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Keeping a Finger on the Pulse of Marine Biodiversity:
How Healthy is it?

Jerry R. Schubel
New England Aquarium, Central Wharf, Boston, MA 02110-3399
Cheryl Ann Butman
Department of Applied Ocean Physics and Engineering, Woods Hole Oceanographic Institution, Mailstop 12, Woods Hole, MA 02543

“If all the beasts were gone, man would die of great loneliness of spirit.”
Chief Sealth of the Duwamish Tribe
in a letter to President Franklin Pierce, dated 1855

Setting the Stage

The world ocean stretches from pole to pole, covers 71% of Earth, and represents more than 99% of the planet's total biosphere volume, or living space. The ocean is nature's ultimate womb. Most scientists believe that life originated there. It is composed of a rich mosaic of habitats large and small, from some of the seemingly most homogeneous and remote, such as the deep-sea floor, to some of the most heterogeneous and accessible, such as the vibrant coral reefs.

The world ocean is the greatest repository of biodiversity at the second highest level of taxonomic organization, the phylum. This level distinguishes organisms according to their basic body plans. Sponges and chordates (which include humans), for example, constitute separate phyla within the animal kingdom. The sequence of phyla roughly reflects the trend in evolution. Of Earth's 33 animal phyla, 28 are found in the ocean, and only 11 are found on land. Moreover, 13 of the animal phyla are endemic (native and restricted) to the marine environment, whereas only one animal phylum is endemic to land: the ancient slug-like Onychophora. At the lowest level of taxonomic organization, the species, biodiversity apparently is much higher on land than in the sea. Yet most of the world ocean is still unsampled, and many of the species collected are still unidentified.

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As ocean exploration continues, large numbers of new entries into the library of marine biodiversity are expected at virtually every level of taxonomic organization, particularly at the species level.

The relentless discovery of multitudes of new species, from microorganisms to vertebrates, has driven a revolution in marine taxonomy—the identification of species. New techniques, including flow cytometry (described later) and molecular tools involving gene sequencing, now replace or augment traditional, morphology-based methods for classifying and identifying a wide variety of marine organisms. Some new taxonomic capabilities have found immediate applications in conservation. With molecular techniques, for example, some whale species now can be identified solely from the meat that is sold in the marketplace; this facilitates enforcement of restrictions on the hunting of threatened or endangered species.

In the sea, as on land, the greatest threats to biodiversity come from one species, Homo sapiens. The imprint of humans is found throughout the world ocean, but it is most evident and poses by far the greatest threat along its margins—in the coastal zone. Still, documentation of changes in biodiversity caused by human activities is limited by the difficulty in sampling most ocean habitats and identifying the organisms collected. That is, assessing the health of marine biodiversity is seriously hindered because, in most cases, we cannot even take its pulse.

There are several excellent books on the general topic of marine biodiversity, in addition to numerous scholarly articles in the burgeoning primary literature (see list at end). Nearly all were written by scientists for scientists or for scientifically literate readers. As a complement to that literature, this paper describes for the layperson a general picture of biodiversity in the world ocean, how humans are altering it, and the threats that loom on the horizon. We also suggest some elements critical to any integrated management plan for minimizing human threats to marine biodiversity. Thus, this paper celebrates the diversity of marine life at all levels, laments the threats to it, and summons humankind to rise to the challenge of its conservation.

General Characteristics

Exploring the Sea

Most people encounter the world ocean only at its margins and experience only a few meters of its depth. Yet the continental shelf, the shallowest region of the sea floor, constitutes a mere 7% of the ocean's area. Of the whole sea floor (about 300 million square kilometers), 83% is more than 1,000 m below the surface and constitutes a zone known as the deep sea. Deep-sea environments are far more difficult to sample and characterize than even the most remote terrestrial habitats. In fact, it is only within the last 50 years that scientists have been able to observe directly, sample, and experiment in untethered “manned” submersibles, like the deep-sea submergence vehicle Alvin (figure 1). But there is a lot of catching-up to do; the deep sea is still the most undersampled marine environment.

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Figure 1
Deep-sea submergence vehicle Alvin being launched from its 274-ft support
ship, research vessel Atlantis. The three-person submersible can dive to almost
5,000 m, enabling it to reach 86% of the world ocean floor. Alvin typically
makes 150–200 research dives each year. It was commissioned in 1964,
is owned by the US Navy, and is operated by the Woods Hole Oceanographic
Institution as a national oceanographic facility. (Photo credit: Rod Catanach.)

Most marine research is done relatively blind from surface research vessels, with nets used to sample the water column and grabs and corers to sample the sea floor. In areas of thousands to tens of thousands of square kilometers, typically less than a square kilometer of the sea has been sampled. That is equivalent to characterizing the entire fauna and flora in a backyard from a sample the size of the head of a pin! Moreover, planktonic (free-floating) and nektonic (free-swimming) marine organisms are constantly in motion, so temporal and spatial variations are easily confounded.

Because of the sampling issues, knowledge of different groups of marine organisms is strongly conditioned by their habitats, their mobility, and the scale of their distributions. In general, distributions of easily accessible, larger, and relatively sedentary organisms (for example, intertidal barnacles and mussels) are better documented than those of inaccessible, smaller, and highly mobile life forms (for example, zooplankton and deep-sea fishes). Microorganisms, which occur in virtually every marine habitat, are by far the most undersampled and undercharacterized. Whales are the largest animals in the world, yet because certain species (for example, blue and sperm whales) are so mobile and can dive deeper than 800 m, there are few accurate estimates of their population sizes, let alone knowledge of their dynamics. Until the 1960s, population sizes were estimated entirely from

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visual observations made from whaling vessels. Photographic identification studies and tag-recapture estimates now provide more accurate information on some coastal species (for example, humpback and right whales), but population sizes and movements of off-shore species remain largely a mystery.

The Aqueous Medium

Marine organisms are enveloped by water, whereas terrestrial organisms are enveloped by air, and the differences between these two fluids—water and air—account for many of the differences in life found in the marine and terrestrial environments. Water is 1,000 times denser than air, and the difference in density has a number of important consequences. First, water acts as a thermostat, buffering against rapid and large changes in temperature not only within the fluid, but for the entire planet. Second, water provides buoyancy that counteracts gravity, reduces the need for physical supporting structures, and facilitates vertical mobility of animals. Third, the much greater kinetic energy (that associated with motion) of water relative to air virtually precludes the existence in the sea of large, rigid, stationary organisms on the scale of trees. And fourth, the much greater dissolving power of water (than of the atmosphere) provides a relatively rich nutritional soup that enables marine plants to receive all their nourishment directly from the enveloping fluid; in contrast, most terrestrial plants require both the atmosphere and the soil to obtain water and nutrients. With respect to optical clarity for photosynthesis, however, the air wins hands down.

The Diversity of Habitats

On land, there are millions of distinct and fixed habitats spanning a large range in size. Some terrestrial habitats are as small as or even smaller than a single tree in a rain forest that supports numerous highly endemic species, and some are as large as the Serengeti plains, stretching for hundreds of kilometers. In the sea, particularly in the water column of the open ocean and over vast expanses of the deep-sea floor, the number of distinctly different habitats is comparatively small. The spatial extent of these habitats is large, however, and marine habitats are intimately connected via the motion and mixing of the fluid medium; thus, endemism is much rarer in the sea than on land. What is surprising is the degree of biological heterogeneity—the biodiversity—that abounds in this seemingly homogeneous seawater medium.

In the sea, organisms have evolved in response to variables other than physical space—variables that might have no terrestrial analogues. In the open ocean, water circulation patterns can create discrete habitats. In the cold coastal waters of the western North Atlantic, for example, are “warm-core rings” that have pinched off of the swift, northward-flowing Gulf Stream (figure 2). Likewise, semienclosed pockets of cold coastal water—cold-core rings—can spin off into the Gulf Stream. Because different species assemblages are associated with different water masses, regional biodiversity is enhanced by these water-mass intrusions.

In the immense sedimentary plains of the deep-sea floor, there is an extraordinary diversity of animals, perhaps rivaling the biodiversity of tropical rain forests. Organisms living on or in the relatively thin layer of sea-floor sediments—the

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Figure 2
Summertime sea-surface temperature from Cape Hatteras to Nova Scotia in
the western North Atlantic. The drawing was made from a satellite image taken
on June 13, 1997. Arrows indicate the direction of water flow (currents) as determined
from drifter studies. (Original satellite image used courtesy of the Ocean Remote
Sensing Group of the Johns Hopkins University Applied Physics Laboratory; satellite
image mosaic overlaid with drifter data was constructed by Dick Limeburner.)

benthos—have evolved largely in response to the highly limited and unpredictable food supply in the deep ocean and thus have remarkable adaptations for exploiting ephemeral and patchily distributed organic matter. In shallow water, benthic organisms experience more habitat variability over small spatial scales than organisms in overlying waters (figure 3). There is also less direct connectivity among habitats in the benthic zone than in the pelagic zone (open water). Thus, most benthic organisms have planktonic larvae (meroplankton) that can expand species distributions over larger areas, provide some insurance against local catastrophic events, and recolonize areas where populations have been eliminated by human activities. The greater habitat diversity and lower connectivity in the benthic zone results in species diversity much greater than that in the water column. Moreover, within the world ocean, the largest number of phyla are represented in the benthos.

In contrast with the seemingly featureless sedimentary sea floor, coral reefs scream and shout with habitat complexity. Coral reefs are, in fact, analogous to rain forests in that the most conspicuous habitat in the reefs is provided by living organisms—the corals themselves. Corals create the underlying structure for the reefs and provide attachment sites for many invertebrates and protection for numerous fishes. Moreover, because corals contain their primary producers—tiny algae called zooanthellae that live in the coral tissue—they have a built-in food source. Coral reefs are believed by many marine-biodiversity experts to be the

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repositories of the greatest biodiversity in the world ocean if one scales them for size, that is, species per unit area. The other contender for this distinction is the deep-sea floor.

Diversity and Ecosystem Function.

Marine ecosystems are knitted together by relationships among organisms, particularly by who eats whom. In the water column, the food web involves encounters between freely moving predators and prey. Chance, random processes, and adaptation to survive for long periods without food are important driving forces in many more marine than land ecosystems.

Ecosystems have functional attributes—such as the capacity to capture, store, and transfer energy and nutrients—and they also contribute to societal needs. Estuarine ecosystems, for example, tend to have relatively low biodiversity but high productivity, and they contain many commercially important fish and shellfish species. In contrast, coral-reef ecosystems have high biodiversity but low productivity and are now exploited largely for ecotourism.

Some species are more important to the functioning of an ecosystem than others. If they are removed, their roles might be lost, leaving a hole in the food web,

Figure 3
Reflectivity of bottom sediments in Massachusetts Bay, just off shore of Boston
(see figure 2), superimposed on the bathymetry. Measurements were made with a
remote-sensing technique—sidescan sonar—where the travel time of sound between
the ship and the sea floor yields information on the texture of the sediments. Areas of
boulders, represented by the lightest tone, were typically found at the crests of the small,
submerged hills. The intermediate gray tone is sand containing various amounts of gravel.
The darkest areas are fine-grained (muddy) sediments, often in the depressions between
hills. Note that the mottled region in the center of the mosaic shows 10- to 100-m-scale
patches of sands and muds. Different communities of organisms occur in different sediment
types, and such intricate heterogeneity in sediment texture results in enhanced local
biodiversity. The strips represent the ship track and are about 150 m apart. The dotted line
is the location of a new wastewater outfall diffuser, which is being installed deep within
the sea floor. The outfall pipe starts at the shore and extends northeast. (Sidescan mosaic
courtesy of Brad Butman of the US Geological Survey.)

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such as a gap in energy transfer, in nutrient cycling, or in some other crucial function. Most critical are the “keystone” species. If one of these is removed—by overexploitation or by a natural or human-assisted disaster—the ecosystem changes dramatically. Sea otters are a keystone species of eastern Pacific kelp communities. Sea otters eat sea urchins, which in turn eat kelp. When sea otters were hunted to near extinction along the US West Coast, urchin populations exploded and devoured the kelps, thus turning magnificent, highly diverse kelp forests into featureless sandflats known as “urchin barrens”.

Few marine ecological studies have identified keystone species and other critical relationships between species composition and ecosystem function. Without such knowledge, human activities that involve broad-scale removal of species or alteration of habitat can easily and inadvertently tip the delicate ecological balance, sometimes with disastrous consequences. Overfishing has already greatly diminished most of the large predators of the open ocean; the repercussions have reverberated throughout the food web (figure 4). Moreover, industrial-scale fishing has recently begun to focus on the slow-growing fishes of the largely unexplored deep sea, with unknown consequences. Researchers do not know which or how many of the commercially hunted fishes, shellfishes, or kelps are keystone

Figure 4
Human activities, such as longline fishing for top predators, can potentially
affect the prey, the prey of the prey, and so on, contributing to the deterioration of the
food web. Longlining also results in by-kill, the incidental deaths of nontargeted species,
such as marine turtles and sea birds.

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species, which or how many have functional equivalents, and whether and how their losses might unravel an ecosystem's intricate web.

The Montage of Marine Biodiversity

In this section, we reveal some of the major components of the montage of marine biodiversity and describe some characteristic properties and processes that contribute to the maintenance of the marine fabric of nature. Examples are chosen to be illustrative; it is impossible to be comprehensive. We close with some observations about the general patterns of marine biodiversity around the world.

Primary Producers

There are many similarities between terrestrial and marine environments. Both depend ultimately on photosynthesis for nearly all their energy. Thus, it always starts with plants. Photosynthetic organisms in both environments produce organic material used as food by herbivorous animals, which are preyed on by carnivorous animals to form complex food webs. A primary difference between the terrestrial and marine environments is that in the ocean, most of the plants are microscopic cells floating in the water. These cells are known as phytoplankton.

The Greek root of the word plankton is planktos, which means “wanderer”. And phytoplankton roam the high seas. But for these plant cells to photosynthesize, they must remain in the upper sunlit layer—the euphotic zone. This layer varies in thickness depending on geographic location, but it rarely exceeds 200 m in the open ocean and can be 10 m or less in coastal areas. Staying within the euphotic zone can be challenging for phytoplankton. Gravity pulls them down, and other physical processes, such as convergences (downward-directed currents), transport them away from the light. Phytoplankton have remarkable adaptations that counteract those forces, such as bubbles of fatty material and elaborate spines that reduce sinking.

Collecting and identifying phytoplankton is demanding, to say the least. The cells are so small (0.1–100 mm) and fragile that they are damaged or destroyed by conventional sampling with nets and filters; this makes identification under a microscope laborious or impossible. In contrast, flow cytometry—a new nonintrusive technique for counting and identifying phytoplankton—uses a laser to discern the fluorescence characteristics, size, and shape of each cell. In the late 1980s, the shipboard use of this technique led to the discovery of a new group of marine photosynthetic bacteria, the prochlorophytes. These tiny (0.2–2.0 mm) organisms account for up to 40% of all chlorophyll (the major photosynthetic pigment) in some regions of the ocean.

At least one-third of the annual global carbon fixation occurs in the sea. A substantial portion of this carbon is fixed by cells less than 1 mm in size because they are so numerous. Some estimates suggest that the annual fixation of carbon by phytoplankton smaller than 5 mm is similar to that by the world's rain forests. In addition to the importance of phytoplankton to carbon fixation, they can affect marine chemistry by taking up and releasing nutrients. Furthermore, because different phytoplankton species are consumed by different animals, conserving

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phytoplankton diversity is critical to conserving the functioning of marine ecosystems.

Whereas phytoplankton account for more than 95% of oceanic primary productivity, the larger multicellular plants—the macroalgae—seagrasses, and marsh grasses—might be the major producers in some near-shore regions. The kelp forests of temperate, rocky shores host a diversity of animal life, from shellfish to sea otters. Floating mats of brown algae harbor unique animal communities in the open-ocean region of the Sargasso Sea. And seagrasses and marsh plants, occupying critical coastal habitat, stabilize sediments and support distinctive populations of small fishes and invertebrates.

Because of light limitations, all marine plants attached to the bottom are restricted to shallow coastal areas. These ocean habitats are the most directly susceptible to human effects. Because they are close to the shore, attached plants are especially vulnerable to human activities in the sea, such as dredging and sewage disposal, and on land, such as agriculture and urbanization. Entry of suspended sediments and nutrients into the sea from these activities often greatly reduces water clarity (limiting photosynthesis) and degrades habitat (for example, for attachment).

The biology of the sea is driven principally by primary productivity that occurs within a region that accounts for less than 1% of the total volume of the world ocean. Most life in the remaining 99% of the ocean volume depends on food produced within the thin upper layer—food that is either preyed on directly at the surface or scavenged at great depth. Alternative pathways to energy production include sulfur-reducing bacteria that obtain their energy from chemical sources (as opposed to the sun) through a process called chemosynthesis. These primary producers are largely symbiotic, living in tissues of other organisms. Although chemosynthesis produces a small fraction of the sea's total primary productivity, it contributes to marine biodiversity by extending the living space of and facilitating a rich variety of microhabitats.

Primary Consumers

Most plant food is much smaller in the sea than on land, and so too are most marine primary consumers. The grazers—the zooplankton (“wandering animals”)—are small animals that spend either all (holoplankton) or a portion (meroplankton) of their lives in the plankton. Meroplankton are the larval stages of such animals as clams, snails, worms, crabs, and flatfish that, as adults, live on or in the bottom. Meroplankton generally bear no resemblance to the adult form and, like the other plankton, are highly adapted to a suspended existence. Holoplanktonic species dominate the zooplankton in numbers and biomass. They exhibit an extraordinary diversity of form and function, ranging in size from the tiny copepods (hundreds to thousands of micrometers) to the larger jellyfish (millimeters to a few meters).

Nearly all major groups of animals on Earth, except insects, are represented in the zooplankton. Whereas insects, as a group, contain three-fourths of all known animal species on the planet and one-half of all known animal and plant species combined, copepods, the dominant animal group within the zooplankton, have

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more individuals than any other group of animals on Earth, except perhaps roundworms. There are an estimated 1 quintillion (1018) copepods in the sea—1,000–1,000,000 individuals under each square meter of sea surface!

Although phytoplankton are largely restricted to the upper sunlit layer, zooplankton can extend their realm vertically by migrating. This behavior enhances their living space and provides them wider access to food and more opportunity to escape from predators. Zooplankton are intermediaries in the food web. They eat the primary producers—phytoplankton—and are eaten by the secondary consumers—finfish, shellfish, and some whales. Most fish and marine mammals cannot eat phytoplankton directly, but need the zooplankton to repackage them into larger and more nutritious food (like energy bars). Remarkably, however, tiny zooplankton are the major food source for baleen whales, the largest animals on Earth. The mouths of these huge whales contain large comb-like filters called a baleen (figure 5). This sievelike structure retains zooplankton-sized organisms that are slurped off by the whale's tongue. There is no terrestrial analogue for this highly size-disparate food chain, which is more extreme than if an elephant fed on a diet of ants!

There are also benthic grazers—a wide variety of suspension-feeding clams, worms, and other invertebrates that extend feeding structures into the water col-

Figure 5
Baleen whale, with typical zooplankton prey shown in the insert. The greatest
size disparity between a predator (whale) and prey (zooplankton) occurs in the marine
environment. (Photo credit: Paul Erickson.)

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umn, where they actively or passively collect plankton. Because these animals process such large amounts of water and are essentially glued in place on the bottom, they are particularly susceptible to human activities that result in the deposition of particles or pollutants on the sea floor.

Secondary Consumers

Although predatory fish—the predominant secondary consumers—swim the entire world ocean, they eat and concentrate in particular areas during important stages of their life cycles, such as reproduction and early development as larvae and juveniles. Thus, for example, salmon return to spawn in the rivers of their births, and eels congregate for mass spawnings in the Sargasso Sea. Protected near-shore areas, such as estuaries and mangrove swamps, are important nurseries for a wide variety of larval and juvenile fishes. Fish can feed at several levels of the food chain, the size of the fish being a relatively good predictor of the size of the prey. Thus, small fish species and larval and juvenile fish eat zooplankton, and bigger fish eat smaller fish.

The coastal ocean has afforded great opportunity for diversification in fish species, providing a wide range of habitats, prey types, and nursery areas. The number of species (13,000) of coastal marine fishes could be more than 10 times greater than the number of species (1,200) of true oceanic fishes—those which spend their entire life cycles in the open ocean. Fish move much more than the food that they prey on. Fish mobility results in cosmopolitan species distributions and blurs the boundaries of biodiversity patterns at any given time.

Marine Mammals and Turtles

Although marine mammals are a relatively small group—only some 119 species—their endearing characteristics have generated a great deal of conservation attention. The ancestors of marine mammals left the land and began their return to the ocean as early as 50 million years ago, evolving a range of diversity greater than what land mammals had left behind.

Whales, manatees, and dugongs are fully adapted to their aquatic habitats, but marine carnivores—sea otters, polar bears, seals, sea lions, and walrus—divide their lives between land and sea. Although the diversity of many animal groups, both on land and in the sea, increases in habitats nearer the equator (for example, table 1), seals, sea lions, and walrus show the reverse pattern. Only the rarest species, the monk seal, occurs and breeds in the tropics. Toothed whales are the most diverse group of marine mammals. On the basis of size alone, it might be thought that all marine mammals would have been collected, identified, and described centuries ago. Yet, for the cryptic and difficult-to-study beaked whales, seven new species were described in this century, the most recent one in 1991!

Marine mammals are characterized by their radical anatomical, physiological, and behavioral adaptations to life in the ocean. Manatees and dugongs are marine herbivores; they depend on rich growths of aquatic plants. Other marine mammals are consummate divers, with thick layers of blubber, fur, streamlined bodies, fins, flippers, and other modifications that allow them to remain below the surface for long periods and at extreme depths. Dives of sperm whales and el-

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ephant seals, for example, to depths of more than 1,000 m for over an hour have been recorded.

The seven species of sea turtles also spend little time at the surface and cover huge distances on their migratory routes. The largest sea turtle, the leatherback, is warm-bodied, enabling it to live in waters from Venezuela to Newfoundland. Coming ashore to breed on tropical beaches every 2–3 years, these turtles can weigh up to 1,500 lb (680 kg) and dive to more than 600 m.

Some Patterns of Marine Biodiversity and Their Causes

Ptolemy once observed that it is the role of the scientist “to tell the most plausible story that saves the facts.” This charge is difficult when the facts are few and several stories could “save” them equally well. That is often the situation in attempts to generalize about patterns in marine biodiversity—for example, geographically, with depth, or across taxa—from existing data. Keeping in mind that marine biodiversity is grossly undersampled and underdescribed, in table 1 we list some of the general patterns in diversity that are fairly clear.

The Origin of Diversity

In most of this paper, we write about biodiversity as a function of natural communities. Another, fundamental way of looking at biodiversity is as the outcome

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of evolutionary processes: the creation and loss of species. Today's biodiversity is only a small sample of the creatures that have come and gone over evolutionary time (Jeffries 1997). The fossil record contains the traces of plants and animals far different from those now occupying ocean habitats.

New species arise from changes in the genetic makeup of subpopulations. In sexually reproducing organisms, one species can become two when subpopulations of the original species become reproductively isolated and thus do not freely exchange genes. If their genetic makeups then diverge so much that the two populations can no longer interbreed, they become separate species. Geography—continents, islands, submerged mountain ranges, deep-sea canyons, seamounts—can isolate populations. Reproductive isolation can also lead to speciation when the breeding seasons or mating behaviors of two subpopulations become sufficiently different.

Physical structure and changes thereof provide opportunities for isolation of populations. Gyres (alterations in oceanic circulation) and land bridges can impose barriers to interbreeding. For example, the Isthmus of Panama separated the Atlantic and Pacific Oceans, isolating many populations that formerly mixed. On the two sides of the isthmus are many common species, but some populations have diverged enough to become separate species.

The Gulf of California formed only 6 million years ago. It is not part of the circulation pattern of the eastern Pacific, so not only do populations of such organisms as sardines, which occur in both water masses, fluctuate independently of one another, but the gulf has endemic species closely related to similar species in the Pacific. For example, the vaquita, an endangered marine mammal closely related to the harbor porpoises of the Pacific and Atlantic, is endemic to the Gulf.

Small marine populations, especially in the nekton, might be less likely to become isolated than terrestrial or freshwater populations of similar size, because of the more “open” nature of marine systems. For example, freshwater covers only 1% of Earth's surface but accounts for 40% of the 23,000 species of fish.

Anthropogenic Threats and Effects

Anthropogenic threats to the biodiversity of the world ocean are in five major categories: overexploitation of resources, pollution, habitat alteration, introduction of exotic species, and global climate change. The first four categories include threats that are both historical and current. Threats to marine life from global climate change are imminent. Marine biodiversity can be affected by a single threat or several threats, sometimes with devastating and unknown consequences (figure 6). The vast oyster reefs of the Chesapeake Bay, for example, that once filtered the estuary's entire volume every week, now filter it only once a year because of stock depletion due to overfishing, pollution, habitat alteration, and disease.

If we were to give the world ocean the equivalent of a physical examination to determine its fitness, a strong, rhythmic heartbeat would represent the healthy system that was characteristic of prehuman times—and indeed typical of most areas until several thousand years ago. Human activities, however, have caused

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Figure 6
The potential effect of a very remote human activity—whaling—on deep-sea
biodiversity. The flesh of falling whale carcasses provides food for deep-sea
organisms, and the skeletons support a chemoautotrophic-based food chain similar
to that in hydrothermal vent and seep areas (indicated as minivolcanoes billowing
puffs of smoke). Thus, whale skeletons might be critical stepping stones for
hydrothermal-vent communities (depicted on the left). Whale carcasses were released
from whaling vessels in densities and geographic patterns that were probably distinctly
different from natural whale falls. In fact, after the early 1900s, the supply of human-killed
whales to the sea floor decreased dramatically because almost the entire whale,
including the skeleton, was used for various products (depicted on the right).
Before and after the 1900s, the number of whales in the ocean was reduced dramatically;
this potentially diminished (and in some cases stopped) the supply
of whale-carcass stepping stones for hydrothermal vent and other chemoautotrophicbased
communities in the deep sea. (From Butman and Carlton [1995]; used with permission
from the American Geophysical Union.)

a rapid deterioration in the health of many marine ecosystems. Understanding the history of effects on marine biodiversity from the four current anthropogenic threats is important for developing strategies to minimize future effects. Maintaining healthy marine ecosystems requires constant vigilance; keeping a finger on the pulse of marine biodiversity could save its life and the critically important ecosystem services that it provides.

Overexploitation of Resources

Overfishing has dramatically reduced the stocks of many, perhaps most, of the preferred edible fish and shellfish species in the world ocean and led, for example,

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to recent closures of the so-called inexhaustible great fishing banks, such as Georges Bank and the Grand Banks. Entire marine ecosystems have been severely, perhaps irreversibly, altered because of overexploitation of top carnivores and grazers. The herbivorous green turtle population in the Caribbean, for example, likely numbered 60–300 million individuals in the 17th century, before the exploration of the New World. The current population numbers only in the tens of thousands—a reduction of more than 99%! Now, several centuries later, we can only speculate on the vast changes in the natural marine ecosystem that resulted from this dramatic decline in perhaps the largest marine reptilian population in the Caribbean—a decline attributable almost entirely to human hunting.

Human hunting (of fish, shellfish, vertebrates, reptiles, and birds) and collecting (of seaweeds, sea urchins, shells, and corals) has removed or nearly removed ecologically important species from otherwise balanced food webs and has had substantial indirect effects, including by-catch and by-kill (the incidental take of nontargeted species), such as the hooking of sea turtles and albatross on longlines used to fish for tuna and swordfish (figure 4); destruction or disturbance of habitat, such as critical sea-floor habitat of benthic invertebrates by shellfish dredges and bottom-fish trawls; and genetic changes, such as the regional hunting to local extinction of some whale species, which decreases the total genetic material in the species's gene pools.

Pollution.

For over a century, the coastal ocean has been assaulted with large quantities of various municipal, industrial, agricultural, and human wastes. For example, chemical pollutants have caused tumors and diseases in fish and shellfish and have affected reproduction in seabirds (DDT made pelican eggshells so thin that they broke when the birds sat on them); oil spills have resulted in local mass deaths of organisms at virtually every link in the food chain; agricultural fertilizers have killed coral reefs by stimulating the growth of seaweeds that overgrow them; and nutrient enrichment in estuaries has stimulated large algal blooms that sometimes lead to the consumption of most of, or all, the oxygen in the water column and deaths of immobile organisms. Although coastal habitats will continue to receive most of the human-derived wastes, the deep sea has been proposed as an additional dumping ground, especially for radioactive material. Dumping one of the most dangerous waste materials in the least-studied marine environment with, arguably, the highest biodiversity on Earth should be reason for great concern.

Habitat Alteration

Coastal habitats have been decisively altered to accommodate the “needs” of human society. For example, large portions of wetlands and salt marshes have been eliminated by dredging, filling, and diking to create new fastlands (dry land), and large areas of mangrove swamps have been altered to create shrimp ponds for aquaculture. Salt marshes and mangroves are highly productive marine systems that serve as nursery grounds for young fish. Seawalls, jetties, and groins, by design, alter the natural currents and thus can affect transport of organisms in the water or organisms that depend on it for food or respiration. Mining (upland and

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coastal) and deforestation cause erosion on land that ends up in the sea. Increased suspended sediment negatively affects such organisms as corals, which require clear water for photosynthesis by their symbiotic zooanthellae. Clear waters once characterized virtually all tropical areas, but no more.

Introduction of Exotic Species

A startling array and number of marine organisms have been transported around the world ocean by humans, principally in the ballast water of ships. Water is pumped into a ship's hold in one port to stabilize its load and then pumped out in another, sometimes halfway around the globe. Introduced species can outcompete and even eliminate local species. Several introductions have changed entire ecosystems. The European zebra mussel introduced into the Great Lakes led to economic losses of hundreds of millions of dollars per year, and the carnivorous American comb jellyfish introduced into the Black and Azov Seas caused declines in the zooplankton biomass of up to 90% and resulted in large declines in the anchovy fishery (anchovies eat zooplankton).

Global Climate Change

For decades, human activities have been generating compounds that rise into the atmosphere and destroy the ozone that shields the planet from the sun's ultraviolet radiation (UV). If such activities continue, marine organisms might suffer because phytoplankton, zooplankton, fish, corals, and benthic organisms experience harmful effects from biologically damaging ultraviolet radiation (UV-B). Global warming caused by enhancement of the “greenhouse effect” (wherein such gases as CO2 and CH4, generated by human activities, prevent the escape of heat radiating from Earth) is expected to cause a substantial increase in sea level and alter ocean circulation. Adaptation typically occurs over very long periods—thousands to millions of years. Thus, marine biodiversity could be seriously affected if organisms cannot adapt to human-accelerated global climate changes that take place over decades or perhaps a century.

Coastal Vulnerability

The most vulnerable parts of the sea are the coastal areas, the focal point of most human activities that threaten marine biodiversity. Assaults on the coastal ocean have been relentless and, in many parts of the world, are still increasing in magnitude, persistence, and area affected. The cause is continuing human population growth, which is disproportionately faster in coastal areas.

Throughout the United States and the world, about 50% of the human population inhabits a narrow fringe around the periphery of the continents, a coastal region that is only 100 km wide. That percentage and the absolute numbers of human beings are increasing each year, and society as a whole is experiencing a new phenomenon—the emergence along the coasts of “mega-cities”, cities with populations over 10 million (table 2). Moreover, most mega-cities are now in the developing world. Because the developing world is concentrated in tropical and subtropical areas, mega-cities occur in coastal regions that have the highest ma-

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rine biodiversity. Large human populations inevitably result in large effects on the natural environment, so all biodiversity—marine and terrestrial—in these regions is at high risk.

Cities and countries in the developing world do not yet have the infrastructure to deal with the environmentally unforgiving consequences of highly localized human populations, such as overexploitation of resources, habitat alteration, and pollution. Thus, wave after wave of unprocessed or uncontained human, municipal, industrial, and agricultural wastes will continue to travel across the land-sea interface unless steps are taken quickly to forestall this situation.

Clearly, humans have been having large, negative effects on marine biodiversity. Luckily, they also can do something about it. It is ridiculous to ask humans, animals with a right to life on this planet, to have no impact on the environment. Virtually every other species has some impact. In fact, herein lies the origin of “ecology”—the study of relationships between organisms and their environment. But what members of Homo sapiens have over other species is the right to choose their impacts and to minimize those which must occur. The foundation for such decisions is in knowledge of natural patterns of biodiversity and the processes that maintain them. Such data are, however, meager, at best, for most organisms in most environments in the sea.

Conservation Strategies

Entire issues of journals and several books have been devoted to strategies and tactics for conserving marine biodiversity at all levels. Our purpose here is much more modest: to identify some critical concepts that form a foundation on which to build any comprehensive, integrated, and sustainable initiative to conserve marine biodiversity—concepts that derive principally from the distinctiveness of marine, compared with terrestrial, systems (table 3)—and to emphasize the importance of raising public awareness and understanding of the need to conserve marine biodiversity.

There is no comprehensive, coherent, integrated plan for conserving the world's marine biodiversity. Development of such a plan will require far greater knowledge than exists today and far greater cooperation across multiple jurisdictions

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than has ever occurred. And it all starts with goals. Goals for conserving marine biodiversity should be stipulated both in terms of values and uses important to society, with measurable and understandable performance indicators, and in terms of the fundamental value of biology. Furthermore, the effective development and execution of any conservation initiative requires a serious reconnection of people with nature. The best opportunity for broad-scale public education and involvement in conserving marine biodiversity is at the coast, where people are most likely to experience and appreciate the sea. The International Year of the Ocean, 1998, was an excellent starting point for global participation. One vehicle for raising public awareness could be the international network of aquariums, which draw more than 200 million visitors each year and where specific local and regional marine-biodiversity issues can be placed in a global context. Whatever the tactics, they must be developed now, lest our children and theirs know not the magnificent beauty and bounty of the sea.

Closing Comments

The world ocean is experiencing substantial and startling losses of biodiversity. Arguments about whether coral reefs or rain forests support the greatest diversity are silly and dangerous; they divert attention from the real issues. Conservation of the planet's biodiversity—marine and terrestrial—is critically important. We choose the word conservation advisedly. Biodiversity cannot be preserved; it can and must be protected or conserved. Evolution and extinction are natural processes. But now, for the first time in the planet's history, one species—ours—has demonstrated its capacity to destroy large numbers of other species and their habitats. Never before has one species had such a profound, pervasive, and pernicious effect on so many others. Ironically, the other creatures with which we share this planet would be far better off in the absence of “intelligent life”.

Acknowledgments

We thank Bob Beardsley, Brad Butman, Just Cebrian, Mark Chandler, Gregory Early, Scott Kraus, Ken Mallory, Dan Pearlman, Carl Safina, Vicke Starczak, Gregory Stone, and particularly Carolyn Levi, for ideas, information, and suggestions for improving this paper. Jayne Doucette and Jack Cook did the graphic illustrations, for which we are grateful. We thank Paul Erickson for the slide show that was part of the oral presentation. C.A. Butman was supported by a Pew Charitable Trusts Fellowship in Conservation and the Environment. This is Contribution 9620 from the Woods Hole Oceanographic Institution.

Suggestions for Further Reading

Angel MV. 1993. Biodiversity of the pelagic ocean. Cons Bio 7:760–72.

Butman CA, Carlton JT. 1995. Marine biodiversity: some important issues, opportunities and critical research needs. Rev Geophys Suppl:1201–9.

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Chandler M, Kaufman L, Mulsow S. 1996. Human impact, biodiversity and ecosystem processes in the open ocean. In: Mooney HA, Cushman JH, Medina E, Slaad OE, Schulze ED (eds). Functional roles of biodiversity: a global perspective. New York NY: J Wiley. p 431–74.

Dobson AP. 1996. Conservation and biodiversity. New York NY: Sci Amer Lib. p 264.

Huston MA. 1994. Biological diversity: the coexistence of species on changing landscapes. New York NY: Cambridge Univ Pr. p 681.

Jackson JBC. 1997. Reefs since Columbus. Coral Reefs 16 Suppl:S23–S32.

Jeffries MJ. 1997. Biodiversity and conservation. New York NY: Routledge. p 208.

NRC [National Research Council]. 1995. Understanding marine biodiversity: a research agenda for the nation. Washington DC: National Acad Pr. p 114.

NRC [National Research Council]. 1996. Stemming the tide: controlling introductions of non-indigenous species by ships' ballast water. Washington DC: National Acad Pr. p 141.

Norse EA (ed). 1993. Global marine biodiversity: a strategy for building conservation into decision making. Washington DC: Island Pr. p 383.

Oceanus. 1995. Marine biodiversity I. Fall/Winter.

Oceanus 1996. Marine biodiversity II. Spring/Summer.

Safina C. 1995. The world's imperiled fish. Sci Amer 273:46–53.

Perlman DL, Adelson G. 1997. Biodiversity: exploring values and priorities in conservation. Malden MA: Blackwell. p 182.

Perrings C, Maler KG, Folke C, Hollings CS, Jansson BO (eds). 1995. Biodiversity loss: economic and ecological issues. New York NY: Cambridge Univ Pr.

Peterson M (ed). 1992. Diversity of oceanic life: an evaluative review. Washington DC: The Center for Strategic and Information Studies. p 108.

Reaka-Kudla ML, Wilson DE, Wilson EO (eds). 1997. Biodiversity II: understanding and protecting our biological resources. Washington DC: Joseph Henry Pr. p 551.

Wilson EO (ed). 1988. Biodiversity. Washington DC: National Acad Pr. p 521.