Eutrophication of Lakes and Rivers

Peter JA Kleinman, US Department of Agriculture, University Park, Pennsylvania, USA Andrew N Sharpley, US Department of Agriculture, University Park, Pennsylvania, USA
Eutrophication is the process of increasing organic enrichment of a water body. The accelerated eutrophication of lakes and rivers represents one of the most pervasive water quality problems in the world.

Introductory article
Article Contents
. Introduction . Elements That Are the Prime Causes of Eutrophication . Primary Sources of Phosphorus and Nitrogen That Contribute to Accelerated Eutrophication of Lakes and Rivers . Public Health Implications of Eutrophication . Ecological Effects of Eutrophication on Aquatic Species . What Has Been Done to Reduce Eutrophication?

Introduction
Eutrophication of lakes and rivers generally results from augmented primary production of phytoplankton, especially algae and cyanobacteria. Blooms of these organisms may aect ecological and human health, impairing the use of lakes and rivers (Table 1). While eutrophication occurs naturally, over the course of centuries, human activities sometimes accelerate eutrophication to a time frame of decades (Figure 1). The accelerated eutrophication of lakes and rivers represents one of the most pervasive water quality problems in the world.

Elements That Are the Prime Causes of Eutrophication

As eutrophication is a process of organic enrichment, the elements that are the prime cause of eutrophication are those required for life: carbon, nitrogen and phosphorus. In 1958, Albert Redeld observed that the ratio of carbon, nitrogen and phosphorus in marine phytoplankton was fairly constant under conditions favourable to growth, 106 carbon : 16 nitrogen : 1 phosphorus. Despite ndings that this ratio can vary considerably, the Redeld ratio has
Table 1 Adverse eects of eutrophication on lakes and rivers (modied from Smith, 1998) Increased biomass of phytoplankton Shift in phytoplankton to bloom-forming species that may be toxic or inedible Increased biomass of benthic and epiphytic algae Change in macrophyte species composition and biomass Decrease in water transparency Taste, odour, and water treatment problems Oxygen depletion Increased incidence of sh kills Loss of desirable sh species Reduction in harvestable sh and shellsh Decrease in aesthetic value of water body

been used to explain the relative importance of these three nutrients to eutrophication. Namely, the proportions of nutrients that are available to phytoplankton dictate their role in limiting primary productivity and hence eutrophication. Because the biogeochemical cycles of carbon and nitrogen include signicant gaseous phases (e.g. CO2 and N2), these elements can be accessed from the atmosphere by freshwater organisms capable of photosynthesis and nitrogen xation (e.g. cyanobacteria). The biogeochemical cycle of phosphorus, however, does not include a signicant gaseous component. Consequently, phosphorus is primarily derived from terrestrial sources. Given the insoluble nature of many terrestrial phosphorus compounds, phosphorus is typically found in very low concentrations in freshwater systems. While phosphorus generally limits the primary productivity of freshwater lakes and rivers, nitrogen constrains aquatic productivity in brackish and saline waters. A variety of studies have conrmed the important role of phosphorus in controlling eutrophication of lakes. For instance, whole lake experiments were undertaken in Ontario, Canada, where experimental lakes were fertilized with combinations of carbon, nitrogen and phosphorus. Addition of phosphorus alone was sucient to increase algal production, as phytoplankton were able to access carbon and nitrogen from the atmosphere because blooms of nitrogen-xing cyanobacteria were stimulated. Primary productivity did not substantially change in lakes that were fertilized with carbon and nitrogen alone (no phosphorus). The susceptibility of rivers to eutrophication diers from lakes, typically due to greater ow, which causes nutrient transport rather than settlement. Only a small fraction of phosphorus transported through rivers, 14%, is captured by organisms and processed into biomass. However, in slow moving or periodically impounded rivers, factors aecting eutrophication approach those of lakes. Although less experimental research has been conducted on the eutrophication of rivers relative to lakes, studies point to phosphorus as the major control
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Eutrophication of Lakes and Rivers

Natural process

Accelerated by land use

Centuries

Figure 1 Effect of land use on accelerated eutrophication.

of primary productivity in rivers susceptible to eutrophication.

Important forms of phosphorus

The chemistry of phosphorus aects its availability to phytoplankton, and hence its potential role in eutrophication. Dissolved inorganic phosphorus, such 2 ), is the only form of as orthophosphate (H2PO4 phosphorus universally available to vascular plants and phytoplankton alike, and is therefore of key concern to eutrophication. In some cases, the biological consumption rate of orthophosphate in surface waters is as rapid as a few minutes. In the laboratory, concentrations of orthophosphate as low as 0.003 to 0.8 mg L 2 1 (parts per billion) are sucient to sustain growth of a variety of phytoplankton. Other forms of phosphorus are much less accessible to phytoplankton, but represent much larger fractions of phosphorus in lakes and rivers. Solid phases of phosphorus, such as phosphorus associated with sediments or incorporated in organic matter, cannot be metabolized readily by phytoplankton. They require dissolution, desorption, or organic matter decomposi2

tion to become available to phytoplankton. Much phosphorus is transferred to sediments at the bottoms of lakes following the death and deposition of phytoplankton. Release of phosphorus from these sediments containing deposits can serve as a signicant storage source of dissolved inorganic phosphorus long after other input sources have been controlled.

Important forms of nitrogen

Major forms of nitrogen that are important to eutrophication include nitrogen in gas and solution phases. Gas phases of nitrogen, such as elemental nitrogen (N2), nitrous oxide (NOx) and ammonia (NH3) may all contribute to river and lake nitrogen levels through biological xation as 2 ) is generally well as wet and dry deposition. Nitrate (NO3 the dominant form of dissolved nitrogen in lakes and rivers, and is readily available to phytoplankton. Organic forms of dissolved nitrogen, such as urea, require hydrolysis to ammonium (NH4) to become available to phytoplankton. In reducing aquatic environments, characterized by little or no oxygen (O2), nitrate can be reduced to some of the gas phases listed above (N2, NOx).

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Decades

Eutrophication of Lakes and Rivers

Primary Sources of Phosphorus and Nitrogen That Contribute to Accelerated Eutrophication of Lakes and Rivers
The sources of phosphorus and nitrogen to lakes and rivers consist of point sources, such as discharges from factories and sewage treatment plants, and nonpoint sources, such as suburban lawns and agricultural lands. On a practical basis, point sources are readily identied and measured, while nonpoint sources are diuse and dicult to identify and measure.

Point sources
In North America and Europe, point sources of nutrient pollution to lakes and rivers has declined steadily, owing to improvements in processing euents from factories and wastewater treatment plants, as well as reducing nutrient inputs to these facilities. For instance, sewage treatment plants now regularly precipitate phosphorus with amendments of iron and aluminium to reduce soluble P content of treated waste water. Before the 1972 Clean Water Act, most laundry detergents in the United States contained from 35% to 75% sodium triphosphate (Na5P3O10). These detergents served as the major source of phosphorus in household waste water. Today, phosphate substitutes are used in detergents and phosphorus contributions to waste water have been greatly diminished.

both solution and solid phases of phosphorus. However, as soluble phosphorus is built up in soils, runo and sometimes leaching serve as increasingly important pathways of phosphorus transport to lakes and rivers. Nitrogen loss from agricultural lands may be attributed to leaching of soluble nitrogen (especially nitrate) and atmospheric losses of nitrogen gases following denitrication and ammonia volatilization. The problem of soil phosphorus build-up is particularly acute in areas with intensive livestock agriculture. Livestock production has intensied due to increased demand for animal products as well as improved protability related to the economics of high animal density operations. Given the specialization of modern agriculture, feed and livestock production are generally conducted separately, resulting in major transfers of nutrients from grainproducing areas to the grain-consuming animal production areas. On average, only 30% of the fertilizer and feed phosphorus imported into intensive livestock operations leaves in crops and livestock produce. Most of these nutrients are applied to soils, resulting in a build-up of soil test P above crop yield requirements and in a P-enriched surface runo. A study conducted by the US Environmental Protection Agency in 1996 found that agriculture is the primary source of nutrients in most US lakes and rivers that are undergoing eutrophication.

Urban runoff
Urban runo represents another major contributor of phosphorus and nitrogen to lakes and rivers. Water from municipal storm drains, golf courses, household lawns and septic systems has been implicated as primary sources of dissolved phosphorus and particulate phosphorus. Because erosion from construction sites can be extremely high, occurring at annual rates of 50 000 tonnes per square kilometre compared with 1000 to 4000 tonnes per square kilometre for agricultural lands, construction areas can be an important source of solid phase (particulate) phosphorus.

Nonpoint sources
Despite great strides in point source control, the nutrient enrichment of many lakes and rivers has not diminished. In North America and Europe, nonpoint sources are now responsible for the majority of phosphorus and nitrogen entering lakes and rivers. In most cases, nonpoint source inputs have not decreased while point source inputs have steadily declined. As a result, more attention is now directed toward nonpoint sources of phosphorus and nitrogen to lakes and rivers. Given the diuse nature of nonpoint source pollution, control requires an integrated approach that addresses both source (availability of phosphorus and nitrogen) and transport factors.

Atmospheric deposition
Atmospheric deposition of nitrogen can be quite substantial, especially in areas prone to acid rain. Worldwide, combustion of fossil fuels is responsible for the annual release of approximately 20 million tonnes of nitrogen to the atmosphere. Atmospheric deposition is the primary source of nitrogen to surface waters in eastern Europe. Because airsheds are much larger and less easily delineated than watersheds, sources of atmospheric nitrogen inputs to lakes and rivers are even more dicult to dene. As a result, measures to reduce atmospheric inputs will be more dicult and contentious than water inputs.
3

Agriculture
Agriculture is a major source of phosphorus and nitrogen to lakes and rivers. Worldwide, more nutrients are added to agricultural soils as inorganic and organic fertilizers than are removed as produce. As these nutrients build up in soil, they are increasingly prone to removal by water and wind. Phosphorus loss from agricultural lands has traditionally been associated with erosion, which removes

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Eutrophication of Lakes and Rivers

Public Health Implications of Eutrophication

The elements that induce eutrophication dier in their direct eects on public health. While phosphorus in water is not considered directly toxic to humans, nitrogen pollution can have a direct eect on public health. Nitrate is a water quality concern because it has been linked to methaemoglobinaemia in infants, to toxicities in animals, and to increased eutrophication in both fresh and saline (e.g. estuaries) waters. The US Environmental Protection Agency has established a maximum contaminant level for nitrate-N in drinking water of 10 mg L 2 1 to protect babies under 36 months of age. This segment of the population is most sensitive because bacteria that live in an infants digestive tract can reduce nitrate to nitrite, thereby causing haemoglobin to transform into methaemoglobin which interferes with the oxygen-carrying ability of blood. Eutrophication aects public health in a variety of fashions. Eutrophic waters often develop foul tastes and putrid smells, and can even become toxic due to harmful algal blooms and algal byproducts such as from cyanobacteria. Such waters may be unt for swimming or consumption. Treatment of eutrophic drinking water presents serious long-term health risks as required chlorination of eutrophic water may produce carcinogenic byproducts such as trihalomethanes.

High

Medium

Biodiversity Dissolved oxygen Primary production P-input flux

Low

Oligotrophic

Mesotrophic

Eutrophic

Figure 2 Conceptualization of freshwater eutrophication (adapted from Correll, 1998).

Ecological Effects of Eutrophication on Aquatic Species

Table 1 and Figure 2 illustrate the eects of eutrophication on aquatic ecosystems, charting the corresponding changes in trophic status, biological oxygen demand (BOD) and species diversity. As primary productivity increases, the decomposition of dead phytoplankton increases BOD, depleting oxygen in the water. In oligotrophic freshwater bodies, even small increases in BOD can make streams uninhabitable to certain sh, such as salmonids. In severe cases anoxia may be induced, such as following blooms of phytoplankton. Accelerated eutrophication of lakes can increase the population of rough sh compared to desirable game sh. This has a negative impact on the value of other recreational aspects of lakes. However, shery managers often recommend a higher productivity to maintain an adequate phytoplanktonzooplanktonsh food chain for optimum commercial sh production. This food chain may be manipulated by stocking of water with certain sh species in addition to P load reductions, in eorts to reduce the incidence of algal blooms and improve overall water quality. For example, stocking lakes with predatory game sh at the top of the food chain (piscivore sh bass, pike,

trout) can reduce the number of planktivore or coarser sh (yellow perch, crappies), on which they feed. Similar results may be obtained by selectively shing planktivores. Zooplankton should then thrive, which in turn will reduce phytoplankton populations, improving water quality. Lake and river use has an impact on choosing water quality goals, which will require diering management. Watershed management often becomes more complex with multiple-use lakes and rivers. For example, a reservoir may have been built primarily for water supply, hydropower and/or ood control with recreation as a side benet, and aesthetic enhancement (including property value) a fringe benet. The US Environmental Protection Agency has developed rapid bioassessment protocols to detect impairments to aquatic life and for assessing their relative severity. Once an impairment is detected, additional chemical and biological tests are needed to identify the causative agent, its source, and to implement appropriate remedial strategies. The protocols have been recently updated to provide more cost-eective and scientically valid approaches. They now focus on an analysis of periphyton, benthic macroinvertebrates, and sh assemblages.

What Has Been Done to Reduce Eutrophication?

Unless current practices are altered, nonpoint source pollution of lakes and rivers will continue. Eutrophication requires a decrease in phosphorus and nitrogen inputs to lakes and rivers. Because phosphorus can continue to be released from sediments years after phosphorus inputs have been stopped, control of nutrient inputs may have to be paired with limnological management methods if eutrophication is to be slowed.

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Eutrophication of Lakes and Rivers

Water quality standards for lakes and rivers

Water quality standards can serve as triggers to require actions to slow or mitigate eutrophication, as well as yardsticks to assess the relative impairment of a lake or river. Early work by Sawyer in 1947 and Vollenweider in 1968 identied critical dissolved P and total P concentrations of 0.01 and 0.02 mg L 2 1, respectively. In the Netherlands, a groundwater standard for dissolved P of 0.1 mg L 2 1 has been set to protect against eutrophication of receiving surface water bodies. In the US, states are required to set their own water quality criteria, but so far only 22 states have quantitative standards and only Florida has adopted the federal USEPA levels. These standards include designated water uses, water quality criteria to protect these uses, and an antidegradation policy. Where water quality standards are not attained, even where best management practices have been implemented, response actions are dened through the Total Maximum Daily Load process of the 1998 Clean Water Action Plan. This process not only addresses pollutant concentrations in stream and rivers, but also considers system discharge and thereby the total pollutant load, as well as the designated use and potential impact on the receiving water body. An ecosystem approach is being used to develop water quality criteria in the US as well as to estimate the response of waters to increased nutrient loadings. Inherent dierences exist in the geography and biology of dierent agricultural regions, forests, wetlands and water bodies. As water bodies reect the lands they drain, an ecosystem framework that describes similar patterns of naturally occurring biotic assemblages, such as land-surface form, soil, existing natural vegetation, and land use was proposed by Omernik in 1987 and later rened by USEPA in 1996. The ecosystem concept provides a geographic framework for eciently managing aquatic ecosystems and their components. For example, studies in the US have shown that the distribution of sh communities approximate ecosystem boundaries as dened a priori by Omernik in 1987. This, in turn, implies that similar water quality standards, criteria and monitoring strategies are likely to be valid within a given ecosystem.

importance of nonpoint source pollution to eutrophication has prompted regulatory action against a variety of nonpoint sources. In The Netherlands, application of phosphorus in manure or mineral fertilizer is regulated based upon a soils phosphorus saturation, a measure of soil phosphorus that relates the amount of extractable phos-phorus in the soil to the soils ability to bind phosphorus. There, a critical soil P saturation level of 25% has been identied. In the USA, a phosphorus site assessment index has been developed to assist farmers in better manag-ing phosphorus. This index incorporates a variety of source factors (soil P, mineral fertilizer management and manure management) and transport factors (erosion potential, susceptibility to runo, leaching potential) to assess the potential of phosphorus loss from specic agricul-tural elds. Sharpley in 1995 found that the index was strongly correlated with phosphorus losses in runo.

Remediation of eutrophic lakes and rivers

A variety of methods exist to reduce the impacts of eutrophication on lakes and rivers. These include the use of chemicals (e.g. aluminium sulfate and sodium aluminate) to inactivate P recycling by stable precipitates, use of algicides (e.g. copper sulfate), biomanipulation, and biomass harvesting. A growing body of evidence suggests that treatment of waters with straw, particularly barley straw, may prevent blooms of phytoplankton, due to the production of certain phytotoxic compounds. These methods represent proximate responses to an existing problem of eutrophication. A sound fundamental understanding of the processes that cause eutrophication exists and at regional and global scales, the causes and consequences of point and nonpoint sources of nutrients are clear. However, we have not always been successful at translating basic research information on the eect of land use on soil and water resources to the implementation of management programmes that are both eective and practical to land managers. Thus, we must conduct interdisciplinary research involving soil scientists, hydrologists, agronomists, limnologists, animal scientists and policy specialists. We must also include the stakeholders when planning this research. Development of guidelines to implement such programmes will also require consideration of the socioeconomic and political impacts of any management changes on both rural and urban communities, and of the mechanisms by which change can be achieved in a diverse and dispersed community of land users.

Point and nonpoint source control of phosphorus and nitrogen

The improvements in point source control of phosphorus and nitrogen may be traced to emission standards. For instance, a maximum dissolved phosphorus concentration of 1.0 mg L 2 1 is identied for euent from sewage treatment plants in the USA. While regulatory controls of nonpoint source nutrient pollution remain limited, increasing awareness of the

Further Reading
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Eutrophication of Lakes and Rivers

Andersson G, Berggren H, Cronberg G and Gelin C (1978) Eect of planktivorous and benthivorous sh on organisms and water chemistry in eutrophic lakes. Hydrobiologia 59: 915. Barbour MT, Gerritsen J, Snyder BD and Stibling JB (1997) Revision to Rapid Bioassessment Protocols for Use in Streams and Rivers: Periphyton, Benthic Macroinvertebrates, and Fish. USEPA 841-D97-002. Government Printing Oce, Washington DC. Breeuwsma A and Silva S (1992) Phosphorus Fertilization and Environmental Eects in The Netherlands and the Po Region (Italy). Rep. 57 Agric. Res. Dep., Winand Staring Centre for Integrated Land, Soil and Water Research, Wageningen. Carpenter SR, Caraco NF, Correll DL et al. (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8: 559568. Cooke DG, Welch EB, Peterson SA and Newroth PR (1993) Restoration and Management of Lakes and Reservoirs, 2nd edn. Boca Raton, FL: Lewis Publishers, CRC Press. Correll DL (1998) The role of phosphorus in the eutrophication of receiving waters: a review. Journal of Environmental Quality 27: 261 266. Grover JP (1989) Phosphorus-dependent growth kinetics of 11 species of freshwater algae. Limnology and Oceanography 34: 341348. Howarth RW, Billen G, Swaney D et al. (1996) Regional N budgets and riverine N & P uxes for the drainages to the North Atlantic Ocean: natural and human inuences. Biogeochemistry 35: 75139. Hughes RM (1985) Use of watershed characteristics to select control streams for estimating eects of metal mining wastes on extensively disturbed streams. Environmental Management 9: 253262. Hughes RM and Larsen DP (1988) Ecoregions: An approach to surface water protection. Journal of the Water Pollution Control Federation 60: 486493. Hughes RM, Larsen DP and Omernik JM (1986) Regional reference sites: a method for assessing stream potentials. Environmental Management 10: 629635. Jaworski NA, Howarth RW and Hetling LJ (1997) Atmospheric deposition of N oxides onto the landscape contributes to coastal eutrophication in the northeast United States. Environmental Science and Technology 31: 19952004. Karr JR, Fore LS and Chu EW (1997) Making Biological Monitoring More Eective: Integrating Biological Sampling with Analysis and Interpretation. Washington DC: Oce of Policy, Planning, and Evaluation, US Environmental Protection Agency. Kotak BG, Keneck SL, Fritz DL et al. (1993) Occurrence and toxicological evaluation of cyanobacterial toxins in Alberta lakes and farm dugouts. Water Research 27: 495506. Lawton LA and Codd GA (1991) Cyanobacterial (blue green algae) toxins and their signicance in UK and European waters. Journal of the Institute of Water Environmental Management 5: 60465. Lemunyon JL and Gilbert RG (1993) Concept and need for a phosphorus assessment tool. Journal of Production Agriculture 6: 483486. Maki AW, Porcella DB and Wendt RH (1983) The impact of detergent phosphorus bans on receiving water quality. Water Research 18: 893 903. National Research Council (1990) Restoration of Aquatic Ecosystems. Washington DC: National Academy Press. National Research Council (1993) Soil and Water Quality: An Agenda for Agriculture. Washington, DC: National Academy Press. Newman JR and Barrett PRF (1993) Control of Microcystis aeruginosa in decomposing barley straw. Journal of Aquatic Plant Management 31: 203206. Omernik JM (1987) Ecoregions of the conterminous United States. Annals of the Association of American Geographers 77: 118125.

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