C REDI T

78 SCIENTIFIC AMERICAN NOVEMBER 2006 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. Reviving Dead BY LAURENCE MEE Zones How can we restore coastal seas ravaged by runaway plant and algae growth caused by human activities?

magine a beach crowded with vacationers en- the globe have emerged [see map on next page]. joying the hot summer sun. As children paddle Determining the causes of this destruction, I about in the shallows, foraging for shells and how it might be prevented and what to do to bring other treasures, dead and dying animals begin to affected areas back to life has been a prime focus wash ashore. First, a few struggling fish, then of my research since the early 1990s, when I pub- smelly masses of decaying crabs, clams, mussels lished my first paper on the ecological crisis in the and fish. Alerted by the kids’ shocked cries, anx- Black Sea. My work and that of others has now ious parents rush to the water to pull their children revealed important details of the events that de- away. Meanwhile, out on the horizon, frustrated grade coastal ecosystems in many parts of the earth commercial fishermen head for port on boats with and has turned up new information that could empty nets and holds. help establish pathways to recovery. This scene does not come from a B horror mov- ie. Incidents of this type actually occurred peri- odically at many Black Sea beach resorts in Roma- nia and Ukraine in the 1970s and 1980s. During that period an estimated 60 million tons of bot- tom-living (or benthic) life perished from hypox- ia—too little oxygen in the water for them to sur- vive—in a swath of sea so oxygen-deprived that it could no longer support nonbacterial life. At its extreme in 1990, the “dead zone,” lo- cated in the northwestern part of the sea off the mouth of the Danube River, extended over an area the size of Switzerland (40,000 square kilometers). On the other side of the world, in the Gulf of Mex- BLACK SEA DEAD ZONE became evident when dying sea life ico off the Mississippi River delta, another huge began washing ashore near the mouth of the Danube River dead zone appeared in the mid-1970s, which at its in the 1970s. Above, dead fish are left strewn across a Black Sea beach by the high tide. A satellite photograph of largest reached 21,000 square kilometers. In the the western Black Sea from 2000 (left) shows the huge past two decades, additional reports of dying or blooms of floating microscopic plants that resulted from depleted areas in coastal seas and estuaries across the river’s nutrient-rich discharge. C REDI T

www.sciam.com SCIENTIFIC AMERICAN 79 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. Baltic Sea

Black Sea Oregon coast

Chesapeake Bay Seto Inland Sea

Gulf of Mexico

OXYGEN DEPLETION Year-round Periodic—usually annual Occasional

DEAD ZONES—areas starved of oxygen (by bacterial decay of overabun- 1990. Polluted runoff from the land often triggers dead zone conditions, dant plant growth) and thus of most animal life—occur in coastal seas, often although some result naturally. The dead zone in the northwestern Black near developed countries. The number of regions affected has doubled since Sea is now much smaller than it was at its largest a few decades ago.

Dead Zone Formation blooms and other unwanted effects. green or even brown as phytoplankton ocean researchers today link Plants enter the food chain when tiny populations burgeon, and the shade they the creation of most dead zones to a phe- seaborne animals (zooplankton), herbiv- cast deprives plants living below them of nomenon called eutrophication, the orous fish and filter-feeding bottom essential sunlight. Sea grasses in shallow overenrichment of the sea by nutrients dwellers such as mussels and oysters bays also become covered with small at- (principally compounds containing ni- graze them or when they die, decay, fall tached algae (epiphytes) and can ulti- trogen and phosphorus) that promote to the seabed, undergo bacterial decom- mately be smothered and die. Algae can ) plant growth. A certain amount of these position and are incorporated into the in addition envelop coral reefs, especial- “fertilizers” is essential to the health underlying sediments. This organic bot- ly where heavy fishing pressure has his page t

(

of phytoplankton—floating algae and tom matter feeds the animals living there, thinned the ranks of resident grazers. ) ; other microscopic photosynthesizers including worms, shrimp and some fish. A major upsurge in the numbers of that form the base for most marine food Normally the numbers of phytoplank- phytoplankton and epiphytes immedi- chains—as well as for the well-being ton are limited by the availability of light ately causes difficulties for nearby sea

of the sea grasses and algae that live and nutrients and by grazing. But large life, but an even worse situation arises preceding pages

on the floors of shallow, well-lit seas. increases in nitrogen and phosphorus when oxygen levels in bottom waters de- ) (

But too much of these nutrients in illu- concentrations enable these minute photo- cline. Lower oxygen concentrations ap- UNEP GEO YEARBOOK 2003

minated waters greatly accelerates plant synthetic organisms to multiply in great pear when bacteria consume oxygen to dead f ish ( growth, leading to disruptive algal profusion. The water eventually turns break down the masses of organic matter that result from animal wastes and the dead bodies of organisms that multiply Overview/Coastal Seas in Trouble SOURCE: BASED ON ); RADU MIHNEA during eutrophication. Much of this ma- ) ; ■ River-borne plant nutrients from the land are killing off life in parts of shallow terial accumulates on the seafloor, where seas around the globe, resulting in so-called dead zones. oxygen is relatively scarce to begin with. ■ Fertilizing chemicals cause microscopic plants floating near the surface Oxygen finds its way into the water satellite image to overgrow, depriving any plants living on the bottom of light and leading to from either photosynthesis or physical satellite image large increases in the amount of decaying organic material falling to the diffusion from the air at the sea surface. seafloor. The bacteria living off the dead organisms use up seafloor oxygen, Should an area whose bottom is covered thereby causing the loss of most animal life there. with dead plants also feature a strong ■ Significant reductions in agricultural and sewage runoff, as well as controls density gradient that prevents mixing on overfishing, can restore these key marine ecosystems. with the overlying water column, the THE VISIBLE EARTH/NASA ( oxygen at the bottom can soon become THE VISIBLE EARTH/NASA (

80 SCIENTIFIC AMERICAN NOVEMBER 2006 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. exhausted, leading to the die-off of entire minuscule zooplanktonic crustaceans. chain engenders more organic matter on animal communities. (Such gradients These animals, in turn, serve as food for the seafloor, which enhances the risk can stem from temperature or salinity fish. Increased nutrient concentrations that a dead zone will follow. differences in the water at various depths.) affect the mix of phytoplankton species Ecosystems altered by eutrophica- This basic sequence— eutrophication such that diatoms often become out- tion also become more vulnerable to in- leading to phytoplankton blooms, excess numbered by smaller or less digestible vasion by foreign species, which can ar- bacterial activity at the bottom, oxygen types. When eutrophication produces rive, for example, in the ballast discharge depletion, and the death of existing plants massive phytoplankton blooms, cope- from transoceanic ships. In the 1980s and animals—has occurred in almost ev- pods often are unable to graze on the the comb jellyfish Mnemiopsis leidyi, ery dead zone examined by researchers. new, abundant phytoplankton species as which probably originated off the east- The details do vary, however, ac- well as the large quantities of organic de- ern coast of the U.S., took up residence cording to the local biological and phys- tritus that result from the disruption of in the Black Sea. By 1990 this voracious ical conditions as well as the rate of sup- the natural ecosystem. This change fa- dead-end predator dominated the eco- ply of plant nutrients from the land. vors the growth of highly tolerant gelat- system completely, at its maximum at- Poorly flushed estuaries, for example, inous organisms such as Noctiluca (re- taining an astounding density of up to are particularly vulnerable to the effects sponsible for nighttime phosphorescence five kilograms per square meter. of eutrophication, because low water that occurs when the water surface is Sometimes shellfish reefs can help flows lead to slow replenishment of oxy- disturbed). Biologists sometimes call stave off degradation of an ecosystem. In gen in bottom waters. This reduction in these jellyfishlike fauna “dead-end spe- many estuaries on the eastern seaboard oxygen has been a persistent problem cies” because higher-level predators have of the U.S., oysters act as ecosystem en- along the eastern seaboard of the U.S., difficulty living off them. Their presence gineers by accumulating into huge reefs where large estuaries, such as the Chesa- reduces the efficiency of the food chain, rising several meters from the seabed; peake Bay, have been affected. leading fish stocks to wane. these reefs support a diverse assemblage The excess of nitrogen and phospho- Such an imbalance in the food chain of organisms, including flounder, snap- rus arriving in coastal seas results in large can be worsened by intense commercial per, silver perch and blue crabs. measure from the changing habits of peo- fishing, particularly where these efforts Hunter Lenihan of the University of ple living in the areas draining into the target high-value “top predator” species California, Santa Barbara, and Charles sea. Rising fossil-fuel use (which releases such as cod, hake, dorado or horse H. Peterson of the University of North nitrogen into the atmosphere), effluent mackerel. Loss of apex fish species leads Carolina at Chapel Hill have shown, for from the mass breeding of food animals to rises in the numbers of small prey example, that the tops of oyster reefs in and intensive farming, and the construc- fish, which results in fewer zooplankton North Carolina’s Neuse River became tion of sewage systems that empty into (the food of the small fish) and, con- refuges for displaced bottom-water spe- bodies of water all lead to greater nutri- sequently, even more phytoplankton. cies at the onset of dead zone formation ent emissions into watersheds. The Mil- Scientists call this sequential process because they projected above the deoxy- lennium Ecosystem Assessment released “trophic cascading.” An inefficient food genated water layer. Mechanical oyster by the United Nations in 2005 reported that the supply of nitrogen-containing compounds to the sea grew by 80 percent from 1860 to 1990. It predicted that the overall outflow to the oceans from hu- man activities will increase by an addi- tional 65 percent by midcentury. Dead zones are thus likely to become even more widespread unless society takes prompt action to reduce plant nutrient runoff. Watery Graveyard although emergence of a dead zone is the final stage of the eutrophica- tion process, marine systems, especially the animal populations, undergo chang- es long before then. A healthy coastal DEAD—AND RECOVERED—BOTTOM LIFE are apparent in these views of two locations on the Black marine food chain often starts with sili- Sea bed earlier this year. The photograph on the left shows a largely depleted area that is covered ca-shelled phytoplankton called dia- with the shells of mussels killed by a lack of dissolved oxygen. On the right is a recovering site

TIM STEVENS toms, which are consumed by copepods, with a thick and diverse cover of algae and large numbers of ascidians (sea squirts).

www.sciam.com SCIENTIFIC AMERICAN 81 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. KEY STAGES IN THE FORMATION OF A DEAD ZONE

The events underlying the creation of the Black Sea dead zone were fairly typical HEALTHY ECOSYSTEM (PRE-1970S) of how similar oxygen-depleted (hypoxic) Oxygen areas form, although the details vary from Phytoplankton level case to case. At the root was eutrophication, an excessive infl ow of plant nutrients that O2 resulted in an overgrowth of algae and other High small fl oating photosynthetic plants, which led indirectly to hypoxia and to the death of plants and animals in the lower depths. Zooplankton The decline of the ecosystem followed three stages described initially by Tatsuki O2 Nagai of Japan’s Fisheries Research Agency, Moderate who studied one of the fi rst known hypoxic regions. These conditions appeared in Japan’s Seto Inland Sea in the early 1960s. He called the natural state the “sea of red O2 bream” (a predator species targeted by local fi shers). Then came the “sea of anchovies,” High when predator species declined, leaving mainly small prey fi sh behind. Finally, there came a “sea of jellyfi sh,” in which most other species died or fl ed, leaving highly The near-surface coastal waters of the northwestern Black Sea initially contained tolerant invading species dominant. Nagai a diverse mix of phytoplankton (fl oating algae and other microscopic plants) as well also was among the fi rst to identify as varied fi sh and other organisms. Shallow waters close to shore featured shoals of immature anchovies, mackerel and bonito. At the middle depths lived large schools overfi shing as a contributor to degradation of top predators, such as whiting, and numerous prey fi sh, plus some jellyfi sh. At the of the sea’s food chain (by removing the bottom, communities of mussels as well as gobies, turbot, sturgeon and hermit crabs top predator fi sh). thrived among extensive meadows of sea grasses and brown and red algae. harvesting frequently shortens the height cals was the Danube, which drains much played an even more significant role. of these reefs, however, which helps to of the watersheds in 11 countries across Before the 1960s the shallow north- destroy the natural resilience of these central Europe, from Germany to Roma- western region of the Black Sea was a di- ecosystems. nia. The main culprits were agricultural verse and highly productive system that runoff, urban and industrial wastewater, included extensive near-shore mats of Black Sea Catastrophe and, in the case of nitrogen compounds, bottom-living brown algae and, further the black sea offers a dramatic ex- atmospheric transport. At least half the offshore, the largest red algae community ample of how undersea ecosystems can increased nitrogen poured into the Black on earth—a fi eld of Phyllophora the size be destroyed by a surplus of nutrients and Sea resulted from modernized farming of the Netherlands. These natural algae also provides insight into how they can practices, including intensive use of fer- meadows coexisted with enormous beds be resuscitated. The waters of the north- tilizers and the establishment of huge of mussels and other bivalves, and the western area of the sea fell prey to eutro- animal production facilities. These agri- whole system supported a large number phication when fl ows of nitrogen and cultural activities also contributed to the of invertebrate and fi sh species. The algae phosphorus compounds from the land rise in the phosphorus effl uent, but in- helped to oxygenate the bottom waters, doubled between the 1960s and 1980s. dustrial and urban waste discharges and the mussels filtered the seawater, The principal pipeline for these chemi- laden with polyphosphate detergents thereby maintaining good light condi- tions for photosynthesis. This ecosystem LAURENCE MEE is director of the Marine Institute at the University of Plymouth in Eng- was highly resilient, being able to accom- land. He also heads the university’s interdisciplinary Marine and Coastal Policy Re- modate large variations in climate condi- search Group. An oceanographer with a Ph.D. from the University of Liverpool, Mee has tions and natural disturbances. As nutri- held research positions at the Institute of Marine and Limnological Sciences in Mexico ent effl uents escalated, however, dense and the IAEA Marine Environment Laboratory in Monaco and has coordinated the United phytoplankton blooms appeared in the

T H E A U T H O R Nations Global Environmental Facility–Black Sea Environmental Program. He became a surface waters. Such luxuriant growth Pew Fellow in Marine Conservation in 1998. Mee’s current work focuses on ways to pro- lowered water transparency, which in

tect the marine environment and the associated drainage basins and coastal areas. turn deprived the bottom algae of light SHAWN GOULD

82 SCIENTIFIC AMERICAN NOVEMBER 2006 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. KEY STAGES IN THE FORMATION OF A DEAD ZONE

The events underlying the creation of the Black Sea dead zone were fairly typical EUTROPHICATION PHASE (EARLY 1970S) DEAD ZONE (LATE 1980S) of how similar oxygen-depleted (hypoxic) Oxygen Oxygen areas form, although the details vary from level level case to case. At the root was eutrophication, an excessive infl ow of plant nutrients that O2 O2 resulted in an overgrowth of algae and other small fl oating photosynthetic plants, which Very Very high led indirectly to hypoxia and to the death of high plants and animals in the lower depths. The decline of the ecosystem followed three stages described initially by Tatsuki Pycnocline Nagai of Japan’s Fisheries Research Agency, (water density who studied one of the fi rst known hypoxic boundary) regions. These conditions appeared in Japan’s Seto Inland Sea in the early 1960s. He called the natural state the “sea of red O2 O2 bream” (a predator species targeted by local Very Very fi shers). Then came the “sea of anchovies,” low low when predator species declined, leaving mainly small prey fi sh behind. Finally, there came a “sea of jellyfi sh,” in which most other species died or fl ed, leaving highly With growing infl uxes of the nutrients nitrogen and phosphorus from terrestrial Eventually, increased shading and rampant hypoxia on tolerant invading species dominant. Nagai runoff, the ecology of the Black Sea coastal region began to change. Massive the seabed fi nally left the bottom waters devoid of life. also was among the fi rst to identify phytoplankton blooms turned the water green or even brown, depriving plants Heavy fi shing had already reduced the numbers of predator living below of sunlight and depositing a steady stream of decaying organic matter fi sh species, and ultimately these and most other large overfi shing as a contributor to degradation in the bottom. Bacteria on the seabed then consumed great amounts animals disappeared from the area. Opportunistic invading of the sea’s food chain (by removing the of oxygen as they feasted on the organic matter and the dead plants, thus species, notably the comb jellyfi sh Mnemiopsis leidyi, top predator fi sh). producing hypoxia on the seafl oor, which killed many organisms. multiplied in great numbers in the upper depths.

and eventually led to their loss, which central economic planning. Suddenly species that had dominated before the altered the entire natural ecosystem. farmers there had little capital to buy onset of dead zone conditions. During the summer months, when fertilizer, so agricultural activities the water column became stratifi ed, ox- slowed. Likewise, many giant animal Long Road to Recovery ygen levels, particularly near the seabed, farms closed, thus profoundly reducing clearly, restoring dead zones began to fall. Many of the affected bi- nutrient runoff. One former pork pro- requires, at a minimum, reducing nutri- valve communities could survive hypox- duction facility in Romania with more ent delivery from nearby lands. But ma- ia for as long as 20 days by closing their than a million pigs had generated the rine ecosystems that have collapsed be- shells and living on internal reserves of equivalent emissions of a city with fi ve cause of eutrophication and hypoxia glycogen—an animal’s chief energy-stor- million inhabitants. may not simply bounce back when hu- age carbohydrate. But when these sup- Within six years the profound drop- mans alter their activities to lower the plies were exhausted, the mollusks died off in nutrient infl ux led to shrinkage of amounts of plant nutrients reaching riv- en masse, which led bacteria and other the dead zone [see box on next page]. ers. This resistance to recovery occurs organisms to consume the remaining lo- Recovery of the sea bottom, however, for three reasons. cal oxygen as they degraded the dead was gradual. For example, studies by River catchments typically possess a animals and to release even more plant my Ukrainian colleagues have shown huge capacity for storing nutrients—ei- nutrients. By the time nearly all the oxy- that mussel beds in devastated parts of ther dissolved in groundwater or ad- gen was gone, all the fauna that normal- the northwestern shelf became fi rmly sorbed on soil particles. Years or even ly lived in the area had either migrated reestablished only in 2002, many years decades may pass before nitrogen and away in search of food and oxygen or after other communities had recovered phosphorus fertilizers and other chemi- perished. The region’s natural ecosystem substantially. This past August a re- cals stop leaching out and passing to the was thus seriously degraded. search expedition we conducted to ex- sea. Nitrogen compounds in particular The area began to recover only when amine the state of the sea revealed major tend to accumulate in groundwater. the communist regimes in eastern reestablishment of benthic algae com- Dead zones can also linger if there is Europe fell at the end of 1989, ending munities, though generally not the same a dearth of nearby healthy populations

www.sciam.com SCIENTIFIC AMERICAN 83 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. of marine plants and animals that can graded state. This new equilibrium aris- ing them is for governments to believe it provide the “seed stock” from which the es from the presence of some remaining is an important goal and to take the missing communities can be restored. species that are tolerant of eutrophica- lead. Indeed, scientists have document- Indeed, the flora and fauna that once tion’s effects and from the arrival of op- ed few cases of dead zone recovery, be- lived in the affected area may even have portunistic creatures from elsewhere. cause reducing nutrient runoff from the gone extinct. It is possible for native ma- Unfortunately, the new state is often land requires major changes in agricul- rine animals to drift large distances as quite stable. Consequently, simply cut- tural practices and wastewater treat- larvae from healthy ecosystems and to ting back the nutrient supply to its pre- ment efforts. Most such programs have eventually reestablish themselves in a eutrophication levels may not restore so far achieved only partial cuts in ter- suitable vacant biological niche. Some- the original ecosystem; lowering nutri- restrial nutrient outflows. times, however, these would-be returnee ent concentrations to levels much below To shrink nutrient loads, compre- species find themselves supplanted by their starting points may be required. hensive plans (at the scale of an entire opportunistic invading organisms that To further complicate matters, the river catchment system) must be put in have taken up all suitable habitats. threshold for change from a natural place that keep nitrogen and phospho- Finally, eutrophication often causes state to a degraded one typically comes rus on the land and out of the water. alterations in ecosystem composition earlier if an ecosystem’s resilience is di- Such efforts are currently under way in that are not easily reversed [see illustra- minished by overfishing. Therefore, it the Chesapeake Bay and in the Black tion on opposite page]. As nutrient con- may also be necessary to reduce fish- Sea. In the latter case, surrounding gov- centrations begin to climb early on, ing activities markedly before the ernments, aided by the United Nations some species decline, but ecosystems as healthy state can return. If the species of Global Environment Facility, have a whole may remain strong for a long the original system have been lost or in- agreed to pursue a landmark initiative while if the natural populations can vaders have appeared, the former pris- to maintain nutrient runoff levels at withstand a relatively high amount of tine conditions may never be regained. those of the mid-1990s, a scheme that phytoplankton growth and the like. At seems to be aiding recovery through pi- some point, however, a threshold is Eliminating Dead Zones lot-scale projects to improve farming reached at which the loss of key species knowing what to do to fix dead practices and waste treatment. yields an abrupt collapse to a new de- zones will not be enough; a key to reviv- Two serious problems must be over- The Black Sea Comes Back The recovery of the Black Sea dead zone underscores the need the next 21 years (b). Red color in a satellite image from 1979 to reduce agricultural, sewage and other nutrient runoff from (c), for instance, clearly reveals a large expanse of the land if affected areas are to be restored to health. The overfertilized water. (In that image and in d, eutrophication dead zone adjacent to the northwest coast of the Black Sea was assessed by determining the concentrations of began to revive only after the communist system collapsed in chlorophyll-a, an indicator of plant growth, in surface waters.) 1989, which prevented the continuation of intensive Within five years after the intensive farming ended, farming—including large-scale raising of livestock and heavy the degraded region had returned to life (b and d), relapsing )

application of fertilizers containing nitrogen and phosphorus only during the exceptionally hot summer of 2001. By 2002 d

(a)—that had been in place since the 1960s. Nutrient residues mussel communities in the area had reestablished them- and c made their way into the Danube River and other watersheds selves. The sea may again be at risk, however, as central and eventually down into the Black Sea, which caused the European economies recover and agriculture there begins to dead zone to appear in 1973 and to return in the summer for intensify again.

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84 SCIENTIFIC AMERICAN NOVEMBER 2006 COPYRIGHT 2006 SCIENTIFIC AMERICAN, INC. come, however, before full and sustain- able recovery of the Black Sea ecosystem High can occur. European authorities have to Threshold 2 take steps to ensure that renewed eco- Threshold 1 nomic development does not lead to the Resilient Co C ol

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Re system joining the European Union. Some farmers from western Europe, where in- tensive agricultural practices have often Threshold 3 caused eutrophic rivers and coastal wa- Low ters, are eager to buy up central Euro- Moderate (Normal) High pean farmland. Nutrient Load Next governments must reduce the intensity of commercial fishing activi- REDUCING NUTRIENT LEVELS to those present before a dead zone has formed may not be enough ties enough to allow depleted stocks of to ensure recovery, as shown in this graph, which relates the health of an ecosystem (in terms of complexity, or species diversity) and the amount of nutrients with which it must contend. A piscine predators to recover. In addi- system with high complexity and moderate terrestrial nutrient inflows tends to be highly resilient tion, the trawls and dredges on fishing until the nutrient load finally surpasses some level (threshold 1), causing the system to collapse boats destroy key benthic communities to a much less complex state. This breaking point arrives earlier (threshold 2) if overfishing has and must be regulated more effectively. depleted the numbers of top predator fish, which reduces species diversity. Unfortunately, the In fact, maritime nations worldwide new degraded state is also typically resistant to change and may recover its lost complexity only when nutrient influxes drop significantly below the starting levels (threshold 3). Even then, an must work to lessen fishing pressure on ecosystem may never return to its previous state if key species have gone extinct. eutrophic areas, difficult as that is to achieve with more than half the planet’s fully decayed and recovery begins again. only restoration of a sea filled with apex fisheries being overexploited today. Al- Scientists have observed this phenomenon predators will be acceptable. though an international agreement has in Baltic Sea estuaries. The challenge for Coastal dead zones remind us that been reached to establish by 2012 a marine resource managers is to maintain humanity cannot simply expect natural global network of marine protected ar- conditions that sustain resilient and di- ecosystems to absorb our wastes with- eas—which would help curb overfishing verse systems—even where full recovery out severe and often unexpected conse- and save the vital seed stock needed for is no longer possible. quences. We now know how to revive dead zone recovery—the agreement’s On a more subtle level, the entire dead zones, but ultimately the steps goals are unlikely to be met, because en- concept of rating the health or quality of required to do so depend on our recog- forcement mechanisms are lacking. an ecosystem depends on the values of nition of the ramifications to the envi- Even if a eutrophic ecosystem makes local inhabitants. For some, the desir- ronment of waste disposal and the de- a partial comeback, authorities must be able outcome of remedial action might gree to which we value the world’s ma- aware that a partial recovery may leave be a sea of small prey fish; for others, rine ecosystems. it in a highly unstable situation. Mussels, for example, have an extraordinary ca- MORE TO EXPLORE pacity for filtering water, and the estab- Marine Benthic Hypoxia: A Review of Its Ecological Effects and the Behavioral Responses lishment of mussel beds on artificial of Benthic Macrofauna. R. J. Diaz and R. Rosenberg in Oceanography and Marine Biology: An Annual Review, Vol. 33, pages 245–303; 1995. reefs has been employed to improve wa- National Estuarine Eutrophication Assessment: Effects of Nutrient Enrichment in the Nation’s ter quality. But bacterial decomposition Estuaries. S. B. Bricker, C. G. Clement, D. E. Pirhalla, S. P. Orlando and D.R.G. Farrow. NOAA, National of mussel excreta and dead individuals Ocean Service, Special Projects Office and the National Centers for Coastal Ocean Science, 1999. consumes large amounts of oxygen, Nutrient-Enhanced Productivity in the Northern Gulf of Mexico: Past, Present and Future. which can result in boom-and-bust cy- N. N. Rabelais, R. E. Turner, Q. Dortch, D. Justic, V. J. Bierman and W. J. Wiseman in Hydrobiologia, cles in locations where water mixing Vol. 475, No. 6, pages 39–63; 2002. is poor and oxygen replenishment is lim- Ecosystems and Human Well-Being: Current State and Trends. Millennium Ecosystem Assessment. Island Press, 2005. Available online from www.millenniumassessment.org/ ited. In these cases, thriving mussel com- en/products.global.overview.aspx munities suddenly collapse, leaving a Restoring the Black Sea in Times of Uncertainty. L. D. Mee, J. Friedrich and M. T. Gomoiu in

JEN CHRISTIANSEN dead zone until the organic material has Oceanography, Vol. 18, pages 32–43; 2005.

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