Upwelling zones, which receive infusions of nutrients from deep ocean waters, support some of the most productive marine ecosystems. However, anthropogenic eutrophication of estuaries and coastal zones has been a growing problem since the latter half of the twentieth century. The main drivers for this have been the increasing proportion of the population moving to the coastal zones, an increase in the burning of fossil fuels, the increase in the use of synthetic fertilizers and the increase in consumption of animal protein, due to the intensive rearing of poultry and pork. Other contributing factors have been the draining of wetlands and the clearing of riparian vegetation. The result of these human activities has been a very large increase of the inputs of certain plant nutrients, particularly nitrogen and phosphorus, into aquatic ecosystems. Whereas phosphorus is often the limiting nutrient in freshwater systems, nitrogen is most often the naturally limiting nutrient in estuarine and coastal systems. Within the estuarine to coastal continuum, multiple nutrient limitations occur among nitrogen, phosphorus, and silica along the salinity gradient and by season.
Nutrients are essential for the algal production that supports food webs. However, there are thresholds where the load of nutrients to estuarine, coastal, and marine systems exceeds the capacity for assimilation of nutrient-enhanced production, and water-quality degradation occurs. An imbalance of N and P in combination with silica leads to shifts in phytoplankton community composition. Impacts can include noxious and toxic algal blooms, increased turbidity with a subsequent loss of submerged aquatic vegetation, oxygen deficiency, disruption of ecosystem functioning, loss of habitat, loss of biodiversity, shifts in food webs, and loss of harvestable fisheries.
Rivers play a crucial role in the delivery of nutrients to the ocean. In the subbasins to the North Atlantic Ocean, specifically in the Baltic catchments, and in the watershed of the Mississippi River, inputs of anthropogenic nitrogen via rivers far exceed other sources of nitrogen input - atmospheric deposition, coastal point sources, and nitrogen fixation. Phosphorus loads, likewise, come mostly from rivers. Direct atmospheric deposition of nitrogen and phosphorus on estuaries and coastal waters may contribute as little as 1% to as much as 30-40% of the total load. The relative sources of nitrogen and phosphorus loads to the coastal ocean correspond to the degree of various anthropogenic activities in the watershed.
The susceptibility of estuaries and coastal waters to eutrophication is largely controlled by the physics of these systems such as the geomorphology, the tidal range, the residence time and flushing rates, and the engineering of river mouths or inlets. Partially enclosed systems with restricted exchange, for example, lagoons, fjords and large estuaries, such as the Chesapeake Bay, are particularly vulnerable. This is also the case for inland seas, such as the Baltic, the Black, and the Adriatic. Some of the symptoms of eutrophication in estuaries may be partially alleviated by ecological engineering measures such as building of treatment ponds, dredging, creating man-made mouths, and wetland restoration and creation.
Several indices are under development or being tested for the evaluation of eutrophication by ecological engineers. They are important management tools and, combined with scenarios of different future outlooks, may be used as future prediction tools. A widely used screening model is the USA National Estuarine Eutrophication Assessment that has been updated into the ASSETS model. It has been applied in most of the USA estuaries, and several European and Chinese systems. Another screening model in widespread use in Europe is the OSPAR Comprehensive Procedure.
Some options for the effective control of point sources of nutrients are available to ecological engineers. These include the construction of urban wastewater treatment plants or the upgrading of existing plants to tertiary treatment. However, the outlook is much bleaker for the control of diffuse sources such as agricultural runoff and atmospheric deposition. The harmonization of presently conflicting policies such as agricultural subsidies (that encourage the excessive use of fertilizers) and environmental policies such as the Clean Water Act (USA) and the Water Framework Directive (EU) may in future help resolve some of these issues. Certainly, changes in the socioeconomic situation of countries and regions can have an effect on eutrophication. The collapse ofcollective farming practices after the breakup of the Soviet Union was one example of how a change in agriculture can relieve the pressures on coastal ecosystems, in this case the Black Sea. However, changes in life styles in European countries as a result of admission to the European Union have resulted in an increase in the per capita consumption of animal protein, and this has increased the nitrogen input into the aquatic systems. Similar increases in animal protein consumption are presently occurring throughout Southeast Asia as a result of booming economies.
Aquaculture is another human activity that can both be affected by eutrophication and can also impact eutrophi-cation. The deterioration of water quality resulting from eutrophication can have serious repercussions on the aquaculture industry. However, the excessive feeding of fish in cage aquaculture can also contribute to the increase in nitrogen inputs into aquatic ecosystems. Conversely, the culture of filter feeding bivalves may significantly graze algal blooms resulting from the over stimulation of phytoplankton production. An apparently contradictory situation of high nitrogen-low chlorophyll may develop in such cases. Conversely, the destruction by over-harvesting of natural filter bivalve beds may favor eutrophication. Such is the case of the Chesapeake Bay where the loss of the oyster grounds probably contributed to the vulnerability of this large estuary to eutrophication.
Poly-culture practices in Chinese bays effectively use macro-algae to mop up some of the excessive nutrients as well as bivalves and abalone as grazers. These can help control the effects of eutrophication, although the aquacultures are still vulnerable to the occurrence of harmful algal blooms.
A common manifestation of eutrophication is hypoxia (dissolved oxygen concentration DO <2m gT1) and anoxia (DO = 0), that is, the depletion of dissolved oxygen in coastal waters, leading to 'dead zones'. When the DO is less than a critical value (typically 2 mg l_ ), mobile animals such as demersal fish, crabs, and shrimp migrate away from the area. Resident animals die when the DO < 1mgl-1. Fisheries have collapsed, notably in the Baltic and Black seas.
Hypoxia occurs naturally in many parts of the world's marine environments, such as fjords, deep basins, open ocean oxygen minimum zones, and oxygen minimum zones associated with upwelling systems. Hypoxic and anoxic waters have existed throughout geologic time, but their occurrence in shallow coastal and estuarine areas is increasing. The severity of hypoxia (either duration, intensity, or size) has increased where hypoxia occurred historically, and hypoxia exists now when it did not occur before. The severity of hypoxia increased in the northern Gulf of Mexico, primarily since the 1960s. Evidence comes from paleo-indicators in accumulated sediments, long-term hydrographic data, and scenarios based on empirical models. The size and frequency of hypoxia in the Gulf of Mexico have increased as the flux of nitrate increased, and there is a direct correlation between nitrate flux to the Gulf of Mexico from the Mississippi River and the mid-summer size of the hypoxic zone.
Aerobic bacteria consume oxygen during decomposition of the excess carbon that sinks from the upper water column to the seabed. There will be a net loss of oxygen in the lower water column, if the consumption rate is faster than the diffusion of oxygen from surface waters to bottom waters. Hypoxia is more likely when stratification of the water column occurs and will persist as long as oxygen consumption rates exceed those of resupply.
Some of the largest hypoxic zones are in the coastal areas of the Baltic Sea, the northern Gulf of Mexico, and the northwestern shelf of the Black Sea (reaching 84 000 km2, 22 000 km2, and 40 000 km2 (until recently), respectively). Hypoxia existed on the northwestern Black Sea shelf historically, but anoxic events became more frequent and widespread in the 1970s and 1980s reaching over areas of the seafloor up to 40 000 km2 in depths of 8-40 m. Recent reductions in nutrient loads to the northwestern Black Sea resulted in a minimization of the hypoxic zone there. There is also evidence that the sub-oxic zone of the open Black Sea enlarged toward the surface by about 10 m since 1970. Similar declines in bottom-water-dissolved oxygen have occurred elsewhere as a result of increasing nutrient loads and anthropogenic eutrophication, for example, the northern Adriatic Sea, the Kattegat and Skaggerak, Chesapeake Bay, the German Bight and the North Sea, and Long Island Sound. The number of estuaries with hypoxia or anoxia continues to rise.
The obvious effects of hypoxia/anoxia include the displacement of pelagic organisms and selective loss of demersal and benthic organisms. These impacts may be aperiodic if recovery occurs, may occur on a seasonal basis with differing rates of recovery, or may be permanent so that there is a long-term shift in ecosystem structure and function. As the oxygen concentration falls from saturated or optimal levels toward depletion, a variety ofbehavioral and physiological impairments affect the animals that reside in the water column or in the sediments or attached to hard substrates. Hypoxia also affects optimal growth rates and reproductive capacity. Mobile animals, such as shrimp, fish, and some crabs, flee waters where the oxygen concentration falls below 2-3 mgl-1. Movements of animals onshore can result in 'jubilees' where stunned fish and shrimp are easily captured, or result in massive fish kills. As dissolved oxygen concentrations continue to fall, less mobile organisms become stressed and move up out of the sediments, attempting to leave the seabed. As oxygen levels fall from 0.5 mgl~ toward 0, there is a fairly linear decrease in benthic infaunal diversity, abundance, and biomass.
Entire taxa may be lost in severely stressed seasonal hypoxic/anoxic zones. Larger, longer-lived burrowing infauna are replaced by short-lived, smaller surface deposit-feeding polychaetes, and certain typical marine invertebrates are absent from the fauna, for example, pericaridean crustaceans, bivalves, gastropods, and ophiuroids. Increasing oxygen stress for the Skagerrak coast of western Sweden in semienclosed fjordic areas resulted in declines in the abundance and biomass of macroinfauna, particularly mollusks, suspension feeders, and carnivores. These changes in benthic communities result in an impoverished diet for bottom-feeding fish and crustaceans.
Cultural and natural eutrophication have both contributed to changes in nutrient input to coastal waters, and led to an overall increase in nutrient availability and an alteration in nutrient composition. The first result of these changes is often an increase of total algal biomass and shifts in species composition potentially leading to secondary disturbance such as harmful algal blooms (HABs). HAB species range from marine, brackish to freshwater organisms and cover a broad range of phylo-genetic types (dinoflagellates, diatoms, raphidophytes, cyanobacteria). Most HAB species form massive blooms of various colors (red, brown, or green). A few species can produce potent toxins. These toxins can directly kill marine mammals and transfer through the food chain causing harm at different levels from plankton to humans. A potential impact of HABs on human health occurs through the consumption of shellfish that have filtered toxic phytoplankton from the water or planktivorous fish. All poisoning syndromes are serious and can be fatal. They are named paralytic (PSP), diarrhetic (DSP), neurotoxic (NSP), azapiracid (AZP), and amnesic shellfish poisoning (ASP). All syndromes, except for ASP, are caused by dinoflagellates. ASP is caused by diatoms, a group of phytoplankton usually thought to be nontoxic. In tropical and subtropical zones, another human poisoning syndrome, ciguatera fish poisoning (CFP), is caused by toxic dinoflagellates that grow on substrate in coral reef communities. CFP toxins are transferred from herbivorous to carnivorous fish that are commercially valuable. Some algal toxins, brevetoxins, are airborne in sea-spray, causing respiratory distress in coastal population, for example, in the Gulf of Mexico. Cyanobacteria (blue-green algae) naturally bloom in still inland waters, estuaries, and the sea during summer. Some cyanobacteria produce potent cyanotoxins (anatoxins, microcystins, and nodularin), which are dangerous and sometimes fatal to livestock, wildlife, marine animals, and humans. These toxins represent a serious health risk in water bodies used for recreational and/or as freshwater supply reservoirs.
Although references to HABs date back to biblical times, the number of toxic events and subsequent economic losses linked to HABs has increased considerably in recent years around the world. Many reports point out an obvious link between pollution and HABs, but there are also other reasons for the expansion of the HAB problem.
Numerous new bloom events have been discovered because of increased awareness and improved detection methodologies (e.g., molecular probes for cell recognition, PCR probes for rDNA specific to genera or species of HABs, enzyme-linked immunosorbent assays (ELISA), remote sensing data from satellites, qualified observers, and efficient monitoring programs). The global increase of aquaculture activities and trade of exotic species has led to improved safety and quality controls that revealed the presence of HAB species and/or toxins in, for example, aquaculture pens, and contaminated seafood. Mortality events and toxicity outbreaks in fish or bivalves resources can no longer go unnoticed. Transport of toxic species in ship ballast water undeniably contributes to the increasingly damaging effect of HABs on fisheries, aquaculture, human health, tourism, and the marine and brackish environment. UNEP has recently ranked HABs among the ten worst threats of invasive species transported in ballast water.
Dispersal ofHABs is influenced by oceanic and estuar-ine circulation, river flow combined with currents, upwelling, salinity, nutrients, and specific life-cycles of various HAB species. The apparent increase in toxic diatoms (Pseudo-nitzschia spp.) off the US and Canada coast is often coupled to physical forcing (storm, wind, rain, and upwelling) and more rarely to the increase in nitrate-N in rivers, for example, from the Mississippi River. Both nutrients and harmful dinoflagellate taxa are introduced from upwelling/downwelling areas to estuaries, coastal bays, or lagoons, for example, the Atlantic coast of France, Spain, and Portugal, Chesapeake Bay, and the Benguela region. Similar processes are observed for cyanobacteria in the Gulf of Finland. Physical convergence, advection, or accumulation process of oceanic dinoflagellates (Dinophysis, Karenia, and Gymnodinium) in embayments also contribute to the extension of HABs in some areas. Large oceanic current systems transport the N-fixing cyanobacterium Trichodesmium from tropical oli-gotrophic regions to W. Florida waters, enriched with Saharian iron dust, where it blooms. Some HABs have specific life cycles including resting stages for diatoms (spores), dinoflagellates (cysts), and cyanobacteria (akinetes). These resting stages provide these algae with a competitive advantage over populations that cannot survive in poor conditions.
Climatic and hydrological changes affect nutrient delivery and processing, for example, the input of micro-nutrients and freshwater from rainfall and river flow, flooding after hurricanes, and tropical storms also favor HAB's growth and persistence. Certain PSP and CFP producers (dinoflagellates) have increased significantly under large-scale changing climatic conditions in temperate environments (Kattegat, NW Spain, and SW Portugal) and in the Indo-Pacific, respectively. Some of these blooms have been linked to the North Atlantic oscillations (NAO) and to El-Nino events that affect local climate in wind-driven upwelling systems.
Despite the importance of natural events in algal bloom formation, many examples relate HABs to anthropogenic activities since World War II. Red tides (dinoflagellates) in Asia, for example, the mouth of the Yangtze Estuary in China and the Seto Inland Sea in Japan, are related to the parallel increasing population density and nitrogen (N) and (P) loadings. Nutrient-enriched conditions in brackish coastal bays and estuaries have been correlated with high abundance of diatoms (central California, Louisiana in the US), dinoflagellates (off the coast of North Carolina - US, Northern Adriatic, Aegean, and Black seas), and haloto-lerant cyanobacteria (Baltic Sea, Brazil, Australia), but the direct cause of this relationship is not fully understood. In tropical regions, eutrophication of reef communities often leads to the overgrowth of macroalgae on corals and high coral mortality that favor the bloom of benthic dinoflagellates (CFP producers). Both elevated N and P concentrations and silicon limitation can favor the dominance of HABs, for example, the haptophyte Phaeocystis in the North Sea. Declining silica input to coastal zones and estuaries is often due to damming of rivers and gives a competitive advantage to marine haptophytes and dinoflagellates over diatoms. The residence time of the water in freshwater systems is increased by the construction of the dams. This allows for the development of freshwater diatom blooms. The silicon-rich frustules of the diatoms are not remineralized as rapidly as organic matter and so dams effectively retain silicon upstream. The ratio of silicon to nitrogen therefore decreases, and estuarine and coastal diatoms may have insufficient silicon to reproduce. The communities of phytoplankton organisms may therefore shift so that diatoms are replaced by nonsilicon requiring organisms such as dinoflagellates and this may significantly alter the food web.
Many potable water reservoirs are under the pressure of expanding population, and are negatively impacted by both sediment erosion, reduced water flow and elevated N and P loading that will stimulate noxious cyanobacter-ial blooms. Similar trends are reported for river systems with weir pools. Many HABs have characteristic modes of nutrition from autotrophy to heterotrophy, that is, can use organic carbon, nitrogen, and phosphorus (mixotrophy and osmotrophy). Recent studies have shown that the increase in organic nutrients could benefit certain HABs (dinoflagellates and prymnesiophytes). The global nitrogen-based fertilizer usage has shifted toward urea-based products and is expected to continue. Thus, significant amounts of urea are transported to estuarine and coastal waters with the potential for increasing eutrophication of these sensitive areas. Since urea is also one very important nitrogen substrate for some HAB species, the global increase of PSP outbreaks is comparable to the increase of urea use for 1975-2005. Aquaculture sites are also a large source of nutrient from animal excreta, rich in N and P, to coastal sediment. Their contribution to HAB formation will depend on the hydrology of the system, for example, HABs proliferate in calm areas.
Among the natural marine environmental contaminants that are health risks, HABs are most prominent. However, the relative effects of natural versus anthropogenic factors on harmful algal blooms cannot yet be resolved.
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