## Eurtrophication Review Articles



# Eutrophication of Freshwater and Coastal Marine Ecosystems
A Global Problem

Val H. Smith

Correspondence address: Dr. Val H. Smith, Department of Ecology and Evolutionary Biology, 1200 Sunnyside Avenue, University of Kansas, Lawrence, KS 66045, USA (vsmith@ku.edu)

DOI: htto://dx.doi.or~10.1065/esor2002.12.142

Abstract Goal, Scope and Background. Humans now strongly influence almost every major aquatic ecosystem,and their activities have dramatically altered the fluxes of growth-limiting nutrients from the landscape to receiving waters. Unfortunately, these nutrient inputs havehad profound negativeeffects upon the quality ofsurface waters worldwide. This review examines how eutrophication influences the biomass and species composition of algae in both fleshwater and costal marine systems. Main Features. An overview of recent advances in algae-related eutrophication researchispresented. Infreshwater systems, a summary ispresented for lakes and reservoirs; streams and rivers; and wetlands. Abriefsummaryisalsopresented forestuarine andcoastal marine ecosystems. Results. Eutrophication causes predictable increases in the biomass of algae in lakes and reservoirs; streams and rivers; wetlands; and coastal marine ecosystems. As in lakes, the response of suspended algae in large rivers to changes in nutrient loading maybehysteretic in somecases. The inhibitory effects ofhigh concentrations ofinorganic suspended solids onalgal growth, whichcanbeveryevident in manyreservoirs receiving high inputs ofsuspended soils,also potentially may occur in turbid rivers. Consistent and predictable eutrophication-caused increases in cyanobacterial dominance of phytoplanktonhavebeenreported worldwide fornatural lakes, and similar trends are reported here both for phytoplankton in turbid reservoirs, and for suspended algae in a large river. Conclusions. A remarkable unity is evident in the global response of algal biomass to nitrogen and phosphorus availability in lakes and reservoirs; wetlands; streams and rivers; and coastal marine waters. The species composition of algal communities inhabiting the water column appears to respond similarly to nutrient loading, whether in lakes, reservoirs, or rivers. As is true offreshwater ecosystems, the recent literature suggests that coastal marine ecosystems will respond positivelyto nutrient loading control efforts. Recommendations and Outlook. Our understanding of freshwater eutrophication and its effectson algal-related water quality isstrong and is advancing rapidly. However, our understanding ofthe effects ofeutrophication onestuarine andcoastal marineecosystemsismuch

more limited, and this gap represents an important future research need. Although coastal systems can be hydrologically complex, the biomass of marine phytoplankton nonetheless appears to respond sensitivelyand predictably to changes in the external supplies ofnitrogenandphosphorus.Theseresponses suggestthat efforts to managenutrient inputs to the seaswillresult in significant improvements incoastal zonewaterquality. Additional newefforts should bemade to develop modelsthat quantitatively link ecosystem-levelresponses to nutrient loading in both freshwater and marine systems. 

### Keywords:Algae;coastalmarineecosystems; estuaries;eutrophication; harmful algalblooms;nitrogen;nutrients;lakes;reservoirs; rivers;phosphorus; phytoplankton; shallow lakes; wetlands Introduction

Humans now strongly influence almost every major aquatic ecosystem, and their activities have dramatically altered the fluxes of growth-limiting nutrients from the landscape to receiving waters. One primary cause has been the rapid intensification of agriculture (Matson et al. 1997). The global production of agricultural fertilizers alone released <10 million metric tonnes of nitrogen in 1950, but may exceed 135 million metric tonnes of N by the year 2030 (Vitousek
et al. 1997). Substantial N is also applied to croplands in the form of animal manures, for which regulatory standards are generally far less stringent than those applied to human sewage (Carpenter et al. 1998a). Similarly, a small but ecologically very significant portion of agriculturallyapplied phosphorus is exported from the land surface to receiving waters (Bennett et al. 2001, Kauppi et al. 

### 1993,Rekolainen et al. 1995, Sims et al. 1998). Atmospheric loading of P to surface waters has also increased (Brunner and Bachofen 1998). In addition, humans use flowing waters as convenient wastewater disposal systems, and the loading of N and P to the world's surface waters is very strongly influenced by human population density and land use (Cole et al. 1993, Caraco 1995). Unfortunately, these nutrient inputs can have profound effects upon the quality of receiving waters (Carpenter et al. 1998a, Correll 1998). Just as fertilizing an agricultural crop
or forest can result in enhanced plant growth, the most common effect of increased N and P supplies to aquatic ecosystems is an increase in the abundance of algae and aquatic plants~ However, the environmental consequences of excessive nutrient enrichment are more serious and far-reaching than nuisance increases in plant growth alone. The degradation of water resources by eutrophication can result in loss of the amenities or services that these aquatic resources provide (Postel and Carpenter 1997). In addition, the eutrophication of both freshwater and coastal marine systems causes a wide array of undesirable symptoms that are either directly or indirectly related to the nuisance growth of aquatic plants (Table 1). Eutrophication accounts for almost one half of the impaired lake area and 60% ofimpaired riverreaches within the United States alone (U.S. EPA 

### 1996a),and eutrophication-related
water quality impairment can have very substantial negative economic effects (Carpenter et al. 1998b, Corrales and Maclean 1995). Eutrophic drinking water supply reservoirs, for example, are much more likelyto have higher treatment costs; greater



## 126 ESPR - Environ Sci & Pollut Res 10 (2) 126 - 139 (2003) 9 ecomed publishers, D-86899 Landsberg, Germany and Ft. Worth/TX, USA ~Tokyo, Japan 9Mumbai, India ~ Seoul, Korea

## Review Articles Eutrophication

Table 1: Adverse effects of freshwater and coastal marine eutrophication

9 increased productivity and biomass of phytoplankton and suspended algae
9 shifts in phytoplankton composi~onto bloom-forming species, many of which may betoxic, orwhich may not be consumed effectively byaquatic grazers
9 increased productivity, biomass, and species composition of attached microalgae (periphyton)
9 increased productivity, biomass, and species composition of marine macroalgae
9 changes in productivity, biomass, and species composition of aquaticvascular plants
9 reducedyields of desirablefinfish and shellfish species
9 reductions in the health and size of marine coral populations
9 threats to endangered aquatic species
9 decreases in water column transparency
9 taste, odor, and filtration problems in drinking water supplies
9 depletion of deep water oxygen
9 decreases in the perceivedaesthetic value of the water body
9 negativeeconomic impacts, including decreased propertyvalues and reduced recreational uses



### difficultiesin meeting standards for disinfectionby-products;

consumercomplaintsdueto objectionabletaste and odor; and healthhazards dueto algaltoxinsinthefinisheddrinkingwater (Cooke and Kennedy2001). Incoastalmarinehabitats,harmfulalgalbloomsmayrender shellfish andfin fishtoxic,orcause massive fish and shrimp kills; bymid-1994, there were 3,164 reported incidents ofhuman poisoning and 148 deaths in the Asia-Pacific region alone (Corrales and Maclean 1995). Economiclosses mayexceed $1 millionU.S. per event, and monitoring efforts may cost up to $50,000 U.S. for each affected

area (Corrales and Maclean 1995).

Because of these problems, there have concerted efforts for several decades by aquatic ecologists and civil engineers worldwide to develop a rational predictive framework to prevent andmanagefreshwatereutrophication (OECD 1982, Cooke et al. 1993). The U.S. EPA has recently published a series ofnutrientcriteriatechnicalguidancemanualsforlakes and reservoirs, rivers and streams, and marine waters (U.S. EPA 2002), and parallel attempts are being made worldwide to evaluate and to predict the responses ofaquatic ecosystems to changes in nutrient loading.
As a result ofglobal effortsto solve the eutrophication problem, we now have a firm mechanistic understanding of the relativeroles ofN andP asgrowth-limitingnutrients;wehave developed models that can predict nutrient concentrations in receiving waters from watershed nutrient inputs and hydrology;and we have developed a series ofmodelsthatthen relate waterbody nutrient concentrations to the critical aspects of water qualitythat are perceived bythe generalpublic as being important and worthy of preservation. In general, an excessive accumulation of algal biomass is the symptom of eutrophicationthat is most easilyperceived and most disliked by the public. A remarkable unity in the response of algal production to eutrophication has in fact been found in most aquaticecosystems thathavebeen studied,and a demonstrated

success inreducingalgalbiomass to publiclyacceptable levels has been the feature held in common by all successful eutrophication control efforts (Smith 1998).
The literature on eutrophication is expanding rapidly, and cannot be reviewed comprehensively in this paper. A large number of historical and technical reviews have appeared during the past several years (e.g., Carlson and Simpson 1998, Correll 1998, Smith 1998, Smith et al. 19.99, Swedish EPA 2000, U.S. EPA 2002), and this informationwilt not be repeated here. The purpose ofthis mini-reviewis to provide

a brief update of our knowledge of the effects of eutrophication on algal-related water quality in both freshwater and coastalmarine ecosystems,and to suggestkeyareas that may be fruitful for future research efforts.

1 Eutrophication of Freshwater Ecosystems

1.1 Lakes and reservoirs


### Effects of eutrophication on algal biomass. Because phosphorus has been identifiedas a keygrowth-limitingnutrient for algae in lakes and reservoirs (Schindler 1977, OECD 1982), phosphorus-based eutrophication classification systems and management schemeshave been developed worldwide. An example of the Swedish eutrophication classification system for lakes is shown in Table 2.

Table 2" Swedish eutrophication classification system for freshwater lakes according to the growing season biovolume of planktonic algae (modified from Will6n 2000
Class:

...... mm perL ;mm per

Particularly small biomass _<0.1 la <0.1

1b Very small biomass 0.1-0.5 0.1-0.5 Oligotrophic
2 Small biomass 0.5-1.5 0.5-2 Mesotrophic
3 Moderately large biomass 1.5-2.5 2-4 Eutrophy I
4 Large biomass 2.5-5 4-8 Eutrophy II
5 Very large biomass >5 >8 Hypertrophy Ultraoligotrophic

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## Eutrophication Review Articles

In general, the growing season average biomass of algae in lakes is strongly dependent upon the concentration of total phosphorus (TP, lag/L) in the water. However, the relative availabilities ofnitrogen and phosphorus change consistently with cultural eutrophication (DowningandMcCauley 1992), and the response ofalgal biomassto TP is stronglymodified bythe total nitrogen to total phosphorus (TN:TP) ratio (cf. Forsbergand Ryding 1980, Smith 1982, Canfield 1983, Prairie et al. 1989, McCauley et al. 1989, Faafeng and Hessen 1993, Seip 1994).
The globalrobustness ofalgal biomass-nutrient relationships has been well demonstrated in many cross-sectional analyses of lakes and reservoirs (Sakamoto 

### 1966, Lund 1970, Dillon and Rigler 1974,Jones and Bachmann 

### 1976,Ahl and Weiderholm 1977, Nicholls and Dillon 1978, Canfield and Bachmann 1981, Chow-Fraser et al. 1994, Seip and Ibrekk 1988, Smith 1990a, Jones et al. 

### 1998,Niirnberg 

### 1996,Mazumder and Havens 1998, Portielje and Van derMolen 1999, Seip et al. 

### 1992,2000, Brown et al. 2000). Information on the responses of lake and reservoir water quality to nutrient enrichment is now available from most ofthe geographical regions of the world (e.g., Africa: Thornton 1980, Harper et al. 

### 1993,Hecky 

### 1993,Kebede et al. 

### 1994,van Ginkel et al. 2000, Varis and Fraboulet-Jussila 2002; Australia: Ferris and Tyler 

### 1985, Davis 1997; Central and South America: Quir6s 

### 1991,1998; Salas and Martino 1991, Jones et al. 1993; China: Chang 2002, Dickman et al. 2001; Europe: Hrb~i&k and Popovsk)~1978; Vyhnfileket al. 1994; Kop~i&k et al. 

### 1996, Istvfinovics and Somly6dy 1999; Greece: Danielidis et al. 1996; Ireland and the U.K.: Harper and Stewart 1987, Traille 

### 1991,Sutcliffe and Jones 1992; Moss et al. 1996, Wilson 1998; India: Bhade et al. 2001, Kaul 1977; Israel: Gophen et al. 

### 1999;Italy: de Bernardi et al. 

### 1996, Heinonen et al. 2000; Japan: Seip and Satoh 1984, Fukushima and Muraoka 1988; Korea: An andJones 2000, 2002; Nepal: Aizaki et al. 1987, Jones et al. 1989; New Zealand: Pridmore et al. 

### 1985,McBride and Pridmore 1988, Duggan et al. 2001; Oman: Victor et al. 2002; Scandinavia: Will~n 2000, Rask et al. 2002; Sri Lanka: Piyasiri 2001; Thailand: Jones et al. 2000; and Turkey: Tanik et al. 

### 1999).

In general, comparative studies offreshwater eutrophication strongly suggest that effortsto control external nutrient loading to many lakes will tend to achieve similar reductions in their average algal biomass, regardless of geographical location (Seipet al. 2000; but for exceptions, see Sas 

### 1989, Moss et al. 

### 1996,Carpenter et al. 

### 1999).However,the growing season or yearlyaverage biomass ofalgae

### perseis probablynotconsciouslymeasured or usedbythe users ofa water body as their primary index of water quality impairment: the maximal concentrations ofalgal biomassthat occur during transient blooms are much more easily detected, and

even more strongly disliked bythe public.Jones et al. (1979) reported a linear arithmetic relationship between mean algal biomass (estimated as chlorophyll a) and maximum algal biomass in U.S. lakes:

Chlm~

. = 1.7 (Chlmoa,) + 0.2, r2 = 0.58 

### (1) Other investigators have reported a much steeper arithmetic slope (2.6 rather than 1.7; see OECD 1982); however, the variance in the relationship ofJones et al. (1979: their Fig. 1) increases strongly with the value of Chl

..... implying that empirical modelsbased on log-transformed data should be stronger and statistically more appropriate. Stadelmann et al. (2001) have examined relationships betweenmean and maximum chlorophyll a during the growing season in Minnesota lakes, and they indeed found a very strong log-linear relationship (note that the dependent and independent variables are reversed in their analysis),

Ioglo (Chl

.... ) = 0.91 Ioglo (Chlma,) -0.20, r2 = 0.91 (2)


### Similarly,Will~n(2000) reported an empirical relationship between late-summer peak biomass and growing-season mean algal biomass (based upon algal biovolume rather than Chl a),

Total Volume~gust = 1.65 (Total VolumeMay.Octo~,) -0.26, r2= 0.75 (3)



### In addition, she reported a strong relationship between annual peak algal biomass and growing-season mean concentrations oftotal phosphorus,

log10 (Annual Peak Total Volume) = 1.512 Ioglo 

### (TPMarch.October) -1.924, r2 = 0.76 (4)


### Phosphorus-based models can also be used to quantify the response ofnuisance algal bloom frequencyto reductions in nutrient loading. For example, Havens and Walker (2002) have developedpredictive models relating water column TP concentrations to the frequency algal blooms in Lake Okeechobee, Florida (USA), which they used to establish in-lake total phosphorus goals that will be required to reduce water quality impairment in this multiple-use lake. Similarly, Lathrop et al. (1998) have developedmodels to predict the phosphorus loading reductions needed to reduce the frequency of blue-green algal blooms in Lake Mendota, Wisconsin (USA). Although both the average and the peak biomass of algae in lakes oftenrespond verysensitivelytochanges innutrient availability,severalcritical site-specificfactors can alter theresponses of algal growth to external N and P loading. For example, variations in depth can potentially modify algal growth (Petersen et al. 1997), and deep lakes produce a lower algal biomass per unit total phosphorus than shallow lakes (Smith 1990a). For example, the May-October mean biovolume of algae in shallow, wind-mixed lakes (mean depth _<3meters) is typically twice as great as the values observed in thermally stratified, deep lakes of similar fertility in Sweden (Will~n 2000). Similarly, Mazumder (1994a) noted higher levels of algal biomass (measured as chlorophyll a) in shallow, mixed lakes than in stratified lakes. In addition to these cross-system differences, lakes with complexphysical structure can exhibit remarkable spatial variations in water chemistry and algal biomass (cf.Phlips et al. 1993). For example, the 

### within-lake variation observedin Table Rock, Missouri (USA)is so large that it almostmatches the magnitude of

### lake-to-lake variation within the entire state (Jones et al. 1997)!



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## Review Articles Eutrophication

In addition to the above effects of morphometry, the hydraulic residence time of a waterbodypotentiallycan influence the biomass ofalgaeproduced bynutrientsifthe water residence time is shorter than the doubling times (ca. 0.5- 1.5 days) ofphytoplanktonalgae (Reynolds 1997). Significanteffects ofhydraulicflushing on phytoplanktonbiomass have indeed been observed in the very small fraction of waterbodies that have exceptionally short water residence times (McBride and Pridmore 1988, Smith 1990a). However, in environments which experience strong seasonality in rainfall and hydrology such as southeastern Asia, dramatic changes in water quality also can occur as a result of periodic monsoons (Jones et al. 1997). Other physical factors can modifythe biological expressions ofeutrophication

as well. For example, high rates of soil erosion in the watershed can result in elevated inorganic turbidity levels that

can strongly attenuate underwater light and potentiallyreduce the algal biomass produced at a given concentrationof totalphosphorus (Canfield and Bachmann 1981, Hoyerand Jones 1982, Ferris and Tyler 1985, Carlson 1991, Jones et al. 1998, Dokulil 1994, Jones et al. 1997).
Biotic factors can also be extremely important. In shallow lakes that have the potentialto develop large populations of aquatic vascular plants (macrophytes), the presence or absence of these plants can strongly modify the biomass of algae produced at a given nutrient supply level(Canfield et al. 1983).For example, Portielje and Van der Molen (1999) reported significantly lower chlorophylla concentrationsin shallow Dutchlakes andpondswith submersed macrophytes coverage exceeding 5% of the total surface area. Shallow lakes inherently have the capacity to develop large macrophytepopulations, and also mayexhibit strong internal phosphorus loading due to regeneration from the lake sediments. Such lakes may not respond to nutrient loading managementin the manner predicted by simple eutrophication models (Moss et al. 1996, Carpenter et al. 1999). In

some cases, shallow eutrophic lakes can alternate between two equilibrium points, in which one stable state is dominatedbymacrophytes,and the alternate stable state is dominated by optically thick phytoplankton communities (Schefferet al. 1993, Scheffer 1998).
The effects of food web structure on algal biomass in lakes have also been extremelywell characterized duringthe past 25 years (Shapiro et al. 1975, Hrbfieek et al. 1978, Carpenter and Kitchell 1993, Mazumder 1994a,b, Carpenter et al. 1995, Lacroix et al. 1996, Carpenter 2002). In particular, lake-to-lake differences in the abundance and structure of fish communitiescan profoundlyinfluence algal biomass by modifying the grazing pressure of zooplankton on phytoplankton.Largecladocerans such as

### Dapbia pulexand

### Dapbniapulicariatypicallybecome abundantin lakes havingfew (or no) planktivorous fish, and these large-bodied herbivores are extremely effective grazers. Lakes dominated by planktivorous (zooplankton-eating) fish thus produce a significantly higher algal biomass per unit TP than lakes dominated by piscivorous (fish-eating) fish, because the intensity of zooplankton grazing on algae is typically lowest in planktivore-dominated systems (Carpenter and Kitchell 1993, Quir6s 1991,1998). However, the effectsoffoodweb structure on algal biomass can also bemodifiedbythe physical structure ofthe environment (e.g., lake depth: Proulx et al. 1996, Bertolo et al. 2000).
Such trophic interactions also offer the potential for using food web manipulations (biomanipulation: Shapiro et al. 

### 1975)as a means to reduce nuisance phytoplanktonbiomass in nutrient-enriched lakes. The record of biomanipulation

as a managementtool oftenhas been positive, butthe actual responses to deliberate fish manipulationshave been highly variable (Gulati et al. 1990, Cottingham and Knight 1995, Sarvala et al. 2000, Sendergaard et al. 2000).
Effects of eutrophication on algal species composition. The biomass ofphytoplanktonis frequently, but not always, the primary focus of attention in lake and reservoir management. Algal species composition in many cases may be a
more importantfacetofwater qualityfor the users and consumers of freshwater. Bloom-forming blue-green algae (cyanobacteria) typicallybecome dominantover other algal species in the phytoplankton of eutrophic lakes (Schindler 

### 1977, Reynolds 1997, Smith 1990a, 2001). These cyanobacteria can form objectionable surface scums (Klemer and Konopka 1989, Paerl 1988); can cause summer fishkills (Barica 1978, Lathrop et al. 1998, Kann and Smith 1999); and can impair the quality of drinking water (Cooke and Kennedy2001, Smith et al. 2003).

In addition, many cyanobacteria can produce highlyhepatotoxic, cytotoxic,and neurotoxiccompoundsthat are hazardous to humans, cattle, domestic animals, and aquatic

consumers (Fulton and Paerl 1987, Hawser et al. 1992,Carmichael 1997, Chorus and Bartram 1999, Sivonen 2000,

van Ginkel et al. 2000, Chorus 2001). Mass occurrences of toxic cyanobacteria are a global phenomenon, althoughthe timing and durationofthe bloom-forming season varieswith geographic location (Sivonen 2000). In Europe alone, surveys using toxicity bioassays or high performance liquid chromatography have revealed an unexpectedly high frequency oftoxic blooms (Fig. 1).
The general patterns ofresponse by toxic cyanobacteria to eutrophication are nicely summarized in a recent comparative study byWill~n et al. (2000). Both the intensityof late

100

E


## -g

I1) 13. 90 8O 70 60 5O 40 3O 2O 10 0

Fig. 1: Frequencies of toxic cyanobacterial blooms in 11 European countries (data from Table 2.2.1 in Sivonen 2000)

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## Eutrophication Review Articles

Table 3: Swedish eutrophication classification s'

Very small biomass rstemfortotal phosphorus and water-bloomingcyanobacteriain late summer (modifiedfrom Willan 2000)



### <0.5 6-12.5 <_2.
2 Small biomass 12.5-25 0.5-1 - 3 Moderately large biomass 25-50 1-2.5 3-4
4 Large biomass 50-100 2.5-5 - 5 Very large biomass >100 >5 4



### summer cyanobacterialblooms and the number oftoxin-producing genera increase with eutrophication in Swedish lakes (Table 3). However, Will6n et al. (2000) found no trend in peak cyanobacterial toxicity (tag/gdry wt. of algae) with lake trophic state, and found that maximum cyanophyte toxicity

wasmore closelyrelated to speciesdominance than to season. While many past studies ofcyanobacteria have focusedprimarily on the phytoplankton of natural lakes, toxic bluegreen blooms also frequently occur in enriched, turbid Australian reservoirs (Davis 1997); similarly, 10 of 15 turbid Kansas reservoirs studied by Dodds (1996) were found to contain potentially toxic, microcystin-producing cyanobacterial strains. The empirical study of Smith (1990b) and the data shown inFig. 2 indicate that cyanobacterial dominance

can increase dramatically with nutrient enrichment in turbid, man-made impoundments; however, this general response is likely to be modified by the presence of high concentrations ofnon-volatile suspended solids (Smith 1990b).

lOO
E 90-1 9 9

>o 801, 9

0 9 ~ 70 -1 9

.a ~ 60-1

.__. 

### $ 50 -1 

### 40 -1 30-1 9

~, 20-1 9

i i 0 50 100 150 200 250 300

Total Algal Biovolume, rng/L
Fig. 2: Relationship between cyanobacterialdominance and trophic state (as measured by summer algal biovolume) in 39 turbid Kansas, USA reservoirs. Data from Carney (2001)



### Empirical models relating the relative and absolute biomass of cyanobacteria to nutrient concentrations (Smith 

### 1985, 1986, 1990b, Smith et al. 1987), and models to predict the response of cyanobacterial blooms to phosphorus loading reductions (Lathrop et al. 1998), have beendeveloped. However, a lively debate is currently being waged in the literature concerning the primary mechanisms that are responsible for cyanobacterial dominance in eutrophic lakes. A number ofpotential mechanisms have been proposed in the literature (Shapiro 

### 1989,Klemer and Konopka 1989), but perhaps the most contentious is the relative role ofnitrogen, phosphorus (N, P) ratios. Empirical and experimental evidence supporting the N:P ratio hypothesis ofcyanobacterial dominance has been summarized by Smith and Bennett (1999), and the N:P ratio hypothesis has also recently been modifiedto include the effects offoodwebstructure byElser (1999). However,other researchers (e.g.,Trimbee and Prepas 1987, Canfield et al. 1989, Jensen et al. 1994, Reynolds 

### 1997,Downing et al. 2001) have concluded from their own analysesthat elevated absoluteconcentrations oftotal phosphorus 

### perse, rather than the presence of low TN:TP ratios, result in cyanobacterial dominance. This extremely important fundamental question remains unresolved, and is

a key topic for future eutrophication research.

1.2 Streamsand rivers 

### Although eutrophication research in streams and rivers has lagged behind that of lakes and reservoirs, the nutrient enrichment of streams and rivers is nonetheless of great concern (Behrendt 

### 1993,Biggs2000). IntheU.S.,concerns about hypoxia in the Gulf of Mexico led to a White House-commissioned task group onthe effects ofreduced nutrient loading on surface water quality in the Mississippi River basin (Brezonik etal. 1999). InEurope, investigators havereported extensive eutrophication of the Bure River system in the United Kingdom (Moss et al. 

### 1989,Moss and Balls 1989); K6hler and Gelbrecht (1998) have documented significant eutrophication in several majorrivers in Germany; and Billen et al. (1994) have demonstrated strong differences in algal development at different sites in the Oise and Marne river system in France. The concept that flowing waters are almost always nutrient-saturated, and the conclusion that physical factors such as light-limitation and short hydraulic residence times consistentlyprevent or restrict anypotential algal responses to nutrient enrichment in rivers, both no longer appear to be tenable (Smith et al. 

### 1999).As will be reviewedin separate sections below,the nutrient enrichment of flowing waters strongly modifies the biomass and community structure of both suspended and benthic algae.
Several nutrient classification systems have been proposed for flowing waters. For example, McGarrigle (1993) concluded that maintaining a mean annual dissolved inorganic phosphorus concentration <47 lag/L was necessary to prevent the nuisance growth of attached algae and to preserve water quality suitable for salmonid fishes in Irish rivers. The U.K. Environment Agency (1998) has used annual mean values of soluble reactive phosphorus (SRP, lagP/L) as the boundaries for four trophic state categories in streams and rivers: oligotrophic (20 lagP/L) mesotrophic (60 tagP/L); mesoeutrophic (100 lagP/L); and eutrophic (200 lagP/L).In contrast, Dodds et al. (1998) have proposed trophic state



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## Review Articles Eutrophication

Table 4: Suggested boundariesfor trophic classification of temperate streams (Dodds et al. 1998)

oligotrophic <20 <60 mesotrophic 20-70 60-200 eutrophic >70 >200 <10 <700 <25 10-30 700-1500 25-75 >30 >1500 >75



### boundaries for temperate streams using concentrations of total nitrogen (TN, lag/L) and total phosphorus, which may be more directly compared to those for lakes (Table 4). The general issue of establishing nutrient criteria in streams is discussed by Dodds and Welch (2000).
Effects of eutrophication on 

### suspended algal biomass. The production of suspended algae per unit total phosphorus is often significantly lower in rivers than in lakes and reservoirs (Dokulil 

### 1994,Soballe and Kimmel 1987, Van Nieuwenhuyse and Jones 1996). This reduced response to nutrients may be caused in some systems by the high washout rate that the flowing water imposes on suspended algal biomass. For example, a very strong inverse relationship was observedbetween suspended chlorophyll a concentrations and discharge inthe Hungarian Danube (cf.Fig.4 in Schmidt 1994). In addition, the potential for high algal productivity in nutrient-rich, well-mixed systems may not be realized if the presence ofsuspended soilsgreatly reduces underwater light availability (Dokuli11994). To myknowledge, light attenuation by suspended inorganic particulates has not been explicitly included in previous empirical models linking nutrient concentrations to suspended algal biomass in fluvial ecosystems. However, data from the Mississippi River (Fig. 3) do not reveal a consistent reduction in the yield of suspended chlorophyll a at stations containing high concentrations ofnon-volatile suspended solids (NVSS, mg/L), and this question should be explored further in additional river systems.
An important prediction of Fig. 3 and other empirical nutrient-chlorophyll models for streams and rivers (e.g., Basu and Pick 1996, Van Neeuwenhuyse and Jones 1996, Lohman and Jones 

### 1999,Champion and Currie 2000) is that reductions in suspended algal biomass should generally occur in rivers that experience significant TP reductions following the imposition of point and non-point source controls. A strong reduction in suspended chlorophyll a (Fig. 4) indeed appears

J

o 

### 8 1000

100

10 [] NVSS:TP<0.13 9NVSS:TP>0.13



## \

[3 []
u 41,~
[] [] 9

[]

1 i 10 100

Total Phosphorus, ug/L 1000

Fig. 3: Relationship between suspended algal biomass andtotal phosphorus in the Mississippi River. NVSS, TP ratios greater than 0.13 indicate high levels of inorganic turbidity, and potential shading inhibition of algal growth in the river. Datafrom Heiskary and Markus (2001) 180 16O 140

:=- 120

~. lO0

~_ 80

o 60 g~ 40
20 Gunston Cove, Potomac River

1997

0 50 100 150 200

Total Phosphorus, pg/L

Fig. 4- Response of Gunston Cove in the tidal freshwater Potomac River USA, to reductions in point source phosphorus loading. Note that the response appearsto be hysteretic.The data shown are estimates of annual

means derived from LOWESS fits to the entire dataset by Jones (2000)



### to have occurred in the tidal freshwater Potomac River (USA)

as a result ofpoint source phosphorus loading controls (Jones 2000). Also of very great interest in Fig. 4 is an apparent hysteresis in this chlorophyll-phosphorus relationship; such hystereticresponses to changes innutrient loading can be seen in lakes (e.g., Lake Washington, USA; see Smith 1998), and

can significantly complicate the recovery of aquatic ecosystems from eutrophication (Carpenter et al. 1999).
Effectsofeutrophication on suspended algal community structure. As in lakes, nuisance blooms of cyanobacteria can seriously degrade the water quality offluvial ecosystems (Paerl et al. 

### 1990,Prygiel and Leitao 1994, Ha et al. 1998, Mitrovic et al. 2000). Heiskary and Markus (2001) provide data that allow an initial test ofthe hypothesis that eutrophication causes predictable and directional shifts in the community structure of suspended algae in flowingwaters. An analysis oftheir data (Fig. 5) suggests that cyanobacterial dominance in large rivers increases strongly and predictably with phosphorus enrichment, just as it does in eutrophic lakes and reservoirs.

(D 

## =E

.I3

e

-(3 O

o o4 90 80
70 60
50 40
30-
20-
10
0 0%BG = 58.9 Iog(TP) - 86.7

r2= 0.72

100 200 300
Total Phosphorus, IJg/L

J

400

Fig. 5: Relationship between blue-greenalgal dominance and total phosphorus in the Mississippi River. Data from Heiskaryand Markus (2001)

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## Eutrophication Review Articles

Phytoplankton dynamicsin rivers thus may not be so different from those observed in shallow lakes (Reynolds 1994), with traditional biotic interactions between algae and nutrients perhaps being dampened or modified by fluvial conditions, but not totallyunexpressed.
Effectsofeutrophication onbenthic algalbiomass. As is true ofperiphytonin lakes (Eloranta 2000, Herve 2000), benthic algae on natural substrates in flowing waters can respond sensitively to anthropogenic nutrient enrichment (Welch et al. 1992). A recent meta-analysis of nutrient enrichment experiments in streams by Francoeur (2001) has confirmed that benthic algal biomass can be significantlyincreased by the addition of either N or P, and Borchardt 

## (1996) published a review ofthe literature on nutrients and stream periphytoncommunities. Krewer and Holm (1986)and Homer et al. (1990) observed a strong curvilinear dependence of periphyton growth on phosphorus in artificial laboratory channels, and this general relationship has been confirmed for loticecosystemsbyDodds et al. (1997, 2002). Similarto the nitrogen-phosphorus interactions documentedin Section 1.1 above for lakes, and consistent with the strong N, P interactions documentedin Francoeur's (2001) streammetaanalysis, the biomass of benthic algae growing on natural substrates appears to be dependent upon both TN and TP concentrations in the stream water (Fig. 6).

1000

100

_9.o x: 1 0

0.1 9 TN:TP<10 0

O TN:TP>10 I~ D [] i1, 9 9

i i 10 100 1000 Total Phosphorus, ug/L A~

10000

Fig. 6: Relationship between benthic algal biomass and total phosphorus in streams. As is true of phytoplankton in lakes (Smith 1982), the yield of periphyticalgae in flowing waters appearsto be reduced when theTN:TP ratio is <10, 1 by mass. Note: these data are based only upon algal samples collected from natural substrates, and errors in the database have been corrected from the dataset analyzed in Dodds et al. (2002)



### Effects of eutrophication on the community structure of benthic algae. Shifts in community structure along nutrient supply gradients are a common feature ofmost aquatic ecosystems, and attached algae in streams are no exception. Whether these communities are influencedby exotic species (e.g. 

## Hydrodictyonreticulatum: Hall and Cox 

## 1995,Hall and Payne 1997), or are undisturbed by exotic invaders, nutrient availability often has a strong selective role in determining the species composition of benthic algal communities. Epilithic diatoms can be used as sensitive indicators of streamwater total nitrogen and totalphosphorus concentrations (Winterand Duthie2001), and Ch&elatet al. (1999) reported marked directional shifts in overall community composition as the total biomass ofbenthic algae increased. The proportion of green algae (Chlorophyta), for example, increased with benthic chlorophyll a and was highest at moderately eutrophic sites. These studies suggest that predictivemodels similarto those developed forphytoplankton communities in lakes, and for suspended algae in rivers (see Fig. 5), can be developed for benthic algae.

1.3 Wetlands 

### Effects of eutrophication on algal biomass and community structure.Wetlands (areas wherewater saturationisthedominant factor determining the nature of soil development, and structuringthe associated plantand animalcommunities:Wolff 1993) are a verycommon feature ofmanylandscapes worldwide.However,asnotedbyCrosbie and Chow-Fraser (1999), the impact of human land use and nutrient loading on the water quality of freshwater wetlands has seldom been documented. Given the consistency of algal responses to nutrient enrichment in lakes, it might be expected that similar nutrient-algal biomass relationships would be observed for wetlands. A plot of data from 22 marshes in the Great Lakes Basin of Ontario, Canada (Crosbie and Chow-Fraser 1999), confirmedthat suspended chlorophylla in these wetlandsresponded strongly to increases in average water column total phosphorus (TP)concentrations (Fig. 7):

log10 (Chlmoa,)= 1.14 Ioglo (TP

....) + 1.17, r2= 0.72 (s)

1000

lO0
m

## 2

10

.J

r 1 10

lOOs
B

10s 9 9 9 nmm

100

Total Phosphorus,pg P/L m m

1000

IC 9 //

9 mm,,#

m 1 f /" /.

m am // / m9 //

99 mm

m jiBe"

9 9 . m j/" 9 ///" 9
//

10 i 100 1000 Observed Chla, pg/L Fig. 7: A. Relationship between suspended chlorophyll a and total phosphorus concentrations in 22 marshes near Ontario, Canada. Each data point represents the mean of two sampling trips during the growing season. B. Predictedversus observedchlorophyll a concentrations for the 22 marshes above, using Equation 4 in Table 2 of Lurid (1998)



### 132 ESPR - Environ Sci & PoUut Res 10 (2) 2003

## Review Articles Eutrophication

Moreover, the algal biomass in these 22 marshes covaried with the predictions of a new empirical model developed for wetlands located on the Swan Coastal Plain ofAustralia (Lund 1998), although the predicted algal biomass consistentlyexceededthe observedvalues. Thisprediction bias may be due in part to the original model specification: the empirical chlorophyll-phosphorus model of Lund (1998) was developed using a mixture of data from lakes (permanently inundated), sumplands (seasonallyinundated), and artificial wetlands. Nonetheless, the data in Fig. 7 suggest that the biomass of suspended algae in wetlands tends to respond strongly and predictably to changes in nutrient inputs.
The possibility also exists that algal communities in nutrient-enriched wetlands experience directional shifts in species composition that parallel those found in lakes, reservoirs, and large rivers. For example, a recent survey of 32 Kansas (USA)wetland areas by Carney (2002) revealedthat the planktonic algae were dominated by cyanobacteria in the most eutrophic wetlands. Effortsto develop newmodels for suspended and attached algae in both freshwater and coastal marine wetlands would be a valuable new area for future eutrophication research; such models could provide objective, quantitative guidance in the restoration and protection of wetlands from excess nutrient loading.

2 Eutrophication of Estuarine and Coastal Marine Ecosystems


### A verylarge fraction ofthe nutrients exported fromthe land surface to streams and rivers ultimately makes its way to the sea, and as a result, estuaries receive more nutrient inputs per unit surface area than any other type of ecosystem (Howarth 1993). Morethan halfoftheworld'shumanpopulation resides within 60 kilometers of the coast, and more than 90% of the world's fisheries depend in one way or another on estuarine and near-shore habitats (Hobble et al. 2000). Increased nutrient loading results in a wide variety of changes in the structure and function of coastal marine ecosystems (cf. Fig. 2 in Schramm 

### 1999), and protecting these systemsfromthemanyadverseeffects ofeutrophication is extremelyimportant (U.S.EPA 

### 1996b,National Research Council 2000, Rabelais and Nixon 

### 2002).As can be seen in Table 5, the Swedish EPA has developed a nutrient-based classification scheme for coastal marine ecosystems that strongly resembles the trophic state categories presented earlier in Tables 2--4 for freshwater ecosystems.
The possibility of applying a limnological approach to the management of coastal marine eutrophication was noted in

Table 5: Swedish eutrophication classification system for coastal marine been roundedfrom the original molar values) 

### the literature over two decades ago (Schindler 1981, Lee andJones 1981). However, althoughfreshwatereutrophication management can be considered a success story in ecosystem science (Smith 1998), ithas recentlybeen questioned in the literature whether the limnologicalexperience can be repeated for estuaries and coastal marine ecosystems (Sharp 2001). Rapidly accumulating evidence suggests that the answer to this critically important question is an increasingly confident

### yes! While estuarine and coastal marine systems

can often be hydrologically and spatially complex, the biomass ofphytoplanktoninthese systemsnonethelesstends to respond predictably to changes in the water column concentrations of total nitrogen and total phosphorus.

An analysis ofDanish coastal waters byNielsen et al. 

### (2002) is an excellent example of recent successes in coastal zone eutrophicationmodeling.Nielsenetal. 

### (2002)analyzeda very large dataset from 162 stations located in 27 Danish fjords and coastal waters, and developed empirical models for total nitrogen (TN, tag/L),chlorophyll a (Chl, lag/L), suspended matter (Wsusp

, mg dry wt./L), and Secchi disk transparency (SD, m) that should help to provide objective guidance for water quality managementin Danish coastal waters,

In (Chl) = 0.963 In (TN) -4.186, r2= 0.30 (6)

In (SD) = -0.444 In (Chl) -0.367 In (Wsusp)+ 2,686, R2= 0.81 (7)

In (SD) = -0.894 In (TN) + 6.818, r 2= 0.48 (8)



### Additionalmodels based upon eithertotal phosphorus or total nitrogen have been developed for coastal marine ecosystems in the Adriatic Sea (Vollenweider et al. 1992); Canada (Champion and Currie 2000, Meeuwig et al. 1998); Mexico (Contreras and Kerekes 1993); Scandinavia (Hfikanson and Wallin 

### 1991,Borum 

### 1996,Meeuwiget al. 2000, Elmgrenand Larsson 2001, Nielsen et al. 2002); and the USA (Boyntonet al. 

### 1996, Bowen and Valiela 2001). Efforts have also been made to apply the OECD's critical load concept to Norwegian marine waters (Hessen et al. 1992), and Janicki (2001) has developed a chlorophyll a-based trophic state index for Florida (USA) estuaries that parallels the highly successful trophic state index created by Carlson (1977) for lakes. Even

moreimportantly,improvementsincoastalmarinewaterqualitytendtofollowreductionsinexternalnutrientloading(Smith et al. 

### 1999,Boesch et al. 2001, Elmgren and Larsson 2001),

as has been documented in many freshwater lakes.
However, as stressed by Richardson 

### (1996), scientists cannot be expected to identify and recommend courses of acsurface water (modified from Swedish EPA 2000; nutrient concentrations have

Very low Summer TN;H~L :
<252 Summer TP, pg/L

<15

2 Low 252-308 15-19

3 Moderate 308-364 19-24

4 High 364-448 24-31

5 Very high >448 >31 August Chloro~y!l a, p~
<1.5

1.5-2.2

2.2-3.2

3.2-5.0
>5.0

ESPR- Environ Sci & Pollut Res 10 (2) 2003 

## 133

## Eutrophication Review Articles

tion to combat coastal zone eutrophication in the absence ofclear goals for environmentalconditions desired in a given

area. Objective water quality targets can be defined by using one or more of the following methods:
1. By applying quantitative water quality criteria developed bylocal,regional,orfederalenvironmentalprotectionagencies, such asthe empiricalboundariesforTN, TP, and Chla concentrations in eutrophic waterbodies that have been proposed for coastal waters (e.g. H~kanson 1994); 2. By using historical data, time series data, or reference region data to establish referencevalues that reflectpristine water quality conditions completely free of any effects of human activity (e.g., Table 2b in Swedish EPA 2000); or 3. By using robust surveymethods that allow local users of the water resource to generate quantitative estimates for the value of a key water quality variable (the Quality Variable of Concern, sensu Reckhow and Chapra 1983), that represents their perception of the critical point at which undesirable water quality is present.
Once target goals have been established, quantitative relationships between water quality and nutrients can be used to calculate the critical water column nutrient concentrations that must be attained in order to reach these target conditions. This information then can be linked to macroscalemodels ofnutrient and water fluxesto the coastal zone (e.g., Valiela et al. 1997) in order to identifythe corresponding nutrient loading rates that must be achieved to obtain desirable water quality in the receiving waters being managed (for example, cf. Fig. 9 in Valiela et al. 2000). However, many critical questions still remain regarding the actual developmentand implementation ofmeasures to protect coastal marine ecosystemsfrom eutrophication, and answering these questions will require thoughtful, trans-disciplinary efforts (cf. Elmgren and Larsson 2001).

3 Conclusions and Outlook


### A remarkable unity is evidentin the global response of algal biomass to nitrogen and phosphorus availabilityin lakes and reservoirs; wetlands; streams and rivers; and estuaries and coastal marine waters. The species composition ofalgal communities inhabiting the water column appears to respond similarly to nutrient loading, whether in lakes, reservoirs,

or rivers. As is true of freshwater ecosystems, the recent literature suggests that marine ecosystems respond positively to nutrient loading control efforts.
As can be seen in the above review, our understanding of freshwater eutrophication and its effects on algal-related
water quality is extremely strong and is advancing rapidly. Unfortunately, however, our understanding of the effects of eutrophication on estuarine and coastal marine ecosystems is much more limited, and this gap represents an important future research need. While estuarine and coastal marine systems may often be hydrologically complex, numerous empirical analyses that have been performed worldwide indicate that the biomass of marine phytoplankton responds sensitively and predictably to changes in the external supplies ofnitrogen and phosphorus. These models in turn suggest that efforts to manage nutrient inputs to the seas will result in significant improvements in coastal zone water quality. Efforts should be made to develop new models that quantitativelylink ecosystem-levelresponses to nutrient loading in both freshwater and marine systems.

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ingMgal Blooms: OutcomesfromCSIRO'sMulti-divisional Bluegreen Algal Program. CSIRO, Canberra, ACT, Australia JonesJR, BachmannRW (1976): Prediction ofphosphorus and chlorophylllevelsinlakes. J Water Pollut ControlFed 48, 2176-2182 Jones JR, Knowlton MF, Kaiser MS (1998): Effects of aggregation

onchlorophyll-phosphorusrelations inMissouri reservoirs. Lake Reservoir Manage 14, 1-9 Jones JR, Knowlton MF, An K-G (1997): Developing a paradigm to study and model the eutrophication process in Korean reservoirs. Korean J Limnology30(Suppl), 463-471 JonesJR, KnowltonMF, Swar DB (1989): Limnologicalreconnaissance of waterbodies in central and southern Nepal. Hydrobiologia 184, 171-189 Jones JR, Lohman K, Umafia VG (1993): Water chemistry and trophic state of eight lakes in Costa Rica. Verh Int Ver Theor Angew Limnol 25, 899-905 Jones JR, Perkins BD, Witt A, Jr, Kaiser MS, Thamasara S, Siriworakul M, Benyasut P (2000): Limnological characteristics of some reservoirs in Thailand. Verh Int Vet Theor Angew Limnol 27, 2158-2166 Jones RA, Rast W, Lee GF (1979): Relationships between summer
mean and maximum chlorophyll a concentrations in lakes. Env Sci Technol 13, 869-870 Jones RC (2000): Long-termtrends in phytoplankton chlorophylla in the tidal freshwater PotomacRiver, USA: Relationship to climatic and management factors. Verh Int Ver Theor Angew Limnol 27, 2959-2962 Kann J, Smith VH (1999): Estimating the probability ofexceeding elevated pH values critical to fish populations in a hypereutrophic lake. Can J Fish Aquat Sci 56, 1-9 Kaul V (1977): Limnological survey ofKashmir lakes with reference to trophic status and conservation. IntJ Ecol Envir Sci 3, 19-44 Kauppi L, Pietil/iinen O-P, Knuuttila S (1993): Impacts of agricultural nutrient loading onFinnish watercourses. Water SciTechnol 28,461-471 Kebede E, G-Mariam Z, Ahlgren I (1994): The Ethiopian RiftValley lakes: chemical characteristics of a salinity-alkalinity series. Hydrobiologia 288, 1-12 Klemer AR, Konopka A (1989): Causes and consequences ofbluegreen algal (cyanobacterial) blooms. Lake Reservoir Manage 5, 9-19 K6hler J, Gelbrecht J (1998): Interactions between phytoplankton dynamics and nutrient supply along the lowland river Spree, Germany. Verh Int Vet Theor Angew Limnol 26, 1045-1049 Kop~cek J, Stuchllk E, Vyhn~lek V, ZSvodsk9 D (1996): Concentration of nutrients in selected lakes in the High Tatra Mountains, Slovakia: effect of season and watershed. Hydrobiologia 319, 47-55 KrewerJA, Holm HW (1982): The phosphorus-chlorophylla relationship in periphytic communities in a controlled ecosystem. Hydrobiologia 94, 173-176 Lacroix G, Lescher-Moutou~ C, Pourriot R (1996): Trophic interactions, nutrient supply, and structure offreshwater pelagic food webs, p 162-179. In: M Hochberg, J Clobert, and R Barbault, Eds, Aspects in the Genesis and Maintenance of Biological Diversity. Oxford University Press, Oxford, UK Lathrop RC, Carpenter SR, Stow CA, Soranno PA, Panuska JC (1998): Phosphorus loading reductions needed to control bluegreen algal blooms in Lake Mendota. Can J Fish Aquat Sci 55, 1169-1178 Lee GF,Jones RA (1981): Application ofthe OECD eutrophication modeling approach to estuaries, p 549-568. In: BJNielson and LECronin, Eds, Estuaries and nutrients. Humana Press, Clifton, NJ, USA Lohman K,JonesJR (1999): Nutrient-sestonic chlorophyllrelations in northern Ozark streams. Can J Fish Aquat Sci 56, 124-130 Lund MA (1998): Are Australian wetlands less productive than Northern Hemisphere wetlands under the same nutrient conditions? Verh Int Ver Theor Angew Limnol 27, 1661-1665 LtmdJWG (1970):Primary production. WatTreat Exam 19, 332-358 Matson PA, Parton WJ, Power AG, Swift MJ (1997): Agricultural intensification and ecosystemproperties. Science 277, 504-509 Mazumder A (1994a): Phosphorus-chlorophyll relationships under contrasting herbivory and thermal stratification: Patterns and predictions. Can J Fish Aquat Sci 51,390-400 Mazumder A (1994b): Patterns of algal biomass in dominant oddversus even-link lake ecosystems. Ecology75, 1141-1149 MazumderA,HavensKE (1998):Nutrient-algae relationships intemperate and tropical lakes. CanJ Fish Aquat Sci 55, 1652-1662 McBride GB, Pridmore RD (1988): Prediction of [chlorophyll-a] in impoundments ofshorthydraulicresidence time: mixing effects. Verh Int Verh Theor Angew Limnol 23, 832-836 McCauleyE, DowningJA,Watson S(1989): Sigmoid relationships between nutrients and chlorophyllamonglakes. CanJ FishAquat Sci46, 1171-1175 Meeuwig JJ, Rasmussen JB, Peters RH (1998): Turbid waters and clarifying mussels: Their moderation of Chl, nutrient relations in estuaries. Mar Ecol Progr Ser 171, 139-150 McGarrigle ML (1993): Aspects ofriver eutrophication in Ireland. Annals Limnol 29, 355-364 Meeuwig JJ, Kauppila P, Pitk~inen H (2000): Predicting coastal eutrophication in the Baltic: a limnological approach. CanJ Fish Aquat Sci 57, 844-855 Mitrovic SM, Hawkins PR, Bowling LC, BuckneyRT, ChengDMH (2000): Low nitrate concentrations in a tidally mixed river coincide with replacement of chlorophytes by the cyanophyte Microcystis. Verh Int Ver Theor AngewLimnol 27, 924-929 Moss B, Hooker I, Balls H, Manson K (1989): Phytoplankton distribution in a temperate floodplain lake and river system. I. Hydrology, nutrient sources and phytoplankton biomass. J Plankton Res 11,813-835 Moss B, BallsH (1989): Phytoplankton distribution in a temperate floodplain lake and river system. II. Seasonal changes in the phytoplanktoncommunities and their control byhydrologyand nutrient availability. J Plankton Res 11,836-867 Moss B, Madgewick J, Phillips G (1996): A guide to the restoration ofnutrient-enriched shallow lakes. Broads Authority, Norwich, UK. 180 pp MyersN (1995): Environmental unknowns. Science 269, 358-360 Nicholls KH, Dillon PJ (1978): An evaluation ofphosphorus-chlorophyll-phytoplankton relationships for lakes. Int Revue ges Hydrobiol 63, 144-154 National Research Council (2000): Clean coastal waters: Understanding and predicting the effects of nutrient pollution. National Academy Press, Washington, DC, USA Nielsen SL, Sand-Jensen K, Borum J, Geertz-Hansen O (2002): Phytoplankton, nutrients, and transparency in Danish coastal waters. Estuaries 25, 930-937 Niirnberg G (1996): Trophic state of clear and colored, soft-and hardwater lakes with special consideration ofnutrients, anoxia, phytoplankton and fish. Lake Reservoir Manage 12, 432-447 OECD (1982): Eutrophication ofwaters: Monitoring, assessment and control. Organisation for Economic and Cooperative Development, Paris, France Paerl HW (1988): Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol Oceanogr 33, 823-847 Paerl HW, Mallin M, Rudek J, Bates P (1990): The potential for eutrophication and nuisance algal blooms in the lower Neuse River, NC. Albemarle-Pamlico Estuarine Study Report 90-15. North Carolina Natural Resources and Community Development, Raleigh, NC

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## Eutrophication Review Articles

Petersen JE, Chen CC, KempWM (1997): Scalingaquatic primary productivity: experimentsunder nutrient- and light-limited conditions. Ecology 78, 2326-2338 Phlips EJ, Aldridge FJ, Hansen P, Zima PV, Ihnat J, Conroy M, RitterP (1993): Spatial and temporalvariability oftrophic state parameters in a shallow subtropical lake (Lake Okeechobee, Florida, USA).Arch Hydrobiol 128,437-458 Piyasiri S (2001): Increasing eutrophy in Kotmale Reservoir, Sri Lanka: A 5-year study. Verh Int Ver Theor Angew Limnol 27, 3604-3607 Portielje R, Van der Molen TT (1999): Relationships between eutrophicationvariables: fromnutrient loading to transparency. Hydrobiologia408/409, 375-387 Postel SL, Carpenter SR (1997): Freshwater ecosystem services, p 195-214. In: GDaily, Ed, Nature's services.Island Press,Washington, DC, USA Prairie YT, Duarte CM, Kalff J (1989): Unifying nutrient-chlorophyllrelationships in lakes. CanJ FishAquat Sci46, 1176-1182 Pridmore RD, Vant WN, Rutherford JC (1985): Chlorophyll-nutrient relationships in North Island lakes (New Zealand). Hydrobiologia 131,181-189 ProulxM, PickFR, MazumderA,HamiltonPB, Lean DRS (1996): Effectsofnutrients and planktivorousfishon the phytoplankton of shallow and deep aquatic systems. Ecology 77, 1556-1572 PrygielJ, Leitao M (1994): Cyanophyceanblooms in the reservoir ValJoly(Northern France) and their development in downstream rivers. Hydrobiologia 289, 85-96 Quir6s R (1998): Trophic cascade effects in a continous series of temperate-subtropicalwaterbodies. Verh Int VerTheor Angew Limnol 26, 2315-2319 Quir6s R (1991): Empirical relationships between nutrients, phyto and zooplankton, and relativefishbiomassin lakes and reservoirs ofArgentina. VerhIntVerTheorAngewLimno124, 1198-1206 Quir6s R (1990): Factors related to variance in residuals in chlorophyll-phosphorus regressions in lakes and reservoirs of Argentina. Hydrobiologia 200/201,343-355 Rabelais N, Nixon SW,Eds (2002): Dedicated issue. Nutrient overenrichment in coastal waters: Global patterns of cause and effect. Estuaries 25(4b), 639-900 RaskM, OlinM, HorppilaJ,LehtovaaraA,V/iis~inenA, Ruuhi~irvi J, SammalkorpiI (2002): Zooplankton and fish communities in Finnish lakes ofdifferent trophic status: responses to eutrophication. Verh Int Vet Theor Angew Limnol 28, 396-401 ReckhowKH, Chapra SC (1983): EngineeringApproaches forLake Management. Vol 1, Data Analysis and Empirical Modeling. Butterworth, Boston, MA, USA Rekolainen S, Pitk/inen H, BleekerA, Felix S (1995): Nitrogen and phosphorus fluxes from Finnish agricultural areas to the Baltic Sea. Nordic Hydrol 26, 55-72 Reynolds CS (1997): Vegetative processes in the pelagic: A model for ecosystem study. Ecology Institute, Oldendorf/Luhe, Germany. 371 pp Reynolds CS (1994): Arephytoplankton dynamics in rivers so different from those in shallow lakes? Hydrobiologia 289, 1-7 Richardson K (1996): Conclusion, research and eutrophication control, p 243-267. In: BBJorgensen and K Richardson, Eds, Eutrophication in Coastal Marine Ecosystems, Volume 52, American Geophysical Union, Washington, DC, USA SakamotoM (1966): Primaryproduction byphytoplanktonin some Japanese lakesand its dependence onlake depth. Arch Hydrobiol 62, 1-28 SalasHJ,Martino P(1991):Asimplified phosphorustrophicstatemodel forwarm-water tropicallakes.WaterResearch25, 341-350 Sarvala J, Helminen H, Karjalainen J (2000): Restoration ofFinnish lakes using fish removal: changes in the chlorophylI-phosphorus relationship indicate multiple controlling mechanisms. Verh Int VerTheor Angew Limnol 27, 1473-1479 Sas H (1989): Lake restoration by reduction of nutrient loading: Expectations, experiences, extrapolations. Academia Verlag, Richarz, St. Augustin, Germany SchefferM (1998): Ecology of shallow lakes. Chapman and Hall, London, UK SchefferM,HosperH,MeijerM-L,MossB,JeppesenE (1993):Alternativeequilibriain shallow lakes.Trends EcolEvol 8, 260-262 Schindler DW (1981): Studies of eutrophication in lakes and their relevanceto the estuarine environment,p 71-82. In: BJNielson and LE Cronin, Eds, Estuaries and Nutrients. Humana Press, Clifton, NJ, USA SchindlerDW (1977): Evolution ofphosphorus limitationin lakes. Science 195, 260-262 Schmidt A (1994): Main characteristics of the phytoplankton of the Southern Hungarian section of the River Danube. Hydrobiologia 289, 97-108 Schramm W (1999): Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. J Appl Phycol 11, 69-78 SeipKL(1994):Phosphorus andnitrogen limitation ofalgalbiomass

across trophic gradients. Aquat Sci 56, 16-28 Seip KL, Jeppesen E, Jensen JP, Faafeng B (2000): Is trophic state
or regional location the strongest determinant for Chl-aFFPrelationships in lakes? Aquat Sci 62, 195-204 Seip KL, Sas H, Vemij S (1992): Nutrient-chlorophyll trajectories

across trophic gradients. Aquat Sci 54, 58-76 Seip KL, Ibrekk H (1988): Regression equations for lake management - how far do they go? Verh Int Ver Theor Angew Limnol 23,778-785 Seip KL, Satoh T (1984): The impact of nutrient load on total biomass and species succession in Lake Suwa, Japan. Verh Int VerTheor Angew Limnol 22, 1142-1149 Sharp JH (2001): Marine and aquatic communities, stress from eutrophication, p 1-11. In: Encyclopedia of Biodiversity, volume 4. Academic Press, New York, USA Shapiro J (1989): Current beliefs regarding dominance by bluegreens: The case for the importance of CO2 and pH. Verh Int VerTheor Angew Limnol 24, 38-54 Shapiro J, Lamarra V, Lynch M (1975): Biomanipulation: an ecosystem approach to lake restoration, p 85-96. In: PL Brezonik andJLFox, Eds, Proceedings ofa Symposium onWater Quality Managementthrough Biological Control. University ofFlorida, Gainesville, FL, USA SimsJT, Simard RR, Joern BC (1998): Phosphorus loss in agricultural drainage: Historical perspective and current research. J Environ Quality 27, 277-297 Sivonen K (2000): Toxic cyanobacteria,p 81-96. In: P Heinonen, Z Giuliano, and A Van der Beken, Eds, Hydrological and Limnological AsPectsofLakeMonitoring. Wileyand Sons,Ltd, West Sussex, England Sondergaard M, Jeppesen E, Jensen JP, Lauridsen T (2000): Lake restoration in Denmark. Lakes Reserv Res Manage 5, 151-159 Smith VH (2001): Blue-green algae in eutrophic fresh waters. LakeLine 21(1), 34-37 SmithVH 

### (1998): Cultural eutrophication ofinland, estuarine, and coastal waters, p 7-49. In: ML Pace and PM Groffman, Eds, Successes, Limitations and Frontiers in Ecosystem Science, Springer-Verlag,New York, USA Smith VH (1990a): Phytoplankton responses to eutrophication in inland waters, p 231-249. In: I.Akatsuka, Ed, An Introduction to Applied Phycology. SPB Academic Publishing, Amsterdam Smith VH (1990b): Effects ofnutrients and non-algal turbidity on blue-greenalgalbiomass inNorth Carolina reservoirs. Lake ReservoirManage 6, 125-131



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## Review Articles Eutrophication

Smith VII, Sieber-DenlingerJ, deNoyelles F,Jr, Campbell S, Pan S, Randtke SJ, Blain GT, Strasser VA (2003): Managing taste and odor problems in a eutrophic drinking water reservoir. J Lake Reservoir Manage (in press) Smith VH, Will~n E, Karlsson B (1987): Predicting the summer peak biomass of four species of blue-green algae (Cyanophyta/Cyanobacteria) in Swedish lakes. Water Resources Bull23, 397-402 SmithVH (1986): Light and nutrient effectson the relative biomass ofblue-green algae in lake phytoplankton. Can J Fish Aquat Sci 43, 148-153 Smith VH (1985): Predictive models for the biomass ofblue-green algae in lakes. Water Resources Bull 21,433-439 Smith VH (1982): The nitrogen and phosphorus dependence of algal biomass in lakes: An empirical and theoretical analysis. Limnol Oceanogr 27, 1101-1112 SmithVII,Tilman GD, NekolaJC (1999): Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100, 179-196 Smith VH, Bennett SJ (1999): Nitrogen, phosphorus supply ratios and phytoplankton community structure in lakes. Arch Hydrobiol 146, 37-53 Soballe DM, Kimmel BL (1987): A large-scale comparison of factors influencing phytoplankton abundance in rivers, lakes, and impoundments. Ecology 68, 1943-1954 SorvalaJ, Helminen H, Karjalainen J (2000): Restoration ofFinnish lakes using fish removal: changes in the chlorophyll-phosphorus relationship indicate multiple controlling mechanisms. Verh Int Ver Theor Angew Limnol 27, 1473-1479 Sutcliffe DW, Jones JG, Eds (1992): Eutrophication: Research and application to water supply. Freshwater Biological Association, Ambleside, United Kingdom Stadelmann TH, Brezonik PL, Kloiber S (2001): Seasonal patterns of chlorophyll a and Secchi disk transparency in lakes of EastCentral Minnesota: Implications for design of ground-and satellite-basedmonitoring programs.J Lake ReservoirManage 17, 299-314 Swedish EPA (2000): Environmental quality criteria: Coasts and

seas. Swedish Environmental Protection Agency Report 5052, Stockholm, Sweden. 138 pp Tanik A, Beler Baykal B, Gonenc IE (1999): The impact of agricultural pollutants in six drinking water reservoirs. Water Sci Technol 40, 11-17 Thornton JA (1980): A comparison of the summer phosphorus loadings to three Zimbabwean water-supply reservoirs of varying trophic states. Water SA 6, 163-170 Traill I (1991): Loch Lomond: A eutrophication study 1987-1989. Clyde River Purification Board Technical Report 96. Scottish Environment Protection Agency, East Kilbride, Scotland TrimbeeAM, Prepas EE (1987): Evaluation oftotal phosphorus as
a predictor of the relative biomass of blue-green algae with emphasis on Alberta lakes. Can J Fish Aquat Sci 4, 1337-1342 UK Environment Agency (1998): Environmental Issues Series - Aquatic eutrophication in England and Wales. UK Environment Agency Consultative Report, December 1998 USEPA (2002): http://www.epa.gov/waterscience/criteria/nutrient/ guidance/index.html US EPA (1996a): Environmental indicators of water quality in the United States, US EPA 841-R-96-02, Office of Water (4503F), US Government Printing Office, Washington, DC, USA USEPA (1996b): National nutrient assessmentworkshop. Proceedings, December 4-6, 1995. US EPA 822-R-96-004, Office of Water, US Government Printing Office, Washington, DC, USA Valiela I, Collins G, KremerJ, Lajtha K, Geist M, Seely B, Brawley J, Sham CH (1997): Nitrogen loading from coastal watersheds to receiving estuaries: New method and application. Ecol Appl 7, 358-380 Valiela I, Tomasky G, Hauxwell J, Cole ML, Cebri~in J, Kroeger; KD (2000): Operationalizing sustainability: Management and risk assessment ofland-derived nitrogen loads to estuaries. Ecol Appl 10, 1006-1023 Van Ginkel CE, Silberbauer MJ, Vermaak E (2000): The seasonal and spatial distribution of cyanobacteria in South African surface waters. Verb Int Ver Theor Angew Limnol 27, 871-878 Van Nieuwenhuyse EE, Jones JR (1996): Phosphorus-chlorophyll relationship in temperate streams and its variation with stream catchment area. Can J Fish Aquat Sci 53, 99-105 Varis O, Fraboulet-Jussila S(2002): Analysisofeutrophication level and critical loads ofLac de Guiers, Senegal. Verh Int Vet Theor Angew Limnol 28, 462--466 Victor R, AIUjaily SR (1999): Waterquality and management strategies of mountain researvoirs in arid northern Oman, p 307- 350. In: MFA Goosen and W Shaaya, Eds Water Management, Purification, and Conservation in Arid Climates, Vol 1. Technomic Publ Co Inc, Lancaster, UK Vitousek PM, Abet J, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman GD (1997): Human alteration of the global nitrogen cycle: Causes and consequences. Ecological Applications 7, 737-750 Vollenweider RA (1992): Coastal marine eutrophication, principles and control, p 1-20. In: RA Vollenweider, R Marchetti, and R Viviani, Eds, Marine Coastal Eutrophication. The Response ofMarine Transitional Systemsto Human Impact:Problems and Perspectives for Restoration. Science of the Total Environment Supplement 1992. Elsevier Scientific, Amsterdam, The Netherlands Vollenweider RA, Rinaldi A, Montanari G (1992): Eutrophication, structure and dynamics of a marine coastal system: results of a ten-year monitoring along the Emilia-Romagna coast (Northwest Adriatic Sea), p 63-105. In:RAVollenweider, R Marchetti, and R Viviani, Eds, Marine Coastal Eutrophication. The Response ofMarine Transitional Systemsto Human Impact:Problems and Perspectives for Restoration. Science of the Total Environment Supplement 1992. Elsevier Scientific, Amsterdam,The Netherlands Vyhnfilek V, Fott J, Kopfi6ek J (1994): Chlorophyll-phosphorus relationship in acidified lakes of the High Tatra Mountains (Slovakia). Hydrobiologia 274, 171-177 Welch EB, Quinn JM, Hickey CW (1992): Periphyton biomass to point-source nutrient enrichment in sevenNew Zealand streams. Water Research 26, 669-675 Will6n E (2000): Phytoplankton in water quality assessment - An indicator concept, p 57-80. In: P Heinonen, Z Giuliano, and A Van der Beken, Eds, Hydrological and Limnological Aspects of Lake Monitoring. Wiley and Sons, Ltd, West Sussex, England Will~n E, Ahlgren G, S6derhielm A-C (2000): Toxic cyanophytes in three Swedish lakes. Verh Int Ver Theor Angew Limnol 27, 560-564 Wilson JG, Ed (1998): Eutrophication in Irish waters. Royal Irish Academy, Dublin, Ireland Winter JG, Duthie HC (2000): Epilithic diatoms as indicators of stream total N and total P concentrations. J NAmer Benthol Soc 19, 32-49 WolffWJ (1993): Netherlands-Wetlands. Hydrobiologia 265, 1-14

Received:August29th, 2002 Accepted: December4th, 2002 OnlineFirst: December 6th, 2002

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