One
Introduction

Marine Biodiversity is Changing and it Matters

Approximately 70 percent of the Earth's surface is covered by water, and most of that is marine. Like all biological systems, the oceans are experiencing an ecologically and evolutionarily unprecedented series of stresses, many of which are changing the structure and organization of marine communities. Because humans rely on the oceans for food, mineral resources, and recreation, and because marine life offers potential future benefits to society, such as in the area of biomedical products, it is critical to develop conservation and management strategies that facilitate the long-term sustained use of the sea by humans while minimizing impacts on nature.

Yet to be determined is the ultimate impact of a growing human population on marine biota—from the smallest plankton to the largest whales, living on the bottom or in suspension, at depths ranging from the highest intertidal shores to the abyss (e.g., Boxes 1 and 2). Continuing human population expansion is reflected in alterations to the global atmosphere and heat budgets, changes in hydrologic and sedimentary regimes, chemical contamination and ocean dumping, and the accelerating overexploitation of the ocean's fish and invertebrate stocks (Ray and J.F. Grassle, 1991; M.N.A. Peterson, 1992; Norse, 1993; Weber, 1993; 1994; NRC, 1994a).

Marine life has been altered to large extents, sometimes with dramatic consequences.

  • Oyster populations of the Chesapeake Bay that once filtered the entire estuary once a week now filter it only once a year because of stock depletion from overfishing and disease (Newell, 1988).


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--> One Introduction Marine Biodiversity is Changing and it Matters Approximately 70 percent of the Earth's surface is covered by water, and most of that is marine. Like all biological systems, the oceans are experiencing an ecologically and evolutionarily unprecedented series of stresses, many of which are changing the structure and organization of marine communities. Because humans rely on the oceans for food, mineral resources, and recreation, and because marine life offers potential future benefits to society, such as in the area of biomedical products, it is critical to develop conservation and management strategies that facilitate the long-term sustained use of the sea by humans while minimizing impacts on nature. Yet to be determined is the ultimate impact of a growing human population on marine biota—from the smallest plankton to the largest whales, living on the bottom or in suspension, at depths ranging from the highest intertidal shores to the abyss (e.g., Boxes 1 and 2). Continuing human population expansion is reflected in alterations to the global atmosphere and heat budgets, changes in hydrologic and sedimentary regimes, chemical contamination and ocean dumping, and the accelerating overexploitation of the ocean's fish and invertebrate stocks (Ray and J.F. Grassle, 1991; M.N.A. Peterson, 1992; Norse, 1993; Weber, 1993; 1994; NRC, 1994a). Marine life has been altered to large extents, sometimes with dramatic consequences. Oyster populations of the Chesapeake Bay that once filtered the entire estuary once a week now filter it only once a year because of stock depletion from overfishing and disease (Newell, 1988).

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--> Box 1: Has human hunting of whales altered deep-sea biodiversity? WAITING FOR A WHALE: HUMAN HUNTING AND DEEP-SEA BIODIVERSITY Organisms in the deep sea are highly food-limited, relying primarily on organic matter raining down from above. Whale carcasses may be particularly important because they are large and sink fast enough with sufficient tissue still intact for exploitation. Lipid-rich whale skeletons have further been found to support an animal community nourished largely by sulfur-reducing chemoautotrophic bacteria. Whale skeleton-associated species are similar, and in some cases identical, to organisms previously thought to be restricted to the chemosynthetic-based hydrothermal vents and other deep-sea microbial reducing habitats. Whale skeletons scattered like islands in the deep sea may thus provide some of the critical stepping stones for organisms between hydrothermal-vent communities, themselves insular and temporary habitats. Given the potentially important role of whales to deep-sea biodiversity, these communities may have been altered by human hunting of whales. A profound effect of whaling was a vastly reduced—and in some regions, obliterated—whale skeleton supply to the deep sea due to an acute decrease in hunting-generated carcasses (after the turn of this century, whalers retained the entire animal) and to a dramatic decrease in whale populations. This decrease meant a severe spatial interruption, if not elimination, of dispersal corridors between reducing-habitat communities, with potentially marked alterations to biodiversity in hot-vent and cold-seep regions. Unfortunately, the magnitude and consequences of changes in biodiversity resulting from this type of human activity are difficult to evaluate because of the lack of data on most whale population sizes and distributions, because the region impacted is far removed from the disturbance source, and because effects are being considered nearly a century after the fact. This example does, however, underscore the importance of ''thinking big" and "thinking remotely" in evaluating the potential impact of society's activities on nature.     Key References: Stockton and DeLaca (1982); C.R. Smith (1985, 1992), C.R. Smith et al., (1989); Bennett et al., (1994); Deming et al., (in press); Butman et al., (in press). The "inexhaustible" fisheries of the great fishing banks (such as Georges Banks and the Grand Banks) are verging on exhaustion or have now been closed (Anthony, 1990), and the historical human hunting of the great whales has resulted in many threatened species (Laws, 1977; Evans, 1987). The coral reefs of the Caribbean, Hawaii, and parts of Australasia are threatened by multiple human activities, such as overfishing (Russ, 1991), physical habitat alteration and destruction (Rogers, 1985; Salvat, 1987; WCMC, 1992), and sedimentation associated with logging and land-based development (Hodgson and Dixon, 1988; Kuhlmann, 1988; Ogden, 1988).

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--> Box 2: Did the elimination of large vertebrates such as manatees, turtles, and groupers from tropical ecosystems significantly alter biodiversity? ELIMINATION OF LARGE VERTEBRATES FROM TROPICAL ECOSYSTEMS Large marine vertebrates (such as whales, manatees, turtles, groupers, and the extinct Steller's sea cow, Caribbean monk seal, and great auk) have been systematically removed from the oceans by humans over the past 500 years. The ecological effects of the reduction or complete elimination of most large vertebrates remain unknown (sea otter impacts on kelp and sea urchins in the Eastern Pacific are an exception). Eighteenth-century Caribbean explorers found extraordinarily abundant populations of large vertebrate grazers (manatees, turtles, and parrot fish), large invertebrate grazers (conch snails), and large carnivorous fish (groupers). These animals consumed seagrasses, algae, sea urchins, other fish, and many other animals. The removal of these consumers must have substantially affected communities both directly (e.g., altering food pyramids and trophic structure) and indirectly (e.g., the resulting increases in seagrass populations altering coastal sedimentation processes). Unfortunately, scientists arrived in the Caribbean two centuries after the large animal expulsion commenced. The elimination of large consumers from a broad region is an example of how early historic alterations at one trophic level can markedly impact modern assumptions and interpretations of both natural biodiversity patterns at other trophic levels and overall ecosystem function. The need for an appropriate retrospective context is clear and further argues for the use of human exclusion experiments (see Box 13) to assess the effects of historical hunting on those species that still survive elsewhere.     Key References: Estes and Palmisano (1974); May et al., (1979); Hay (1984); Thayer et al., (1984); Duggins et al., (1989); Vermeij (1993); Jackson (1994). Invasive species are increasing dramatically, with more than 3,000 species a day in motion inside the giant aquaria that serve as ballast tanks in oceangoing vessels (Carlton and Geller, 1993), sometimes completely altering the trophic structure of bays and estuaries into which the ballast water is discharged (e.g., Nichols et al., 1990; Horoshilov, 1993). Filling and development of coastal habitat has resulted in total wetland losses of 50 percent in Washington, 74 percent in Maryland and Connecticut, and 91 percent in California (Dahl et al., 1991), with a concomitant loss of critical seagrass and marsh habitat that host a diversity of invertebrates and fish (including many economically important species), protect coastlines from erosion, enhance nutrient cycling, and improve water clarity (Fenchel, 1977). There are thus significant reasons for concern. The timing is critical for

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--> determining the processes that contribute to these fundamental changes and for developing a predictive understanding that will allow preservation and restoration of the ocean's biodiversity. The dual issues of change and loss of marine biodiversity are not trivial and have unified marine scientists—oceanographers, ecologists, and taxonomists—in a common cause. National and international social and economic implications of accelerating change bear directly on interrelated subjects, such as: the ocean's capacity to sustain economically significant fisheries, the quality of bays and estuaries as nurseries for important stocks, the loss of species with important potential for biomedical products, the increasingly chronic nature of blooms of toxic algae, the recreational value of ocean margins, and the aesthetic value of marine environments that remain close to their aboriginal state. Marine biological diversity is changing, and it does matter. This document identifies the urgent need for a national research program on the biological diversity of marine systems. In this research plan, biodiversity is defined as the collection of genomes, species, and ecosystems occurring in a geographically defined region. This agenda focuses on a novel program where ecological and oceanographic research would be integrated at all relevant spatial scales, from local to regional, and over appropriate time scales for distinguishing changes in biodiversity due to effects of human activities from natural phenomena. Integral to this initiative are taxonomy (here defined as the descriptive branch of the larger field of systematics) for documenting the magnitude and patterns of biodiversity, and predictive models for hypothesis development, testing, and extrapolation, and for developing guidelines for management and conservation. The Depth and Breadth of Underdescribed Marine Biodiversity "The future historians of science may well find that a crisis that was upon us at the end of the 20th century was the extinction of the systematist, the extinction of the naturalist, the extinction of the biogeographer—those who would tell the tales of the potential demise of global marine diversity." Carlton (1993, pg. 507) There are many exciting recent discoveries of previously unknown marine organisms that form critical links in ecosystem function. These discoveries often were facilitated by the development of new sampling and analytical techniques and emphasize a science that has been exploring just the periphery of the biodiversity frontier in the oceans. Examples include the following:

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--> The brown tides that led to the demise of the bay scallop industry of southern New England in the 1980s were caused by a protist that was previously unknown and had no genus or species name (Sieburth et al., 1988). Major estuarine fish kills have now been associated with a previously undescribed "phantom" dinoflagellate whose existence and identity were only announced in 1992 (Burkholder et al., 1992). In the open ocean, the prochlorophytes, a group of marine, free-living, bacterial primary producers, were not discovered until the late 1980s—and yet they are now known to account for up to 40 percent of the chlorophyll in some ocean regions (Chisholm et al., 1988; R.J. Olson et al., 1990; S.W. Chisholm, pers. comm., 1994). Species of marine nonphotosynthetic microbes—bacterial taxa now known as Eubacteria and Archaea—are now being discovered at a rapid rate thanks to new molecular genetic techniques and are the basis (along with enhanced awareness of the widespread abundances of marine viruses [Bergh et al., 1989; Proctor and Fuhrman, 1990]) for rapidly evolving concepts of marine microbial diversity and the role of microbes in global geochemical cycles (Box 3). What was once thought to be a single species of algal symbiont in the Caribbean star coral (that is in fact at least three coral species, as discussed later) is now known to be three major groups of symbionts (Rowan and Powers, 1991, 1992) that occur at different depth zones (Rowan and Knowlton, in press). The ecological significance of these findings is currently being investigated, including the possibility that the symbiont species have different propensities for expulsion from the three coral species, which may help to explain the phenomenon of variable coral-bleaching episodes (N. Knowlton, pers. comm., 1994). There are numerous undescribed species in even the most familiar of ocean environments—ranging from the common harpacticoid copepods and worms of shelf muds to the tiny nematodes and highly colorful sea slugs in tropical lagoons. Table 1 provides a glimpse of the magnitude of underdescribed diversity of marine invertebrates at the level of individual taxa. At the level of entire ecosystems, there are environments such as the deep sea and polar regions that are so undersampled that hundreds of new species are discovered during each expedition to a new area. Indeed, knowledge of the ecology and evolutionary history of the deep sea has been fundamentally altered by the discovery that the diversity of abyssal communities is dramatically higher than previously thought (J.F. Grassle, 1991; J.F. Grassle and Maciolek, 1992). None of these estimates of underdescribed marine biodiversity takes into account the innumerable and ecologically important benthic and planktonic protists, which alone may comprise at least 34 phyla and 83 classes (Corliss, 1994), nor the vast complexity of the undescribed parasites that live on and in other marine organisms. New views of the true scale of marine biodiversity dictate substantial rethinking of current understanding of the processes that create and

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--> Box 3: Knowledge of marine microbial biodiversity is being revolutionized by the application of molecular genetic techniques. MOLECULAR ECOLOGY AND SYSTEMATICS: PROVIDING NEW PERSPECTIVES ON MARINE MICROBIAL DIVERSITY The application of molecular genetic techniques and approaches is now providing a remarkable new perspective on the biodiversity of the abundant and ubiquitous planktonic bacterial assemblages in the oceans. Oceanic microbes are integral components of marine food webs: they often dominate the plankton biomass, they are extremely important in the Earth's biogeochemical cycles, and they are responsible for much of the cycling of organic matter in the sea. The biodiversity of these assemblages is virtually undescribed. Conventional identification methods involving culturing have identified an estimated 1 percent of the microbes present in marine samples. With molecular techniques it is now possible to begin to determine the composition, diversity, and variability of the remaining 99 percent of the marine bacterioplankton. The vast prokaryotic assemblages found in the food-limited (oligotrophic) open ocean, for example, are now being described, with important implications for understanding their functions in these ecosystems and their responses to environmental perturbation. The recent discovery of abundant and widespread new phyla of microorganisms underscores the extent of ignorance with regard to microbial biodiversity. Indeed, in some cases these organisms are known solely from their DNA sequences. The application of molecular techniques to discover new microbial groups in the ocean, supplementing traditional microbiological techniques, throws open a door to the unknown: for example, fundamentally new types of organisms appeared in only the first few plankton samples examined with molecular genetic techniques from one small site in the open ocean off of San Diego, California.     Key References: DeLong et al., (1989, 1993); DeLong (1992); Fuhrman et al., (1992, 1993); Giovannoni et al., (1990, 1993); Schmidt et al., (1991); Ward et al., (1990). maintain diversity, and of the impacts of human society on ocean ecosystems. It is probable that these breakthroughs represent only the smallest fraction of the exciting discoveries that lie ahead. Most of the species in the ocean may still remain undiscovered and undescribed (e.g., Table 1). These gaps in knowledge of the magnitude and extent of marine biodiversity have real consequences. Inadequate knowledge of the species present in a given marine community or ecosystem limits understanding of ecosystem function and predictions of how human alterations impact that function. Understanding which species are critical in energy flow from lower to higher trophic levels in a food chain, for example, may be nearly impossible if many members of a particular group of prey or predators are undetected or undescribed. As noted elsewhere in

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--> TABLE 1 Examples of the Magnitude of Underdescribed Biodiversity Among Marine Invertebrates in Familiar and Easily Accessible Marine Environments Site Taxon Number of Undescribed Species out of Total Collected in the Taxon Sourcea Gulf of Mexico Copepods (harpacticoids) 19-27 of 29 (shelf site, 18 m) D. Thistle New Guinea Snails, sea slugs 310 of 564 (one lagoon) T. Gosliner Philippines Snails, sea slugs 135 of 320 (one island, multiple sites) T. Gosliner Georges Bank Marine polychaete worms 124 of 372 (shallow shelf, multiple stations) J. Blake Hawaii Marine polychaete worms 112 of 158 (6 liters of coral reef sediment, one island) Dutch (1988) Great Barrier Reef Marine flatworms (polyclads) 123 of 134 (two islands) Newman and Cannon (1994) aPersonal communication to J.T. Carlton unless indicated otherwise. NOTE: The third column represents an estimate of the number of undescribed species of a given taxon found in samples taken at the site and habitat indicated. Sampling effort and number of samples varied among studies. this report, this does not mean that every species in a system must be described in order to understand that system. Rather, sufficient knowledge of the breadth and depth of the diversity of animals, plants, microbes, and other life present at a site or in a region is needed to understand the ecological roles of abundant and critical species and the functioning of the ecosystem. These considerations are not limited to ecological interest; as with the discovery of previously newly described terrestrial species which proved to be of biomedical value, the next newly described organism in the sea could prove to be a key species in the rapidly developing field of marine biotechnology (see Box 14). Significant Opportunities for Forging New Horizons Although the number of undescribed, underdescribed, and inaccurately described species in the oceans appears daunting, new techniques and approaches are rapidly improving the ability to detect and describe the genetic, species, and ecosystem diversity of the oceans.

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--> Genetic Diversity With new molecular techniques, surprising levels of genetic diversity are now being discovered in marine organisms ranging from phytoplankton (Wood and Leathern, 1992) to sea turtles (Bowen et al., 1991, 1993), often calling into question critical concepts of speciation in the sea (Palumbi, 1992). Application of molecular techniques for evaluating intraspecific genetic diversity has further provided valuable information for the identification and management of endangered species. Evidence from mitochondrial DNA (mtDNA) analysis has shown, for example, that the last remaining and highly restricted population of several hundred Kemp's ridley sea turtles is, in fact, genetically distinct from the closely related sister species, the olive ridley, that is more widespread, thus confirming the need to protect the former species (Bowen et al., 1991). Recent mtDNA analysis of humpback whales has shown genetic differences over surprisingly short distances with important implications for conservation (see Box 11). Species Diversity Molecular genetic techniques combined with classic morphometric approaches are now revealing numerous sibling species complexes within what were frequently believed to be single species (Knowlton, 1993). Examples include the following: Perhaps one of the world's best-known marine invertebrates, the mussel Mytilus edulis, is now known to be three distinct species (McDonald et al., 1992)—and yet this mussel has formed the basis, on the presumption that it was one species, for the pollution-monitoring "International Mussel Watch Program" (NRC, 1980). The different growth rates of at least two of these cryptic species evidently result in observed different body burdens of some contaminants (Lobel et al., 1990), leading to further explorations of the implications of species-specific variations in contaminant uptake on comparative programs like Mussel Watch (B. Tripp, pers. comm., 1994). A number of abundant and widespread tropical species of corals and bryozoans, the subjects of intensive ecological studies, are now known to be species complexes (e.g., Knowlton and Jackson, 1994). A particularly striking example is the common Caribbean star coral Montastraea annularis, which is now known to be at least three distinct species (Knowlton et al., 1992). Furthermore, the three species have different growth rates and carbon isotope ratios, parameters routinely used to estimate past climatic conditions, thus affecting previous estimates of global climate change. The marine worm Capitella "capitata" was once regarded as a cosmopolitan "indicator" species of disturbed, organic-enriched sediments, but it is now known to be 15 or more sibling species that occur from the intertidal zone to the deep sea (J.P. Grassle and J.F. Grassle, 1976; J.F. Grassle and J.P. Grassle, 1978;

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--> J.P. Grassle, 1980; J.P. Grassle, pers. comm., 1993). Most of the species differ in some of their life-history characteristics, such as larval development type, brood size, and generation time. Thus, the use of sibling species within this complex as bioassays of environmental degradation hinges on understanding the ecological consequences of their life-history variation. Cryptic sibling species have now been discovered in important commercial species, including the oyster Crassostrea, the shrimp Penaeus, and the stone crab Menippe, with important implications for conservation and management (Knowlton, 1993). Examples exist for both exploited and protected species. Identification of the Spanish mackerel Scomberomorus maculatus as two species that mature at different ages and sizes (Collette et al., 1978) dictates the avoidance of using life history data of the first species for management of the second species. Use of molecular techniques has also suggested that the common dolphin (Delphinus delphis) is actually two species that may have different distributions and abundances (Rosel et al., 1994), and therefore different requirements for protection. These types of discoveries help to foster an appreciation of the true extent of marine biodiversity, and add a considerable new dimension to estimates of how many species exist in the ocean. It is clear, however, that molecular techniques provide one of the most powerful means for revealing a new understanding of the ocean's complexity (see Box 3). Habitat and Ecosystem Diversity Advanced instrumentation and sampling have revealed new species assemblages in novel habitats in the oceans, such as hydrothermal vents (J.F. Grassle, 1986; Tunnicliffe, 1991), whale carcasses (C.R. Smith et al., 1989), wood debris (Turner, 1973, 1981), and sites of hydrothermal, brine, and hydrocarbon seepage (Williams, 1988; Kennicutt et al., 1989; Southward, 1989; MacDonald et al., 1990). As with the discovery of new genomes and new species, it is doubtful that hydrothermal vents or whale skeleton biotas have closed the final chapter on the discovery of novel habitats or ecosystems in the sea. Are there, for example, unique biotas in the abyssal depths of the mid-Atlantic Ocean singularly tied to sinking masses of the pelagic seaweed Sargassum? Moreover, new discoveries are unlikely to be limited to just the vast deep-sea depths. Discovery of novel chemoautotrophic associations, shallow and deep (reviewed in Bennett et al., 1994), is a striking reminder that the biodiversity of the majority of the Earth's surface may be dependent on yet undiscovered and unanticipated habitat diversity. Continually improving capabilities for exploring large regions of the ocean floor and water column (e.g., see Box 12) now set the stage for searching the sea in ways impossible to imagine only a few years ago.