimental studies back onboard ship to measure the krill's rates of feeding, growth, and respiration. A krill's life Antarctic krill, Euphausia superba, is the largest and often the most abundant of five shrimp-shaped euphausiid spe- cies that inhabit Southern Ocean waters. They grow to lengths of 6.5 centimeters and can live for seven to eight years — al- though most get eaten early in life, and few, if any, die of old age. In most ways, the life history of krill is typical of crustaceans. Life begins as a fertilized egg that hatches into a larva called a nauplius. Then, as the larva grows, it goes through a series of lar- val stages (called metanauplius, calypto- pis, and furcilia — several stages of each). When the larvae's exoskeletons become too small, they molt and grow progres- sively larger exoskeletons, until they be- come adults. But in some other ways, Antarctic krill have an unusual life history, facing chal- lenges inextricably linked to their envi- ronment. To survive here, they need not only the long light conditions of summer, but also the icebound sea of winter. Scientists on the British Antarctic expe- ditions discovered 80 years ago that krill eggs sink to depths of 500 meters or more before hatching, perhaps to avoid preda- tion near the surface. (That requirement fits nicely with the depths of the western Antarctic continental shelf.) But the lar- vae eventually have to swim back up to sunlit surface waters to find enough food (phytoplankton and zooplankton) to grow through their larval stages to adulthood. Antarctic water is very cold, only 1°C to -1.8°C, and the cold temperature slows the krills' larval development. Krill eggs hatched in the austral spring only make it to the fourth, or furcilia stage, before win- ter sets in. By that time, pack ice covers the water, and no phytoplankton grow. Neither krill larvae nor adults have stored enough lipids (fat) to provide energy to see them through until spring. So how do they make it? Survival tactics Two field seasons of the Southern Ocean GLOBEC program in the Ant- arctic fall and winter have significantly improved our understanding of how krill survive the winter. Part of the answer is that krill larvae that reach the surface congregate in, or just under the bottom of, pack ice. In the open ocean, anything that can be used as surface will be — to grow on, huddle on, feed on, or get caught on. In the pitted underside of the ice are phytoplank- ton, ice algae, microzooplankton, and or- ganic detritus. We found that larval krill have flexible feeding habits and can eat this diverse, albeit scarce, buffet. We found from shipboard studies that at least some larval krill are able to obtain enough food within and under the ice to meet their nutritional needs during the austral winter, though they could not find enough food to grow. But they can delay their growth, molt- ing, and development, or even suspend them for a time. They can even survive some period of starvation by digesting some carbon and nitrogen from their own exoskeletons and muscles. 52 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.ed Hot spots and cold spots As for the adult krill, we discovered two "hot spots" where large populations ot krill accumulated: Labeauf Fjord in Marguerite Bay and Crystal Sound just north of Adelaide Island. The krill in these areas occurred in a dense layer be- tween 50 and 120 meters below the sea surface. We found another hot spot off the northern end of Alexander Island, a region of rough bottom topography. We are currently analyzing our data to ex- plain these hot spots. Not surprisingly, large numbers of seals, penguins, and whales also fre- quented these areas. While scientists on Palmer surveyed and counted krill, sea birds, penguins, seals, and whales, other investigators aboard Gould focused on experimental studies of seals and pen- guins. They temporarily captured a num- ber ot animals to measure their physi- ological properties and later released them. At the same time, they attached tags carrying temperature and pressure sensors and a transmitter that could send data via satellite back to a computer log- ging system. The data recovered from tagged Cra- beater seals and Adelie penguins revealed their diving and feeding behavior, and researchers discovered some movements that they hadn't suspected. For instance, Adelie penguins can dive to much greater depths and can travel farther and faster than scientists previously believed.' Be- cause the tags recorded top predators' activity for some time, we were able to see that hot spots ot krill identified during the cruises continued to be focal points for the predators long atter our ships left the area. Elsewhere in the region, to our sur- prise, krill did not make up the majority of the zooplankton population. Instead, animals more typical of other ocean eco- systems, such as copepods (small crusta- ceans) and pteropods (small planktonic snails) dominated in the water. We still believe krill are the most important part in the chain linking primary phytoplank- ton producers to the top predators, but in SHIP AT REST— The R/V Laurence M. Gould, docked after the 2002 winter cruise, dwarfs the buildings of the U.S. research outpost at Palmer Station, Antarctica. some areas, other zooplankton play im- portant roles in the ecosystem. The Antarctic frontier There is still more to learn about the ecosystem. What about the adult krill? Large adults were abundant in 2001, when the weather was milder. They were largely absent— as were the larval krill — during the second year, when conditions were colder. Where did they go? Was this related to the early onset of pack ice for- mation in 2002? Even with the icebreaker, we could not reach several places, because the ice pack was impenetrable. In these areas, we sus- pected, the adult krill would be found. Newer technologies, though, will soon help us meet the challenge of the Antarc- tic. For example, autonomous vehicles (robotic vehicles that don't need tethers) and moorings equipped with biological sensors could gather data under the ice when ships cannot take us there. Some ot these vehicles and moorings are now being developed. (See "Sensors to Make Sense of the Sea," page 68.) A more pow- erful icebreaker now being developed specifically for Antarctic research will provide better access to ice-covered seas. The Antarctic region is a formidable and sometimes forbidding place in which to work, but it is also a region of great beauty. Even more, it is susceptible to cli- mate change. It is a linchpin in the forces that cause global climate variability — since melting polar ice will create cascad- ing effects through the world. It will be important for us to be able to anticipate the impacts of climate change on the Southern Ocean ecosystem. To do that, we anticipate that future research pro- grams will build on GLOBEC's legacy of an integrated, multidisciplinary ecosys- tem approach, and we will do more work in the harsh, dark Antarctic winter. Growing up near the seashore in central California, Peter Wiebe devel- oped a love for and a curiosity about the oceans at an early age. As a youth, he spent hours free-diving in the Monterey Bay area, and he as- sembled his first scuba gear in 1954. His undergraduate studies took him to northern Arizona, a region whose oceans disappeared 40 million years ago, thus making him too late to study them firsthand. He returned to California and the Scripps Institution of Oceanography to obtain a Ph.D. in biological oceanography, and then came to Woods Hole Oceanographic Institution in 1969. Now a senior scientist at WHOI, his interests have focused most recently on the dynamics of zooplankton populations on Georges Bank and on krill living on the continental shelf region of the Western Antarctic Peninsula— two components of the U.S. Global Ocean Ecosystem Dynamics Program. For his efforts leading the GLOBEC program, the National Oceanic and Atmospheric Administration awarded Wiebe its Environmental Hero Award for "tireless efforts to preserve and protect the nation's environment." Woods Hole Oceanographic Institution 53 Run Deep, But Not Silent A new tagging device lets scientists 'go along for the ride' into the underwater world of whales By Peter Tyack, Senior Scientist Biology Department Woods Hole Oceanographic Institution Whales are among the most elusive animals that humans have ever hunted. Pursuing whales across the seas and centuries, whalers made careful obser- vations of whale behavior whenever and wherever they surfaced. But sperm whales, for example, spend about 95 percent of their time beneath the waves. Studying five percent of their behavior was enough to learn how to kill them, but it has taught us very little about how they live. But now, for the first time in history, we can accompany a whale on its dive, hear what it hears, and observe its nor- mal, natural, previously hidden behavior in the depths. Working closely together, scientists and engineers have created an innovative device— the digital acoustic recording tag, or D-tag. It attaches to a living whale and records nearly every- thing that happens on its dives, without disturbing the animal. (See "Playing Tag with Whales," page page 57.) On land, behavioral scientists spend years carefully observing animals such as wolves, lions, or chimpanzees to build up a detailed record of how they behave in response to social or environmental circumstances. Often the researchers re- main hidden, or they acclimate the wild animals to their presence, before they can trust that their observations reflect natu- ral behavior. We cannot do that with whales. We can't be unobtrusive, because boats can't be hidden. And we can't observe whales for long, because most of the time, we can't see them at all. Scientists have had no practical way to follow along on a TAG TEAM — Researchers succeed in the challenging task of using a 40-foot carbon-fiber pole to attach a revolutionary digital recording tag, or D-tag, to an elusive whale during its brief stay at the surface between dives. The tag attaches with suction and records sounds and whale movements during several dives. It releases automatically after about 12 hours. 54 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Different sounds for different purposes 200 400 600 800 regular clicks Q codas c buzzes 6 p.m. 9p.m. midnight 10 20 40 50 sperm whale's epic dives, 600 to 1,200 meters down into the cold, dark depths, on their all-consuming mission to search for enough food to keep their massive bodies fueled. Until now. Pioneering whale studies Whales live in a world of sound, not sight. Like bats, they send out and receive sound signals and are guided through the sea by what they hear — using both sounds reflected back from objects and sounds made by other whales. Sound is the currency of their lives; they rely on it for knowing where the bottom is, for finding food, and tor communicating with each other. Researchers also use sound for locat- ing whales. Nearly 50 years ago, biologist William Schevill and physical oceanog- rapher Valentine Worthington at Woods Hole Oceanographic Institution were the first to record the sounds of sperm whales, using underwater devices called hydrophones. WHOI biologist William Watkins made enormous advances in identifying which sounds are made by which species of marine mammal. So careful were these pioneering sci- entists' methods that we still use their results 45 years later. They still represent some of the best data sets available, accu- rately measuring and attributing sounds to the different whales that made them, and I have avoided many wrong turns by being attuned to this resource. With hydrophones, scientists could listen to sounds in the sea and begin to know where, what kind, and how many whales there are in an area. But what the whales were doing below the surface has remained hidden. The D tag's origin and evolution Ecologists place tags on a variety of an- imals to track their movements, and they have tagged marine animals, too: whales, dolphins, seals, turtles, and even a great white shark. Such tags record depth a few times each minute and can transmit data only when near or at the surface, giving scientists a record of the tagged animal's location and depth over time. I came to WHOI originally to develop a small tag for captive dolphins that would light up when a dolphin made a sound, allowing us to tell which indi- vidual made which sound. It worked well for captive dolphins, but I had not con- sidered using it in the wild. In the early 1990s, a graduate student at the Univer- sity of Guelph named Andrew Westgate developed the first tag that could be used on wild porpoises to record time and depths of their dives. Unlike earlier tags used on seals, it was not on a collar, but temporarily attached to the porpoise. It was designed to fall off the animal and be recovered by researchers who could then download the data. His success led me to pursue an archiving tag for wild whales, which would have a greater capacity to mea- sure behavior and sound. WHOI engi- neer Mark Johnson began to build a tag that would record not only times and depths, but also any sounds in the wa- ter— both the whale's sounds and sounds in the whale's environment. Over the last five years he has refined the D-tag into a remarkable device that attaches to a whale with suction cups and stays on during a dive, while not disturbing the animal — a critical consideration it you Woods Hole Oceanographic Institution 55 want to observe normal behavior. The D-tag records and stores what the animal is doing and what its environ- ment is like. Beyond time, depths, and sounds, the tag records temperatures in the environment surrounding the whale; and the whale's pitch, roll, speed, and di- rection. It measures this information 50 times a second. After up to 12 hours and multiple dives, the tag releases its suction automat- ically, floats, and sends out a radio signal so we can recover it aboard ship. So much data is recorded about the whale's dive that it can take three hours to download. Applying the tag The success of the tag depends on being able to attach it to a whale, of course, and that depends on having a way to reach a sperm whale from a small boat, while keeping some distance away. While working with North Atlantic right whales, WHOI biologist Michael Moore and engineer Richard Arthur developed a cantilevered, 40-toot, carbon-tiber pole, which researchers in small boats can use to deliver sedatives, ultrasonic transduc- ers for sigmoidoscopies, or a suction tag to a whale at the surface. Without this invention, we couldn't tag the whales. Even with it, it's still a dif- ficult process that requires luck, patience, decent weather, and some measure of fortitude. We find ourselves in tiny boats, trying to sneak up on large and often intractable wild animals to stick some- thing on them with a long pole, during the small fraction of time they are at the surface. Any one of our "subjects" could swim away from us or dive at any time. The work is exciting on many levels. What whales say and hear Like us, whales use different sounds for different purposes. Data from the D-tag show us that sperm whales don't waste time or energy in travel. They spend very little time at the surface, dive nearly straight down to very deep water, then spend quite a bit ot time at this "foraging depth," hunting for food, before coming nearly straight up again to the surface. When whales begin a dive to find and capture prey, they start producing sounds called "regular clicks" roughly once per second, at depths of several hundred me- ters. They use the regular clicks, it seems, to orient themselves. For most regular clicks, the tag records sound echoes re- flecting from both the ocean's water sur- face and the bottom. Sperm whales also seem to use regular clicks as a sonar to find patches of prey. But as they close in on their prey (mostly squid), they rapidly accelerate their click rate into a sound we call a "buzz," which seems to be used to locate the prey pre- cisely enough to capture it. Whales also use sound to commu- nicate with each other. The D-tag has revealed that they make rhythmic pat- terns of clicks called "codas" not only when they are near the surface, but also during the start of their descents and the end of their ascents, when they interact with one another during their dives. We have tagged two to three sperm whales at the same time and have discovered, after downloading data from the recovered tags, that the whales dived in synchrony, on similar dive tracks to the same depth. They maintained a steady distance be- tween each other, apparently by listening to each other's regular clicks. Using the D-tag on a smaller toothed whale called a beaked whale, Mark John- son and WHOI biologist Peter Madsen, working in my lab, have been able, tor the first time, to record and hear not only the sounds a whale makes when foraging, but also the echoes reflecting off the prey, returning to the whale, and recorded by the tag. The tags have even captured the sound of prey being captured. Noise pollution Whales also hear, and react to, sound from other sources, including boat en- gines, military sonar, or airguns used to explore for oil and gas beneath the seafloor. We don't vet know the exact range of frequencies they hear, but the D-tag will allow us to investigate whales' responses to different ambient sounds. Ongoing studies on whale ear anatomy by Darlene Ketten at WHOI can give in- formation on what frequency range they are likely to hear (See "How to See What Whales Hear," page 59.) There is grow- ing concern that human-generated sound may interfere with the whales' navigation, feeding, communication, and lives. During a sperm whale cruise that happened to coincide with the invasion of Grenada, Bill Watkins and I found that sperm whales become silent when exposed to sonar sounds, and when ex- posed to airguns, they have reduced rates of buzzes associated with catching prey. We don't know yet how much of an inter- ruption ot their normal feeding this can cause, or the possible ramifications it may have on reducing the energy available tor their growth and reproduction. The D- tag can tell us what happens on multiple dives ot a single animal and also lets us compare dives of many different animals, so that we can build up a library of a pop- ulation's behaviors. The future of this work is immensely exciting. We will be able to learn what whales have known for eons — what their lives are like. We hope it will also help to protect them from unintended impacts of seagoing humans. Peter Tyack writes: "My parents had me sleeping in the sail bag of a daysailer in Manchester Harbor at seven months old, and I have always loved going to sea. Intrigued by animal behavior and wanting to do field re- search, I went to Harvard in the early 1970s, as the fields ot behavioral ecology and sociobiol- ogy came of age. I initially majored in biologi- cal anthropology, fascinated by primate social behavior. But a course with WHOI biologist William Schevill on cetaceans convinced me that marine mammals were just as fascinating and offered many more unexplored research opportunities. From then on, I studied acoustic communication and social behavior of whales and dolphins. Donald Griffin and Roger Payne made it possible for me to do Ph.D. research at Rockefeller University on the songs of hump- back whales. After that, I came to WHOI, where I have happily worked ever since." 56 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edi Playing Tag with Whales Engineers overcome nightmarish specifications to create a dream instrument By Mark P. lohnson, Research Engineer Applied Ocean Physics £ Engineering Oept. Woods Hole Oceanographic Institution The challenge of designing a device to learn what marine mammals do on dives is the stuff of dreams for an elec- tronics engineer. In the spring of 1999, the time was right to build the digital acoustic record- ing tag, or D-tag — an instrument to re- cord the movements of whales and the sounds they make and hear in the ocean. Miniature cell phones, MP3 players, and Personal Digital Assistants had created a demand for small, lightweight, dense memory components and batteries. In many ways, the tag is just like an MP3 player, PDA, and home medical monitor rolled into one, and then sealed against seawater and pressure in the deep ocean. Helped by electronics engineers Tom Hurst and lim Parian at WHOI, and a summer student studying mechanical en- gineering, Alex Shorter, we put together the first D-tag in record time. Driving us was an opportunity in the summer of 1999 to use the tag on endangered North Atlantic right whales, as part of an effort to understand why they are hit by ships all too often. A small, chock-filled package The D-tag is actually a miniature computer with its own microprocessor, memory, and software. It records sound using one or two hydrophones (underwa- ter microphones) with better-than-CD quality — not only the sounds made by the tagged whale but also sounds from other whales, noises from boats, and all of the sonars and sound sources in the area. The tag also contains a digital com- pass, a pressure sensor (the underwater equivalent of an altimeter) to measure the depths of a whale's dive, and an orienta- tion sensor that measures the animal's pitch and roll. The pitch sensor records the whale's body undulations fast enough for us to count each beat of its tail fluke. Think ot the displays in the cockpit of a small plane: The tag sensors are measuring similar things but under water. Everything gets stored in digital form. The tag has as much as six gigabytes of memory, enough to record continuously tor a full day. Putting it on, getting it back To keep out the saltwater and survive harsh treatment from socializing ani- mals, the tag has a plastic skeleton and is sealed inside a thick urethane bag. To keep the weight and size down, the tag does not have a pressure housing (the aluminium bottle normally used to pro- tect electronics from high pressure in the deep ocean). Instead, we spent a lot of time at the WHOI pressure-testing facil- ity choosing electronic components that would withstand pressures of up to 3,000 pounds per square inch — that's 200 times atmospheric pressure at sea level. As a re- INVENTIVE COLLABORATION— Engineer Mark Johnson (right) and biologist Peter Tyack work together to learn about whale behavior, using Johnson's D-tags to record whale movements, depth, and sounds on dives. Back in the lab, D-tag data tell the story of the whales' dives, from their swimming behavior to the kinds of vocalizations they use while foraging. Woods Hole Oceanographic Institution TAGGED — D-tags were placed on deep-diving pilot whales in a collaborative project with the University of La Laguna, Canary Islands, to study their behavior during dives and in response to ferries and whale-watching boats. suit, the entire electronics unit measures about 4 by 1.5 by 1 inches and weighs about 5 ounces — no problem for even a small whale to carry. To allow us to retrieve the tag after it comes off the whale, it is equipped with flotation so that it rides atop the surface like a buoy, and a tiny radio beacon, so we can find it by tracking its radio signal. Of course, the tag is no use at all if it doesn't stick to the whale, and so we have spent a lot of time studying suc- tion cups. For three years, we tested ev- ery suction cup we could find to figure out which would hold best. Finally, we decided that we had to build the cups ourselves to get the right mix of strength and softness — to be tenacious and yet not hurt the whale. Using a mold built by the WHOI shop, we now make cups out of medical-grade silicone that work incredibly well. New heights (and depths) for D-tag That first caffeine-powered field sea- son in 1999 — working with northern right whales in the Bay of Fundy with the International Fund for Animal Welfare- was just the start. Since then, D-tags have been used on more than 30 field expedi- tions all over the world. We have worked with D-tags on sperm whales in the Gulf of Mexico and Italy, on manatees in Belize, on narwhals in north- ern Canada, on beaked and pilot whales off the Canary Islands, and on hump- backs oft Australia and Cape Cod. Col- leagues have taken the tags to Antarctic islands to study fur seals and to Califor- nia and Canada to work on blue whales and gray whales. D-tags have gone on the deepest dives ever recorded on a marine mammal and have discovered the sounds made by two of the world's most mysterious whales: Cuvier's and Blainville's whales are little-known mid-si/.ed beaked whales whose only claim to public attention is their occasional mass strandings as- sociated with sonar use during naval maneuvers. Many marine mammalogists have never seen these whales alive. They are very shy and usually live way out in the big blue. They are so inconspicuous at the surface that you can sail right by them unless the sea is flat and you know what to look for. We have learned that these whales are incredible divers. Using D-tags, we have recorded dives 85 minutes long with depths of up to 1,900 meters. Amazingly, the tag is sensitive enough to hear echoes from objects in the water, insonitied (lit up — but with sound) by the click sounds made by the beaked whales. An increasingly noisy ocean Marine mammals are one of the least understood groups of animals. D-tags allow us to explore the world the way marine mammals do: with sound. (See "Run Deep, but Not Silent,"page 54.) Meanwhile, human noise in the oceans is increasing by the decade as more and faster ships are made, as oil exploration moves into deep water, and as navy ships with high-power sonars patrol for submarines. There are ample signs that these noises can disrupt marine mammals, even causing mass strandings and death. But without a more complete understanding of how whales use and sense sound, we cannot begin to figure out which noises are problematic and at what levels (See "How to See What Whales Hear," page 59.) My hope is that this device will even- tually help us learn how to be better neighbors under water. Mark Johnson grew up in New Zealand, that southern paradise with a beach for every person (and sheep). He was always close by the ocean — which defined everything. A box of tran- sistors thrown out by an electrician neighbor lured him into the world of electronics, sound, and music. He studied engineering at the University of Auckland and pursued a Ph.D. working on anti- noise (an electronic method to cut down noise) at the Acoustics Research Center in Auckland. Tak- ing a "holiday" job at WHOI in 1993, Johnson was drawn into Peter Tyack's marine mammal group. Now in the twelfth year of his holiday, the D-tag project has sent him traveling around the world and given him the opportunity to work with some amazing animals— and biologists. When not fol- lowing whales, he gets as far away from the ocean as possible: Deserts and mountains tend to stay still under your feet. 58 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag. How to See What Whales Hear Biomedical imaging reveals new insights into marine mammal ears By Darlcne Ketten, Senior Scientist Biology Department and Kate M.ul i n, Science Writer Woods Hole Oceanographic Institution On summer nights, if you sit qui- etly at the edge of a field or watch the edges of the light pools around street lamps, you will see bats swooping through shadowy darkness in search of moths or other flying prey. They detect and catch their targets through echoloca- tion, or biosonar, the animal equivalent — and precursor — to man-made sonars. Bats generate signals in their nose and throat that produce echoes, which the bats monitor to determine the size, shape, speed, and direction of their prey, as well as other objects in the area. Biosonar is also how they navigate in dark caves. Bats' large, distinctive, convoluted, mobile ear flaps are critical for the fine-grain acous- tic analysis they do during echolocation. Now flood that field with seawater and make it not only dark but profoundly deep and filled with a myriad of exotic creatures and objects. That is the dim and complex world in which whales live. Although whales and dolphins are air- breathing mammals, they spend approxi- mately 85 percent of their time under water. Compared to sound, light does not penetrate water well, and it is not surpris- ing that whales and dolphins rely primar- ily on hearing rather than sight to sense their environment and communicate. The Odontoceti — toothed dolphins and whales that hunt fish, squid, and other prey — evolved parallel abilities with bats, actively using clicks and pulsed sounds tor underwater echolocation. However, there is one very striking difference between bats and dolphins. The latter appear to have no outer ears. Dolphins and whales abandoned external ears as a concession to better underwater mobility. Still, they do have ears buried inside their heads: fascinating ears in fact, with exceptional range that operate at extraordinary depths. With the help of a common medical tool — biomedical computerized tomog- raphy, more commonly known as CT and MRI scanning — we are beginning to get inside the heads of whales and dolphins. Using biomedical imaging techniques, we can thoroughly explore just how their ears are constructed — and see how and what they hear. Into the inner ear Whale hearing is difficult to study by conventional methods. Whales are large, elusive, diverse creatures, and research on most species is substantially restricted because of their endangered status. One approach to learning how whales hear is reverse engineering, which is essentially the clockmaker's child approach to sci- ence. We can examine stranded animals to determine not only what may have caused their deaths, but also, literally, what makes them tick. Virtually all mammals have the same three basic ear components: an external ear flap, or pinna, is connected via an ear canal to the middle ear cavity, which has an eardrum and bony lever system READY TO SCAN — Postdoctoral Investigator Soraya Moein Bartol and Senior Research Assistant Scott Cramer position an Atlantic white-sided dolphin, which stranded and died, on the WHOI CT scanner bed before imaging, while CT technologist Julie Arruda (front) examines previously generated images. Woods Hole Oceanographic Institution for amplifying sounds, and then an inner ear, which transduces sounds into neural impulses. In marine mammals such as seals and otters, the pinnae are reduced to allow them to swim faster; in whales and dolphins, the sleekest and fastest of marine mammals, these outer ears are gone completely. Traditionally, investigating the in- ner workings of whales and dolphins has been done by dissection. But to examine the parts, you are compelled to disassem- ble the relationship of those parts, which is fundamental to understanding their effective operation. Even worse, conven- tional dissection requires time, espe- cially when the subject outweighs you by several hundred pounds. By the time you can get to many structures, they have de- teriorated beyond recognition. We knew there are robust, complex inner ears buried deep in dolphin and whale heads, but we did not know how sound gets into those inner ears. Seeding an innovative idea At WHOI, we took a different ap- proach; or rather, we updated the tradi- tional one. We still dissect, but our dis- sections are digital. Biomedical scanning rapidly and non-invasively reveals in great detail the internal structure ot the object or animal that is imaged. We can use im- aging techniques to see into most living animals. To image rare and deep-ocean materials, we do not need to remove them from their protective containers. Above all, we see the synergy of inter- nal structures. For ill or stranded animals, we can locate and examine pathologies or traumas non-invasively — precisely what scanners were designed to do tor humans. The idea ot using a CT scanner to probe inside marine mammals was a rad- ical idea a decade ago. In 1998, with fund- ing from the Andrew W. Mellon Indepen- dent Study Award program at WHOI and from The Seaver Institute, the first large- scale study of marine mammal auditory systems using computerized tomography was undertaken using CT and MRI scan- VISIBLE HEARING— This 3-D CTscan image of a blue whale's inner ear (18 millimeters in diameter) shows typical mammalian inner ear structure, including a spiral cochlea and the vestibular system that controls balance. ners in area hospitals. This study dem- onstrated the extraordinary potential of scanning for marine mammal research, since it allowed high-resolution anatomi- cal surveys of many individual animals in an unprecedentedly short time. In 2000, the Office of Naval Research, and particularly Admiral Paul Gattney, former Chief ot Naval Research, fur- thered the effort by providing start-up funds to install a high-capacity CT scan- ner at WHOI that was dedicated exclu- sively to marine research. How CT scanners work CT scanners use X-rays to produce an image of density differences of internal structures. The denser an object, the less X-ray energy is transmitted through the object to the detectors, and the brighter the object in the image. For this reason, bone appears white, air looks black, and soft tissues are varying shades of gray in an X-ray. In common single plane X-rays, such as chest films, the detector is a sheet of film that is exposed by a single pulse from the X-ray tube. Consequently, the output is a flat image in which one struc- ture overlays another. CT scanners employ a bank of elec- tronic detectors that monitor the X-ray attenuations from multiple pulses and po- sitions, as the X-ray tube moves through an arc around a patient or specimen. This complex, multi-dimensional matrix of at- tentuations is then deconvolved to gener- ate images that represent the attenuations in thin cross-sections. It is, in a very real sense, a virtual dis- section, slice by slice, of all structures. The WHOI scanner allows us to image slices as thin as 0.1 millimeters and to de- tect attenuation differences that are sev- eral thousand-fold. Using scanning techniques to look at whale and dolphin ears, we can study the geometry and composition of ears and other head tissues from microscale to macroscale and thereby gain insights into what and how they hear. We also see sometimes how they were damaged. The impacts of sound Sound is energy. The louder a sound an animal can hear, the greater the po- tential tor damage to its ear. Some loss of hearing from day-to-day wear and tear is normal; some is excessive and avoidable, as far too many of us are well aware from exposure to loud music, power tools, or other intense sound sources. However, just to complicate matters, not every sound is equally dangerous to all ears. Because different species have differ- ent hearing capacities, what is impercepti- ble to one animal may be annoying or even harmful to another. An ultrasonic dog whistle is imperceptible to humans but clearly heard by any normal dog or cat. Even more important, the effects of sound can range from the physical, with actual damage to parts ot the auditory system, to behavioral; sounds so disturb- ing that animals abandon normal activ- ity, such as feeding and breeding, or even alter their migration paths. Both physical and behavioral effects potentially have serious impacts on indi- viduals or on entire species. Consequent- ly, understanding hearing in marine mammals is not just a matter of curiosity, but fundamental for marine conserva- tion and possibly even for the survival of some species. 60 Oceanus Magazine • Vol. 43, No. 2 • 2005 Ships, sonars, and strandings The ocean is a naturally noisy place. Sounds are generated by volcanism, wind, waves, earthquakes, and by animals themselves. However, all human activi- ties in or near the water are adding to this natural suite of oceanic sound. In recent years, mass strandings of whales — in Greece in 1995, the Baha- mas in 2000, and the Canary Islands in 2002 — have focused attention on the pos- sible effects of man-made sound in the oceans. In those cases, multiple U.S. and NATO ships were engaged in exercises employing multiple and intense sonars in narrow straits. While the presence of these ships and the exceptional sound field produced by the exercises clearly coincided with the strandings, we are not yet able to de- termine exactly what mechanism led to them. We examined many of the strand- ed animals using our scanner system and found distinctive traumas, but the damage is not strictly acoustic. Rather, it appears to be more consistent with stress than directly sound-induced. In other cases, however, we have found damage to ears, often from aging or long-term noise exposures that clearly impaired the animals' hearing and there- tore their ability to function in the wild. At this point, we do not know precisely what noises are most harmful, either di- rectly or indirectly, to any marine mam- mal species, but this is a critical area of research that we must pursue intensely and rapidly. The inside story of dolphin ears One ot our first major discoveries answered the original mystery of the missing external ears: Without external pinnae and no obvious canal, how does sound enter dolphins' heads and how does it get to the inner ears? Researchers had speculated that since dolphin inner ear bones were located near their jaws, perhaps the soft tissues and bone of the jaw played a role. Unfor- tunately, that was hard to prove, because INTERNAL EARS — A 3-D image generated from a CTscan highlights selected tissue groups of a bottlenose dolphin's head. It shows the relationships of the exterior skin (blue), brain (pink), inner ear bones (red), and specialized auditory fats (orange). The fats form paired lobes inside the head along the jaw and are very similar in shape to the outer ear flaps (pinnae) of bats. fat tissue in the area deteriorated rapidly and the relationships between tissues were disrupted as soon as they were cut during dissections. CT scanning gave us the first undis- turbed images of this region. In fact, it provided the critical clues: The fatty lobes near the jaw were connected to the ear and had shapes similar to bat pin- nae. In effect, bats and dolphins seem to have parallel ear evolution. Dolphins have pinnae that are just as complex and large as bats, but they are internal — an advantage under water both hydro- dynamically and functionally; these specialized tats have acoustic proper- ties similar to seawater. Consequently, in terms of both shape and physics of sound in water, they are the aquatic analog of land mammal outer ears that were designed to capture and conduct airborne sound. The speed of sound in water Scanning also allowed us to mea- sure the locations of dolphin ears in situ, which explained why the ears are spread so far apart in dolphin heads. Dolphin ears are widely separated to accommo- date the speed of sound in water, which is 4.5 times taster than in air. One clue to determining the location of a sound source is the difference in ar- rival time between your ears. Humans have trouble locating sound sources under water, because, acoustically, our heads "shrink" nearly five-fold because of the increased speed of sound through water. As dolphins evolved, they expanded their heads and inter-ear distances to match sound speeds in water, which explains their extraordinary ability to localize sound sources three times better than humans. Scanning also provided the first data on the inner ear of the true behemoths of Woods Hole Oceanographic Institution 6 A SECRET SEEN — This 3-D image shows an intact, near-term fetus discovered inside an Atlantic white-sided dolphin that stranded and died. The fetus's flippers are folded and its ribs are lightly mineralized, but the cross-section reveals fully matured ears. the oceans. Blue and fin whale ear bones are massive, approximately the size of a human brain case and at least twice as dense. To demineralize these ear bones to dissect them by traditional methods would take more than two years. With scanning, we can digitally slice them to see inner ear features in less than an hour. Anatomy reveals hearing capacity Although all mammal ears have the same basic parts, there are some important differences among species in some struc- tures that account for differences in hear- ing capacities. No two species have exactly the same hearing ability. Different animals can detect different frequency ranges and have different sensitivities at any one fre- quency. Most mammals hear frequencies well above the range ot human hearing, termed ultrasonics. Some also hear well at very low frequencies, even the seismic sounds generated by earthquakes. To study both normal and abnor- mal hearing, our laboratory has used the scanner to image all parts of the auditory system of more than 30 species of marine mammals. Each ear from an unknown hearer is compared with those from species with well-documented hearing character- istics. In particular, we construct "maps" of the stiffness and mass of ear components of animals whose frequency ranges are known and compare the stiffness and mass of newly imaged marine mammal ears to calculate their resonant frequencies. Thus, we can determine the critical commonali- ties for hearing in all mammals — as well as critical differences for specialized hearing like echolocation and for hearing under water instead of in air. We also make maps this way for the few marine mammals species for which hearing has been tested. These are our model controls, as our maps are consis- tent with audiograms or hearing curves of tested animals. The new ear maps from untested species have led to the discovery that whales have some of the widest hear- ing ranges of any mammal and that some species are capable of hearing at seismic or hyper-ultrasonic frequencies. We now know that some species of whales have a 12-octave hearing range, compared to eight in humans. Some whales hear well down to 16 hertz (or cycles per second), versus our lower limit ot 50 hertz, while others hear as high as 200 kilohertz. The typical high-frequen- cy cutoff for humans is 16 kilohertz. For bats, it is 60 to 70 kilohertz. This work is coordinated also with other WHO1 laboratories doing basic research on marine mammal sounds, div- ing, and foraging behaviors, as well as ap- plied research on acoustic devices to warn highly endangered species of impend- ing ship strikes. (See "Run Deep, But Not Silent," page 54 and "Whither the North Atlantic Right Whale?" page 29.) So far, we know there is no single sound bite that is perceptible or harmful to all marine creatures, but with luck, we may be able soon to provide guidelines that will help preserve some of them. I ~\arlene Ketten is a neuroethologist, studying how behavior is linked to sensory system anatomy in various species. She started out to be a Ro- mance language specialist but discovered as an undergraduate that biology opened many more mysterious worlds inside the heads of exotic animals. While working on her doctorate at The Johns Hopkins Medical Institu- tions, she began using computerized tomography (CT and MRI scanning) to explore how biomedical imaging techniques could be used to investi- gate how inner ears in different species are structured and coupled to the rest of their heads. This led to micro-imaging work at Harvard Medical School to improve diagnosis of causes of hearing loss in human ears. In 1997, she joined the Biology Department of Woods Hole Oceanographic Institution and brought her combined backgrounds of neuroethology and neuroradiology to bear on modeling hearing in marine mammals based on their specialized auditory system anatomy, and most recently on analyzing potential effects of man-made noise in the oceans. In addition to basic research, she does specialty forensic analyses ot heads and necks of stranded animals for NOAA National Marine Fisheries Service investigations. Although much of her work involves mathematical models and 3-D software, she has never lost her prefer- ence for working directly on the "wetware." 62 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Peering into whale heads— with- out the loss of tissue and time that normal dissections cause— was the initial motivation for using a CT scanner for marine mammal re- search, but our current scanner has had more than its share of other types of species and objects. Some of the specimens scanned here, particularly to assist the work of other research- ers, have been remarkable. Scan data obtained at the WHOI facility have proven invaluable for in- vestigating everything from diagnosing sinus infections in live, sneezing seals to imaging shark balance organs, coral reef fish swim bladders, flippers of all forms, fractures in great whale jaws, oral reef growth patterns, pressurized CT scan menagerie ocean sediment cores, and, most exotic of all, the complex mineral substruc- ture of hydrothermal vent chimneys. Animals as small as grass shrimp have been scanned to help modelers determine how much sound energy large groups of similar invertebrates, called krill, reflect at different fre- quencies. Acoustical oceanographers use such models to determine whether reflected signals at sea actually repre- sent deep layers of millions of krill in patches throughout the oceans. Land creatures that also have been scanned in the last two years include tigers, hedgehogs, bats, and even an elephant and a hippopotamus (parts only— they are just a tad too big for whole ones to fit on the table). In 2005, the scanner is scheduled to move into a new facility on the WHOI Quisset campus. Moving the scanner is not trivial; in fact, the scan- ner has a good deal in common with the megalithic money on Yap. Both are giant toroids that, once in place, are daunting to shift. The scanner move will require two engineers, a rigging crew of up to six workers, and two weeks of disassem- bly and reassembly time. Still, the ef- fort will be worth it, as the new facil- ity incorporates overhead hoists anc tracks connecting the scanner room with surgical and storage facilities that will allow us to transport, scan, and understand an even wider range of creatures that may come our way. MEGALITHIC TO MINIATURE— The WHOI CT scanner is a unique resource for scientists studying internal structures in animals. Both marine and terrestrial animals have been scanned to let scientists "look inside." Among specimens examined this way are (clockwise from lower left): a mandible (lower jaw bone) of a North A tlantic right whale, prepared for scanning by MIT/WHOI graduate student Regina Campbell-Malone and CT technologist Julie Arruda; a large core section of coral, with an intricate internal canal structure that once housed coral polyps, positioned on the scanner bed by scientists Anne Cohen andHanumant Singh with Arruda; a Siberian tiger head, for research by Edward Walsh of Boy's Town Research Hospital to determine what tigers hear and how they protect themselves from their own extraordinar roars; and a live bat, carefully cushioned and sedated, watched by biologist Darlene Ketten, for ONR-funded research by James Simmons of Brown University to help understand bat ears and echolocation. Woods Hole Oceanographic Institution 6' Revealing the Ocean's Invisible Abundance Scientists develop new instruments to study microbes at the center of the ocean food web By Rebecca Cast, Associate Scientist Biology Department Woods Hole Oceanographic Institution Microbes. They are invisible to the naked eye, but they play a criti- cal role in keeping our planet habitable. They are everywhere, in abundant num- bers, but are still difficult to find. They come in a multitude of varieties, but too often are difficult to distinguish from one another. Wherever there is water (fresh or salt), there are usually microbes — microscopic, single-celled organisms. In the ocean, they form an unseen cornucopia at the center of a food web that ultimately nour- ishes larger organisms, fish, and people. Their fundamental role in the ocean's food supply makes them critical targets for study, and scientists would like to know much more about them. They would like to identify them and count them. They would like to learn more about how marine microorgan- isms (part of what we call plankton) eat, grow, reproduce, and interact with other organisms. They would like to deter- mine how changes in the ocean might affect the microbial communities' vital- ity and viability. Finding minuscule life forms in a seemingly infinite ocean isn't trivial. But in recent years, oceanographers have been developing new techniques and instruments to identity and count marine microorganisms. Year by year, we are learning more about them and discovering that they are even more numerous, varied, and important than we thought. A diverse microbial community Some marine microbes are bacteria, or prokaryotes — simple cells with no specialized organelles, which are among the smallest of living things. Others are eukaryotes — larger and more complex cells with a nucleus, mitochondria, and other organelles. Eukaryotic microbes, also called pro- lists, include both producers, such as algae, and consumers, such as protozoa. They thrive in a variety of habitats— liv- ing suspended in the water, in bottom sediments, or on other objects. They form communities, or assemblages, of different species that photosynthesize, consume each other, and are, in turn, consumed by other things in the ocean's food web. In the last few years, we have consider- ably advanced our knowledge of the struc- A Gallery of Protists A heliozoan is heterotrophic, meaning it consumes both plant and animal matter. Tintinnids have transparent, vase-like shells for protection. Thye are consumers of a wide variety of cells and detritus. , Diatoms (such as Corethron, above) are at the center of the food web, using photosynthesis to live, grow, and multiply. 64 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edi ture and function of these assemblages — particularly planktonic assemblages that we sample by collecting the water they inhabit. We now know that these plank- ton assemblages are diverse, composed of species with widely different sizes, growth rates, and nutrition. Not surpris- ingly, we know more about the larger pro- tists (greater than 100 microns) than the smaller ones (under 20 microns). Larger protists are easily visible using light or electron microscopes. They have features that remain intact throughout procedures to sample, preserve, and examine them, which can break or distort cells. These features are often lacking in the smaller organisms; and if they are present, they are harder to see and characterize. Identifying protists has always in- volved some type of microscopic analysis, with someone looking at the shapes, or morphology, of the cells. But now we also use molecular methods— techniques that give scientists the ability to detect and identify the presence of even small pro- tists based upon their DNA in water sam- ples. Scientists have begun to describe the genetic composition of communities of species that live and interact in the same water. Our next objective is to overcome several technical challenges so that we SHORE TO SHIP— WHOI researchers Alexi Shalapyonok, Heidi Sosik, and Robert Olson (left to right) carefully load the FlowCytobot onto a WHOI research vessel for installation on the seafloor at the Martha's Vineyard Coastal Observatory. The instrument counts and identifies protist cells in the water, and the data is transmitted via undersea cable back to shore. can routinely monitor changes in protist populations over time. Sampling the invisible So tar, all of our detection and iden- tification techniques, both morphologic and molecular, have relied on collecting samples from remote sites and analyz- ing them in laboratories. But these tech- niques don't give us all the information we need. Collecting samples from ships means physically taking separate water sam- ples, at separate times, in separate places. Samples taken this way are, quite literally, just single samples— of one location at Single-celled organisms are critical links in the ocean's food web. Though ubiquitous and abundant, their microscopic size make them hard to sample and study. These protists, all found in Antarctic waters, are between 20 and 100 micrometers. Viewed end-on, the diatom Coscinodiscus is a study in symmetry and pattern, reminiscent of a sunflower's seeds. The dinoflagellate Dinophysis , plump and harmless-looking, produces a toxin that causes diarrhetic shellfish poisoning. Dictyocha, a silicoflagellate, has an intricate, internal glassy skeleton and a starry shape that helps it avoid sinking. Woods Hole Oceanographic Institution 6'. OVER THE SIDE — The Submersible Incubation Device hangs from a cable, ready to be moored on the sea bottom, where it will take samples of surrounding seawater and measure photosynthesis in the ocean. one time. They don't provide a continu- ous picture of protists in a given area of the ocean. And they don't allow us to detect how the protists respond to rapidly changing environmental conditions. What researchers want is the ability to collect and analyze samples over long time periods in the ocean; to have a con- tinuous sampling and recording proce- dure, and to obtain data in as close to real time as possible. Overcoming engineering hurdles Several technical challenges, how- ever, still make it difficult to remote- ly detect and count microbes in their own environment. One is the number of organisms, or microscopic cells, in a given water sample. In most marine planktonic environments, microbes are present in low numbers and organisms targeted for study may only be a small proportion of the total population. To overcome this low density, researchers in the laboratory must often concen- trate several liters of water into a much smaller volume for analysis by pass- ing it through filters designed to retain the protists, then resuspending them in smaller volumes for analysis. Once water samples are collected and concentrated, microbes can be analyzed in several ways, so automated systems must be designed to accommodate the analysis method. For instance, if scien- tists want to use only the organisms' ge- netic material to identify them, collection systems must be able to break open cells and collect their DNA. If they want to study the whole organisms, though, the systems must keep the cells intact. In fact, researchers are already devel- oping instruments that can either detect a genetic signal from a microbial popula- tion or monitor one of its biological ac- tivities— and do it autonomously, without requiring scientists to be on the scene. The instruments can be programmed to collect water samples over periods ranging from hours to months and spaces ranging from inches to miles — depending on the particular microbes and biological activities scientists want to study. The in- struments inject water into flexible bags containing a solution that preserves cells tor later examination. SID, ESP, and FlowCytobot Three examples of instruments for remote analysis of marine microbes have been developed to solve many technical problems. The Environmental Sample Processor, developed by Chris Scholin at Monterey Bay Aquarium Research Institute, attach- es to a mooring anchored to the ocean bottom and collects and preserves water samples. It extracts nucleic acids from the protists in the water and detects specific organisms by their DNA. It can also pre- serve samples for microscopic analysis in the laboratory. Researchers have already used it to detect species that cause harm- ful algal blooms and to distinguish types of planktonic larvae in the ocean. It will soon have even greater capacity to detect and distinguish organisms. The Submersible Incubation Device, a moored instrument developed by Craig Taylor at WHOI, determines levels of photosynthesis in the water around it by robotically measuring carbon dioxide taken up by phytoplankton in the sam- ples. Up to 50 of these experiments can be performed before the instrument needs to be removed from the ocean to analyze the samples and determine what species are present. A third instrument, FlowCytobot, is a submersible flow cytometer — a device that counts single cells flowing through it. Developed by Robert Olson at WHOI, it is also anchored to the seafloor near the coast. It counts and analyzes micro- bial cells in the water continuously for up to two months. FlowCytobot identifies microbes by the way they scatter light, 66 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu or by the way certain pigments in the cells emit fluorescent light. (See "Little Things Matter A Lot," page 12.) Because it samples continuously, scientists can see changes in plankton populations over time that cannot be detected by tradi- tional sampling. A coastal observatory network The ultimate goal is a continuous, re- mote system that can detect, distinguish and count microbes in the environment. In the laboratory, scientists can do all these things by filtering samples, identi- fying DNA within them, and examining microbes under microscopes. But design- ing, programming, and building a system to carry out all of these steps remotely is a challenge. One of the difficulties is that DNA analysis requires heat, which requires power. Remotely deployed instruments depend on batteries for power, and add- ing batteries quickly makes instruments too heavy, big, and costly to build. To overcome this hurdle, scientists have sought a viable alternative: developing long-term installations of instruments powered by cables from a nearby shore. In recent years, several coastal ocean observatories have been built that have cables linking power nodes on the ocean floor with shore-based facilities. One of these is near Woods Hole at the Martha's Vineyard Coastal Observatory (MVCO). Instruments plugged into seafloor nodes receive power from the cables and trans- mit data back via the cables. This level of available power has stimulated the de- velopment of new biological sensors and methods that will let scientists take mea- surements continuously and accurately. We are developing several instrument modules, for example, into the Flow- Cytobot automated system at MVCO (http://www.whoi.edu/insstitutes/coi/fa- cilities/mvco.htm) The system will detect microbial cells, identity them genetically, and obtain accurate counts of particular species. It will let us monitor specific mi- crobial populations that play significant TIRELESS UNDERSEA WORKER— The robotic Environmental Sample Processor (ESP) lifts off the deck and begins its journey to the seafloor off Monterey, Calif. It will be moored there for a lengthy stay and take repeated samples ofprotists in the water. roles in the food web and detect changes taking place daily. The development of new sensors is also important to national efforts to build an infrastructure of ocean obser- vation systems. Ocean observatories are the wave of the future in many fields of oceanography. Some will monitor coastal water; others will monitor the open ocean. Many already exist, and many more are being planned through sev- eral national programs. These programs will incorporate existing coastal obser- vatories into a network, expand their research capabilities, and build more observatories at key coastal sites. We will use the observatories, each with seafloor cables supplying power, to collect and share information on a previously invis- ible microbial world — the broad group of tiny cells that control the coastal ocean's food supply. B: ( iologist Rebecca Cast uses molecular methods to study the mi- 'croscopic ocean. An associate scientist in the WHOI Biology Department, she examines the ecology of single-celled non-bacte- rial organisms, or protists, in the marine environment. Her work is often based in the Antarctic, where she studies protists in seawater, sea ice, and slush. She is interested in their diversity, distribution, and abundance, and how their proteins function in the extreme cold. Beck)' received her Ph.D. from the Department of Molecular Genetics at Ohio State University in 1994, and then came to WHOI as a postdoctoral scholar, where she has remained, keeping warm between visits to the ice and slush. In other projects, she studies sym- biotic relationships of protists— where they occur and how they function. She is developing techniques to detect human pathogenic organisms (Giardia and Cryptosporidium) and invertebrate parasites (Quahog Parasite Unknown or QPX, a parasite in clams) in coastal ocean waters. Woods Hole Oceanographic Institution 67 Sensors to Make Sense of the Sea An expanding variety of sensors is changing they way we monitor dynamic ocean systems By Scott Gallager, Associate Scientist Biology Department Woods Hole Oceanographic Institution In science, the key to understanding any situation is careful observations and measurements. The key to observing and measuring, however, is being there- in the moment— and that has always proved challenging for oceanographers. It is difficult and expensive to go to sea, hard to reach remote oceans and depths, and impossible to stay long. Like scientists in other fields, oceanographers use sensors to project their senses into remote or harsh environments for ex- tended time periods. But the oceans pres- ent some unique obstacles: Instruments are limited by available power, beaten by waves, corroded by salt water, and fouled by prolific marine organisms that accu- mulate rapidly on their surfaces. The oceans also surpass the limits of human observation at both extremes. It takes a long and large perspective to mea- sure the exchange of greenhouse gases between Earth's entire atmosphere and oceans, over seasons or decades. On the other hand, chronicling the transfer of gas molecules at the interface between air and water requires a nanosecond-short, millimeter view. Once again, sensors can extend observations to detect phenomena beyond human capabilities. But it takes a wide spectrum of sensors and platforms to survey whale populations and their global migrations, while simultaneously collecting information on the microscop- ic plants and animals that whales eat. Today, rapid advances in micro- and nanotechnology, biotechnology, com- puting power, and sensor integration are fueling development of a new generation of low-power, cost-effective, high-preci- sion sensors that will withstand extended deployments in harsh environments and be able to relay data in real time. What's more, these sensors will be mounted on an expanding variety of observatory plat- forms that provide unprecedented access: satellite imaging systems, autonomous underwater vehicles carrying sensors on wide-ranging surveys, and ocean obser- vatories with cables that continuously transmit power to instruments and send their data back. In July 2003, the WHOI Ocean Life Institute and Deep Ocean Exploration Institute, along with the National Sci- ence Foundation and the Office of Naval Research, sponsored a workshop called Temperature (°C) Abundance of copepods Time (decimal day) Time (decimal day) OBSERVING THE SEA FROM SHORE — A variety of sensors on ocean observatories provide running data logs on changing conditions in the sea. At left, temperature and salinity data from the seafloor to the surface off Martha's Vineyard over three weeks (day 274 to 296), collected by the Autonomous Vertically Profiling Plankton Observatory (AVPPO), show distinct water layers at the start that become less distinct. (Saltier and warmer waters are red; colder, fresher waters are blue.) At right, a video plankton recorder on the AVPPO captures images of tiny planktonic animals called copepods, while compiling a record ofcopepod abundance over three weeks (middle). The data shows that during a passing storm (days 277 and 278), the copepod population swam down to keep away from surface waves. 68 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu Monitoring An Ecosystem The Polar Remote Interactive Marine Observatory (PRIMO), scheduled to be deployed off Antarctica in 2006, will be the first cabled observatory capable of remaining un- der the ice for a year. It receives power from and sends data back through an electro-optical cable to Palmer Station in Antarctica. A winch system drives an instrument platform up and down between surface waters and the seafloor. It is equipped with instruments that measure salinity, tempera- ture, depth, oxygen, water motion, sound, water turbulence and clarity, light, nutrients, chlorophyll, organic matter, the amount and types of phytoplankton, zooplankton, and larg- er animals present, along with the platform's own orientation— all to help reveal the com- plex interactions and dynamics of the fer- tile ecosystem in the Southern Ocean. PRIMO is a collaborative project, led by Vernon Asper of the University of Southern Mississippi and Scott Gallager of WHOI. Sea ice CO2 from atmosphere Ice Copepods Current and chemical sensors detect water mixing that brings nitrate and iron up from the depths to sunlit surface water. Photosynthetic plankton need these nutrients to grow. Proximity sensor ensures that the observing platform does not hit the ice sheet. Other sensors monitor the seasonal formation and melting of sea ice. A^dQ-, Sound waves pwelling lutrients Temperature and salinil sensors monitor changes in the thermocline, the boundary between warmer and colder, denser water. Plankton detectors measure sound w^.^ reflected back from some types of plankton to measure their abundance. Phytoplankton . Marine snow Fluorescence and chemical sensors measure phytoplankton at the base of the food chain. Phytoplankton convert carbon dioxide from the atmosphere to oxygen, and decompose into "marine snow" that sinks and serves as food for other Downwelling irradiance To reveal the amounts and wavelengths of light in the ocean and its effect on organisms, sensors measure light radiation into the ocean and reflected back from the seafloor. Midwaterfish Sound waves ""\ Acoustic listening devia record sounds from ^\ marine mammals. An electro-optical cable sends power to the observatory and relays data back to Palmer Station in Antarctica. A winch system drives an instrument package wnn sensors up and down between surface and seafloor. Woods Hole Oceanographic Institution 69 OBSERVATORY OVERBOARD— Scientists and crew aboard R/V Connecticut lower the Autonomous Vertically Profiling Plankton Observatory (AVPPO) to the seafloor. The AVPPO carries instruments that record changing conditions in the coastal ocean, including its temperature, salinity, motion, levels of chemicals and dissolved gases, and the numbers and kinds of organisms living in the area. Data are relayed via cable to the WHOI Martha's Vineyard Coastal Observatory. "The Next Generation of in situ Biologi- cal and Chemical Sensors in the Ocean." It brought together ocean scientists and engineers with colleagues from the fields ot biomedical technology, nanotechnol- ogy, and electrical engineering to explore new approaches and possibilities for ocean sensors. The workshop presented an excit- ing vision and road map for sensors in the not-so-distant future that will allow quantum leaps in what we can observe and discover in the oceans. Our decade- old dream is now becoming a reality: to be able to observe phenomena in the ocean continuously, on all scales and in real time, and to be able to interact with sensors in the oceans — all from shore. Testing the waters Oceanographic sensors come in all flavors: They measure light, temperature, sound, mass, or chemical species. All of these senses will be needed to gain the full picture of all the interacting physical, biological, and chemical dynamics going on in the oceans. Scientists have a fairly good idea of what we need to measure in the ocean. To study ocean pollution, for example, ocean chemists require sensors that detect syn- thetic compounds, such as those derived from plastics and petroleum products, automobile exhaust, storm and sewer runoff, pesticides, fertilizers, surfac- tants, and chlorofluorocarbons (Freon). To understand how chemical cues help organisms find food, or initiate mating or spawning, we need sensors to iden- tity complex organic molecules and learn their concentrations and persistence in the environment. To determine whether the oceans can absorb excess greenhouse gases, we need sensors that measure climatically and ecologically important gases such as car- bon dioxide, methane, hydrogen, hydro- gen sulfide, and radon. Other chemical sensors can indicate how much carbon dioxide is converted by photosynthetic plankton into organic carbon, and how much of this sinks to the deep ocean— to mitigate the buildup of greenhouse gases, or to feed hungry populations of deep- sea organisms. All these sensors, along with others that measure seawater prop- erties such as temperature, salinity, and turbulence, will let biological oceanogra- phers begin to see how ecosystems work and how they change over microseconds to decades. Identifying the inhabitants To learn how organisms respond to changing habitats and interact with each other, oceanographers first need to determine when and where species are present, from bacteria to whales. To identify organisms over the scale of microscopic plankton (micrometers) to a full ocean (thousands of kilometers), scientists need systems that integrate optical and acoustic sensors, which give complementary information. Sound propagates far in water, provid- ing information over long distances. But it travels in long wavelengths that yield only low spatial resolution. Light, on the other hand, scatters quickly in water, but travels in short wavelengths, giving us high-resolution information on small or- ganisms and their "spheres of influence" — a few body lengths around them. Some integrated systems already exist. One is the Bio-Optical Multifrequency Acoustical and Physical Environmental Recorder, or BIOMAPER-II, developed at WHOI, which was used recently to survey krill populations around Antarctica. (See "Voyages into the Antarctic Winter," page 48.) Towed behind a vessel, BIOMAPER- II carries an acoustic system to detect small marine organisms such as krill or plankton, a video plankton recorder to take pictures of them, and other sensors to measure water properties. But just knowing the locations, con- centrations, and types of species is still not sufficient. Scientists also need infor- mation on organisms' feeding, growth, and reproduction. Integrated systems will soon carry sensors that sample, analyze, and identify biological mole- cules— among them DNA, proteins, en- zymes, and lipids — that signal biochem- ical activities. The Environmental Sample Pro- cessor, developed by Chris Scholin at Monterey Bay Aquarium Research In- stitute, is a working example. Attached to a mooring on the seafloor, it extracts nucleic acids from water samples and detects specific organisms by their DNA. (See "Revealing the Ocean's Invisible Abundance," page 64.) 70 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmac An expanded toolkit Exciting additions to our sensor arse- nal are already being developed. To begin to measure tiny "needles" of dissolved gases, trace metals, elements, and nutri- ents in the "haystack" of the oceans, sev- eral new approaches show great promise. Laser-Induced Breakdown Spectros- copy (LIBS) uses a laser to vaporize tiny amounts of a material and determine its elemental composition based on the light spectrum it emits. WHOI scientists are collaborating with the Army Research Laboratory to develop oceanographic sensors using LIBS. Raman spectroscopy uses laser light to cause tiny samples ot water to vapor- ize and the molecules in the water to vibrate. That changes the spectrum of light scattered from the molecules, thus revealing many high molecular weight compounds in the water, including large organic molecules such as lipids, pro- teins, and amino acids. Raman spectros- copy can also be used to detect dissolved carbon dioxide. It may soon be possible to identify microorganisms in seawater by scan- ning it with light and measuring the way they scatter light at different wavelengths. Miniaturized equipment to make this measurement already exists, and advanc- es in mathematical analysis techniques (known as spectral deconvolution) may allow us to detect the species, concentra- tions, mass, chemical compositions, and even nucleotides (components of DNA) in seawater samples. Scientists are just beginning to mea- sure chemicals in the extremely harsh conditions of hydrothermal vents and seeps, where the high temperatures (up to 400°C or 750°F) and corrosive nature of hydrothermal fluids make them al- most impossible to sample directly with sensors. A promising technology for these conditions, called voltammetry, si- multaneously detects a variety ot chemi- cal ions including oxygen, hydrogen sul- fide, iron, and manganese. Voltammetry employs electrodes to scan seawater with a range of voltages while measuring the electrical current output occurring in response to the volt- age scan. This output is recorded as a spectrogram: a graph of multiple peaks in which the location and height of the peaks are proportional to the types and amounts of ions in the seawater. 'Wiring' the oceans But all these sensors are of little value unless they can get out into the ocean and stay there. Autonomous underwater ve- hicles (AU Vs) are one way to accomplish that mission, but oceanographers have also been developing exciting new cabled observatories that provide continuous power to plugged-in instruments and two-way communications to scientists ashore. Developed and developing obser- vatories are being located to study various ecosystems, including productive coastal areas, harbor entrances, or regions under polar ice. At WHOI, the Martha's Vineyard Coastal Observatory will soon become the homeport of a new observing plat- form called the Autonomous Verti- cally Profiling Plankton Observatory (AVPPO), which is designed to observe daily, seasonal, and annual changes in the coastal Atlantic Ocean ecosystem (left). A winch system drives a platform on a 15-minute trip from the seafloor to the surface. It is equipped with a range of instruments — 35 sensors in all — that measure salinity, temperature, oxygen, water motion, water turbulence and clar- ity, light, chlorophyll, organic matter, the amount and types of zooplankton and phytoplankton present, along with the platform's own orientation in the water. These measurements can be correlated with weather and storm events and will help us monitor the coastal ecosystem's response to climate and other changes. A similar instrument, the Polar Re- mote Interactive Marine Observatory (PRIMO), will soon be installed under the ice in the Southern Ocean and cabled to shore from Palmer Station on the western peninsula of Antarctica. It will be the tirst cabled remote observatory in the harsh Antarctic environment and our tirst long-term, real-time look at this fer- tile ecosystem that supports a wealth of marine life. PRIMO will transmit data via cable and satellite and give researchers and stu- dents a direct link to critical phenomena and events, including storms, currents, sea ice formation, and the spring phyto- plankton bloom that fuels an entire food web. It will also provide clues on how this delicately balanced ecosystem might re- spond to the receding ice edge and other changes related to climate. Like other observatories, PRIMO will be used in concert with AU Vs by including docking facilities for AUVs in the future. We have entered a new era with a changing paradigm of how we sample the ocean. We soon will "wire the oceans" with instrumental "eyes, noses, and hands" — which can't help but dramati- cally expand our understanding ot what's going on in the oceans. Stay tuned, the best is yet to come. Scott Gallager has been interested in the inhabitants ot lakes and oceans since his college days. His interest in engineering and elec- tronics goes back even further: While still in high school, he published his first paper, "A Color TV You Can Build," in Popular Mechanics. He earned a bachelor's degree in biology and environmental sciences at Alfred University and a master's degree in marine sciences at Long Island University, and then worked at WHOI as a research assistant, associate, and specialist while completing a Ph.D. in biology at Boston University. After a postdoctoral position at Dalhousie University, he returned to WHOI, where he is an associate scientist in the Biology Department. His interests have led him to use electronic and computer technology to study how planktonic organisms live in and adapt to their environments, and their functional morphology and biophysics. He works in coastal Atlantic, Arctic, and Southern Oceans, building instruments to remotely monitor ocean ecosystems. He often talks to teachers and students and has originated a Boy Scout merit badge program in oceanography. Woods Hole Oceanographic Institution 71 Down to the Sea on (Gene) Chips The genomics revolution is transforming the way scientists can study life in the oceans By Mark E. Hahn, Senior Scientist Biology Department Woods Hole Oceanographic Institution A half-century ago, James Watson and Francis Crick (aided by Ro- salind Franklin and Maurice Wilkins) discovered the double-helical structure of deoxyribonucleic acid (DNA). Other sci- entists soon showed how DNA — through a triplet code of nucleotide bases on the DNA "spiral staircase" and through ribo- nucleic acid (RNA) intermediaries — in- structs cells to assemble essential life- sustaining proteins. These discoveries opened the door to a new understanding of life by revealing the genetic "blue- prints" that underlie the ability of organ- isms to grow, survive, and reproduce. A revolution in biotechnology ensued, giving scientists methods to isolate and identity genes, make millions of copies of them, and determine their sequences of nucleotide bases. Together, the acceler- ating pace ot biotechnological advances and the exponential increase in DNA se- quence information ignited an explosion in molecular biology and led to the emer- gence of a new field: genomics. These advances were initially applied in the bio- medical arena, leading to new informa- tion on the genes responsible for heritable diseases, the molecular signatures of can- cer cells, the biology of human pathogens, and genetic factors that influence an indi- vidual's sensitivity to drugs or toxicants. Now, the genomics revolution has reached the oceans. New genomic tech- niques are being used to find previously unknown life forms in the oceans; to learn how species, and genes themselves, evolved over Earth's long history; to un- derstand the genetic tools that allow spe- cies to adapt to diverse and often harsh environments; and to investigate species' responses to pollutants. Genomics gives marine scientists powerful new ways to address age-old questions about life in the oceans. What is genomics? Genomics is more than simply deter- mining the sequence of nucleotides in an organism's genome (the entire set of genetic information contained within a cell's DNA). It is a new approach to ques- tions in biology, distinguished from tra- ditional approaches by its scale. Rather than studying genes one by one, genomic approaches involve the systematic gath- ering and analysis of information about multiple genes and their evolution, func- tions, and complex interactions within networks of genes and proteins. Genomics has two branches. One is structural genomics — studies ot how genes and genomes are organized and how that varies among individuals, popu- lations, and species. It includes character- ization of the sequences of DNA nucleo- tides that encode proteins, as well as the DNA found between and within genes that does not code for proteins. Using structural genomics, we can compare DNA sequences among in- dividuals of a species to reveal minor variations in the DNA nucleotide code at certain positions in the genome, called "single-nucleotide polymorphisms, " or SNPs (pronounced "snips"). These SNPs can be responsible for genetic diseases, or for hypersensitivity or resistance to drugs or toxicants. By comparing DNA sequences among species (called "comparative genom- ics"), scientists can identity changes in genomes that have occurred as species evolved. They can also begin to deter- mine the function of specific DNA se- quences shared among different species. The second branch is functional genom- ics— the study of the RNA and proteins produced by genes (referred to as "gene expression"), and how these molecules in- teract to carry out cellular processes. Among the most elegant and widely used tools of functional genomics is the mi- croarray, or "gene chip" (see figure), which became available less than a decade ago. By using microarrays to simultaneously measure the amounts ot hundreds or thou- sands ot specific RNAs contained in cells or tissues, biologists can "see" what cells are doing and how they are responding to par- ticular environmental conditions. Genes reveal marine biodiversity Though the genomics revolution immediately swept into biomedical re- search, its entrance into oceanography and marine biology lagged. But marine scientists at WHOI and elsewhere have now begun to take advantage of genomic methods and approaches, aided by three recent developments. First, the costs of instruments to do genomic research, especially the costs of DNA sequencing, have declined dramati- cally over the past five years. Second, ef- forts to sequence genomes have started to include more marine species, from bacte- 72 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu ria to animals. And third, recent studies have shown that genomic approaches can be used even if a species' genome sequence is not yet known. Marine organisms with unusual or unique adaptations, for ex- ample, can now be studied using genom- ics. In addition, by sequencing DNA from samples ot seawater or ocean sediments, scientists can find new organisms by com- paring the newfound genes with similar gene sequences ot known organisms. To study single-celled marine organ- isms, scientists are hampered because it is often difficult to replicate the microbes' undersea conditions in the laboratory and culture the microbes successfully. But molecular and genomic approaches are yielding important and sometimes sur- prising information about the diversity, abundance, and ecological roles of ma- rine microbes in diverse environments, including extreme environments such as the deep sea and polar regions. (See "The Deeps of Time in the Depths of the Ocean," page 17.) Recently, the genomes of several marine microbes have been sequenced, providing a window on their genetic, biochemical, and physiological adapta- tions to their diverse physical, chemical, and biological environments. Some of the microbes' unusual physiological abilities, inferred initially from genomic sequences taken from environmental samples, have been confirmed subsequently by detailed study of expressed proteins. For example, Ed DeLong's research team at the Monterey Bay Aquarium Re- search Institute isolated genes encoding a novel type of light-harvesting pigment that mediates an unusual form ot photo- synthesis in marine bacteria. Genomic studies of uncultured bacterial samples from oceanic waters showed that these pigments are much more diverse and widespread than expected. These findings are changing the way we think about the importance of marine bacteria in the flow of carbon and energy in marine ecosys- tems, including their possible role in the uptake of atmospheric carbon dioxide. How gene chips work Fish in clean water Fish in polluted water Fish cell X cDNA Sample solution is applied to a microarray. Each spot on the microarray has multiple copies of single-stranded DNA from a known fish gene. A strand of sample cDNA will bind to DNA with its complementary sequence ofnucleotides. Microarray chip •••„ ••••• • •• . • ____ • • ___ •••_ i Genes with decreased expression in polluted fish, compared to clean fish Genes with increased expression in polluted fish, compared to clean fish Red fluorescent dye is attached to complementary DNA (cDNA) from cells in fish in clean water; green dye to cDNA from cells in . <_ fish in polluted water^^f ^A _ ._^^Dfv "^ ~ Polluted fish's Fish cell Clean fish's cDNA(red) /' V* ( VN A scanner reads pattern of dyes to show which cDNAs are present in the samples, and thus, which genes are expressed in the fish cells. Genes expressed at the same level in polluted fish and clean fish Genes not expressed in either fish Genomic insights into evolution Genomic information also provides a key to unlocking longstanding mys- teries of evolutionary history. Scientists are comparing the characteristics of ge- nomes—DNA sequences, gene structure, and chromosomal organization — to infer evolutionary relationships among organ- isms. Such studies are helping scientists construct the tree of life, which traces the evolution of organisms from ancestral single-celled beginnings to the diversity that exists today. Such studies have shown that an organism's DNA can come not just from its direct ancestors but also from dis- tantly related species. Though genes are transferred vertically (from parent to offspring), a surprising 17 percent of the DNA in some bacterial species has been acquired by horizontal gene transfer (be- tween species). Genes encoding bacterial antibiotic resistance, a major problem in hospitals, are known to be passed around in this way, but the implications of hori- zontal gene transfer in the marine envi- ronment are not yet well understood. To understand age-old evolutionary mysteries of how animals evolved such a variety of body plans— from jellyfish to mollusks, crustaceans, worms, and verte- brates—biologists are now using genom- Woods Hole Oceanographic Institution 73 ics to elucidate the structure, expression, and evolutionary history of the genes responsible for generating morphological diversity during embryonic development. Genomic studies in a variety of animals, including tunicates (marine invertebrates that are close relatives of vertebrates), have helped reveal the importance of a set of genes known as the Hox cluster. The specific positions of the Hox genes on the chromosome influence how these genes are expressed during embryonic develop- ment and ultimately how they affect the shape of the embryo. Genome sequencing in animals, plants, and fungi also has revealed that at certain times in evolutionary history, various lin- eages developed duplicate genomes — that is, extra sets of the same genes. The extra genes increase the chance that mutations providing advantageous anatomical, physiological or biochemical traits will be retained. In this way, genome duplications may promote biodiversity. Genomic studies have shown that one or two whole genome duplications occur- ring more than 450 million years ago may have facilitated the evolution of verte- brates (animals with backbones). Another more recent genome duplication may have led to the extraordinary diversity of bony fishes (about 30,000 species), which ac- count for about half of vertebrate species. Genomic clues to symbiosis Genomics is also providing insights into the factors that underlie symbiosis, the fascinating interrelationships between two organisms that can be either mutu- ally beneficial (mutualism) or harmful to one member ot the pair (parasitism). Genomic sequencing ot symbiotic organ- isms has shown that dramatic changes in genome structure often occur during the evolution of their association. Parasites, for example, often exhibit reductions in size and gene number, accompa- nied t loss ot the ability to carry out certain b, u-mical reactions. Scienu .'.Iso using microarray- based measures ot gene expression to un- derstand symbiotic mechanisms between reef-building corals and dinoflagellates that help corals grow and build their skel- etons. The studies will also yield better understanding of coral bleaching, which occurs when the dinoflagellates leave or are ejected from the corals. Adapting to the environment Scientists have learned that changes in an organism's environment, includ- ing pollution, often elicit compensatory changes in the expression ot specific genes. For example, Andrew Gracey and George Somero at Stanford University's Hopkins Marine Station have used mi- croarrays to identify genes involved in the ability of a burrow-dwelling fish, the goby Gillichthys mimbilis, to adapt to the re- duced oxygen levels (hypoxia) that occur in its intertidal burrows. Similarly, scientists at WHOI are studying the genes and proteins involved in the response offish to contaminants such as chlorinated dioxins and poly- chlorinated biphenyls (PCBs). At WHOI, Heather Handley-Goldstone and John Stegeman have used microarrays to identify genes associated with heart mal- formations caused by dioxin in embry- onic zebrafish. In my lab, we use genomic techniques to trace the evolution of genes encoding receptor proteins through which diox- ins and PCBs cause altered gene expres- sion and toxicity. We have found that fishes have more of these receptor genes than mammals, possibly explaining the extreme sensitivity of fish to these chemicals. At the same time, we are also studying how small changes in these genes — SNPs — might be involved in PCB resistance that sometimes develops in At- lantic killifish (Fundulus heteroditus) liv- ing in highly contaminated sites such as the harbor in New Bedford, Mass. From genomics to bioinformatics Despite the progress in applying ge- nomics to marine systems, challenges remain. One of the most significant is dealing with the huge amounts ot data generated in genomic experiments, which must be analyzed in relation to environmental or physiological mea- surements collected at the same time. To accomplish this, we use bioinformat- zcs— mathematical and computational methods for analyzing and visualizing genomic data. As bioinformatic approaches become more sophisticated and essential, biolo- gists without extensive mathematical backgrounds will need enhanced training in computational genomics and bioinfor- matics. We will also need to recruit more mathematicians and computer scientists into the marine science community. The conceptual and technical ad- vances associated with genomics are revolutionizing research in biology and medicine. The emergence of genomics gives the marine science community an unprecedented opportunity to address old questions in new ways and to formu- late new questions stimulated by our ex- panding genomic understanding ot life in the oceans. I^^^i "\ /T ark Hahn first visited Woods Hole in 1966 when his father, who _ <^| i-VJ. worked for Eastman Kodak in Rochester, N.Y., spent a week at the ^ ^ Marine Biological Laboratory on business. Left to his own devices, the eight-year-old boy wandered around the docks and spent hours at the National Marine Fisheries Service aquarium, fascinated with the fish, seals, and turtles on display. This nascent interest in marine biology remained quiescent while he pursued a B.S. in biological sciences at Harpur Col- lege ot'SUNY Binghamton and then a Ph.D. in biochemical toxicology at the University of Rochester School of Medicine and Dentistry. Given the opportunity to rekindle his marine interests through a Surdna Foundation postdoctoral fellowship at WHOI in 1987, he turned a one-year fellowship into a thriving research program in comparative and molecular toxicology that involves a large group of talented colleagues. Hahn lives on Martha's Vineyard with his wife, a kindergarten teacher, and son. 74 Oceanus Magazine • Vol. 43, No. 2 • 2005 • oceanusmag.whoi.edu MBI. WHOI I.1BHAKY UH lfl3Z A The Ocean Institutes In 2000, Woods Hole Oceanographic Institution established four Ocean Institutes to accelerate advances in knowledge about the oceans and to convey discoveries expeditiously into the public realm. The Ocean Institutes' goals are to catalyze innovative think- ing that can open up new scientific vistas, to spur collaboration among scientists in different disciplines, and to stimulate a rich and productive edu- cational environment that will engage future leaders of oceanography. Con- currently, each Institute's mission is to shorten the time between acquiring knowledge and making it accessible to decision-makers who can use this in- formation to benefit society. The Deep Ocean Exploration Institute investigates Earth's dy- namic processes beneath the oceans , where more than 80 percent of all earthquake and volcanic activity occurs and where the clues to understanding the inner workings of our planet lie. The seafloor is our window into the dynamic, fundamental processes that gener- ate natural disasters, produce oil and mineral resources, create and destroy oceans and continents, build mountains and islands, and foster life. The Deep Ocean Exploration Institute: • explores how our dynamic planet evolves and changes • examines the basic forces that create earthquakes and volcanoes • develops technology related to seafloor observatories and deep-submergence vehicles • investigates unusual chemosynthetic communities of life on and below the seafloor • explores potential new energy and mineral resources in the oceans The Ocean Life Institute explores the ocean's extraordinary di- versity of life — from microbes or whales — to identify ways to sustain healthy marine environments and to learn about the origin and evo- lution of life on Earth. The more we look into the oceans, the more we find remarkable life forms thriving in environments ranging from Antarctic sea ice to the volcanic crust below the seafloor. The Ocean Life Institute: • explores biodiversity in the oceans • finds ways to monitor and sustain the health of marine ecosystems • studies marine life's physiological and ecological adaptations • investigates the evolution of life in Earth's oceans • develops new techniques and instruments to explore ocean lite The Ocean and Climate Change Institute seeks to understand the role of the ocean in regulating Earths climate and to improve our ability to forecast future climate change. The ocean stores vast quantities of heat, water, and carbon dioxide and works with the at- mosphere in regulating global and regional climates — on time scales ranging from days (storms and hurricanes), seasons (monsoons), years (El Ninos), to centuries and longer. The Ocean and Climate Change Institute: • identifies the climatic effects of ocean circulation patterns • develops an ocean-monitoring network to forecast climate changes • examines geological records to better understand ocean behavior • studies ocean dynamics that may trigger large, abrupt climate shifts • evaluates the ocean's response to the buildup of greenhouse gases •~ rum i ~\\m The Coastal Ocean Institute examines one of the most vital — and vulnerable — regions on Earth: the coast. Our planet's exploding population has put stress on the fragile coastal ocean and has ex- posed more people to coastal hazards such as storms, beach erosion, and pollution. Understanding the complex, delicately balanced pro- cesses at work in coastal areas is the key to ensuring that they remain productive and attractive. The Coastal Ocean Institute: • studies basic processes underlying the coastal ocean's fertility • provides sound science to guide coastal management policies • examines uses of coastal resources, such as wind, oil, and fisheries • identifies strategies to mitigate coastal hazards • promotes awareness of the coastal zone's importance to society Woods Hole Oceanographic Institution 75 WOODS HOLE OCEANOGRAPHIC INSTITUTION Woods Hole, MA 02543 • 508-457-2000 • www.whoi.edu . : ' ^^J