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Eutrophication and environmental policy in the Mediterranean Sea: a review

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Eutrophication and environmental policy in the Mediterranean Sea: a review Michael Karydis & Dimitra Kitsiou Received: 23 November 2010 / Accepted: 24 August 2011 / Published online: 29 September 2011 # Springer Science+Business Media B.V. 2011 Abstract The Mediterranean Sea is a semienclosed basin connected with the open sea mainly through the Strait of Gibraltar. Due to the circulation pattern and the long residence time ranging between 80 and 100 years, the Mediterranean Sea is a sensitive environment to eutrophication pressures. The main body of water of the Mediterranean is characterized by very low nutrient concentrations, and therefore, the Mediterranean is classified among the most oligotrophic (very poor waters in nutrients) seas of the worlds oceans. However, some coastal areas, mainly in the northern part of the basin, receive excessive loads of nutrients from sewage effluents, river fluxes, aquaculture farms, fertilizers, and industrial facilities, showing intense eutrophic phenom- ena with many adverse effects for the marine ecosystem and humans. Various national and international author- ities, in addition to monitoring, have taken legal and administrative measures to mitigate eutrophication trends in the area. The Mediterranean environment is a good paradigm of integration of extensive legal frame- work, scientific knowledge, and administrative practices. The Barcelona Convention, the Mediterranean Action Plan, and European Union Directives on water quality and coastal management, together with scientific infor- mation derived from international research programs in the Mediterranean, provide a sound background for practical actions in eutrophication problems. In the present work, the problem of coastal eutrophication in the Mediterranean is reviewed in connection with public policies of the Mediterranean States based on national and international legislation and scientific knowledge on Mediterranean oceanographyecology and actions co- ordinated by international bodies. These common actions and practices on coastal management are also discussed in relation to the need for sustainable development and protection of the coastal zone in the Mediterranean Sea. Keywords Coastal eutrophication . Water quality . Marine eutrophication policy . Coastal management . Legislation . Marine strategy Introduction The Mediterranean Sea is a basin connected to the Atlantic Ocean through the Strait of Gibraltar; it is a typical evaporation basin and is characterized by an anticlockwise circulation pattern. The residence time of the Mediterranean water masses varies between 80 and 100 years. Although the Mediterranean waters were considered to be in general of good quality, eutrophication problems started emerging in the 1960s, mainly located in coastal areas. Big cities, tourist resorts, and harbors seem to be the major threat for the Mediterranean marine environment. High Environ Monit Assess (2012) 184:49314984 DOI 10.1007/s10661-011-2313-2 M. Karydis (*) : D. Kitsiou Department of Marine Sciences, University of the Aegean, University Hill, Mytilene, Lesvos Island 81100, Greece e-mail: [email protected]
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Page 1: Eutrophication and environmental policy in the Mediterranean Sea: a review

Eutrophication and environmental policyin the Mediterranean Sea: a review

Michael Karydis & Dimitra Kitsiou

Received: 23 November 2010 /Accepted: 24 August 2011 /Published online: 29 September 2011# Springer Science+Business Media B.V. 2011

Abstract The Mediterranean Sea is a semienclosedbasin connected with the open sea mainly through theStrait of Gibraltar. Due to the circulation pattern and thelong residence time ranging between 80 and 100 years,the Mediterranean Sea is a sensitive environment toeutrophication pressures. The main body of water of theMediterranean is characterized by very low nutrientconcentrations, and therefore, the Mediterranean isclassified among themost oligotrophic (very poor watersin nutrients) seas of the world’s oceans. However, somecoastal areas, mainly in the northern part of the basin,receive excessive loads of nutrients from sewageeffluents, river fluxes, aquaculture farms, fertilizers, andindustrial facilities, showing intense eutrophic phenom-ena with many adverse effects for the marine ecosystemand humans. Various national and international author-ities, in addition to monitoring, have taken legal andadministrative measures to mitigate eutrophicationtrends in the area. The Mediterranean environment is agood paradigm of integration of extensive legal frame-work, scientific knowledge, and administrative practices.The Barcelona Convention, the Mediterranean ActionPlan, and European Union Directives on water qualityand coastal management, together with scientific infor-mation derived from international research programs in

the Mediterranean, provide a sound background forpractical actions in eutrophication problems. In thepresent work, the problem of coastal eutrophication inthe Mediterranean is reviewed in connection with publicpolicies of the Mediterranean States based on nationaland international legislation and scientific knowledge onMediterranean oceanography—ecology and actions co-ordinated by international bodies. These commonactions and practices on coastal management are alsodiscussed in relation to the need for sustainabledevelopment and protection of the coastal zone in theMediterranean Sea.

Keywords Coastal eutrophication .Water quality .

Marine eutrophication policy . Coastal management .

Legislation .Marine strategy

Introduction

The Mediterranean Sea is a basin connected to theAtlantic Ocean through the Strait of Gibraltar; it is atypical evaporation basin and is characterized by ananticlockwise circulation pattern. The residence timeof the Mediterranean water masses varies between 80and 100 years. Although the Mediterranean waterswere considered to be in general of good quality,eutrophication problems started emerging in the1960s, mainly located in coastal areas. Big cities,tourist resorts, and harbors seem to be the major threatfor the Mediterranean marine environment. High

Environ Monit Assess (2012) 184:4931–4984DOI 10.1007/s10661-011-2313-2

M. Karydis (*) :D. KitsiouDepartment of Marine Sciences, University of the Aegean,University Hill,Mytilene, Lesvos Island 81100, Greecee-mail: [email protected]

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nitrogen and phosphorus loads from sewage outfallsof big coastal cities, rivers, industrial installations, andlechates from fertilizers stimulate excessive growth ofphytoplankton and phytobenthic organisms, causing anumber of diverse effects for the marine ecosystem andhumans. Although long-term scientific research (UNEP/FAO/WHO 1996; Krom et al. 2010) has shown that themain body of the Mediterranean Sea is in goodcondition, there are coastal areas, especially in enclosedgulfs near big cities in estuarine areas and near ports,where marine eutrophication is a serious threat.

Marine eutrophication was recognized as a problemin 1960s not only through ecological research but alsobecause of problems identified in coastal waterssimilar to the problems already encountered in lakes(Hutchinson 1967). Relevant research during the 1960sand 1970s was limited to urban effluents and organicforms of pollution that enhance eutrophication (NRC1969). During that time, the main scientific interest inmarine pollution issues was focused on heavy metalsand organic pollutants such as dichlorodiphenyltri-chloroethane (DDT) and polychlorinated biphenyls(PCBs). It has been reported that, in the 1970s,publications on marine eutrophication in the journalsMarine Pollution Bulletin and Ambio accounted onlyfor the 2% and 7% of the total number of publications,respectively (de Jong 2006). The BIOSIS AbstractiveService provides the information that the number ofpapers in scientific literature increases significantlyover the last 20 years (Nixon 1995). Negative effectsresulting from nutrient inputs were documented insemienclosed gulfs, coastal areas, estuaries, and sew-age outfalls (EEA 1999). However, it is difficult inlarge marine bodies such as the Baltic and the NorthSea to discriminate between anthropogenic and naturalcauses of eutrophication. On the other hand, variousauthors have supported the view that nutrient inputs ofterrestrial origin increase aquatic productivity, a bene-ficial effect on fisheries and aquaculture. During thattime, much effort was placed on deciding whether thelimiting nutrient was nitrogen or phosphorus (Rytherand Dunstan 1971). The complexity of the nitrogencycle and the well-established view that phosphoruswas the limiting factor in lakes, delayed the answer tothis question; it is known by now that, with only fewexceptions (Krom et al. 1991), nitrogen is the limitingnutrient in the marine environment (NRC 2000). Sincethe 1980s, eutrophication was recognized not simply asa problem of local interest but also as a large-scale

problem. The Group of Experts on the Scientific Aspectsof Marine Pollution (GESAMP) stated that eutrophica-tion was one of the major courses of immediate concernin the marine environment (GESAMP 1990). Sincethen, eutrophication became a concern of internationalbodies and governments in Danish, Swedish, German,and Mediterranean countries. It was decided at the 2ndNorth Sea Conference in 1987 that nutrient input shouldbe reduced by 50% (de Jong 2006).

As early as the 1960s, it was realized that theprotection of the Mediterranean waters should be amultinational effort involving all Mediterranean States.As a result, in 1975, the Mediterranean States andEuropean Economic Community (EEC) adopted theMediterranean Action Plan (MAP). The objectives ofthe MAP were the assessment of water quality, pollutioncontrol, formulation of natural environmental policies,and coastal development in an environmentally friendlyway with better use of marine and coastal resources.MAP policy has been a good paradigm towards theunderstanding of the natural environment and humanpressures that would provide a basis for action. MAPobjectives have also enhanced the involvement ofscientists in administrative aspects. This was addedvalue to policy makers whenever public consensus wasrequired. Specialized scientific duties started emergingsince the 1970s on developing analytical techniques,conducting marine research, performing environmentalquality assessment, and proposing measures for envi-ronmental protection and measures for mitigatingmarine pollution. Scientific collaboration among statemembers increased mobility of scientific and adminis-trative personnel and strengthened solidarity amongMediterranean States in joining efforts for environmen-tal protection; Mediterranean Pollution (MED POL),the main monitoring program in the Mediterranean,is an ongoing effort including the monitoring ofvariables related to eutrophication problems.

Further legislative measures by the EuropeanUnion (EU) such as the Water Framework Directive(WFD), the Urban Waste Treatment Directive, theNitrates Directive, Habitats Directive, and BathingWater Directive (BWD) have provided guidelines andrules for stepwise reduction of coastal marine eutro-phication. In addition, a number of internationalenvironmental programs have been materialized overthe last 30 years: (a) programs from internationalorganizations such as United Nations EnvironmentProgramme (UNEP), IOC, the Blue Plan, and several

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coastal area management programs and (b) EUresearch programs on the Mediterranean environmentsuch as the Physical Oceanography of the EasternMediterranean (POEM), Program for the WesternMediterranean (PRIMO), and MATER (EEA 2001)provided a sound scientific background to supportfurther public policies on marine eutrophication.

The objectives of this paper are to (a) review theproblem of marine eutrophication in the MediterraneanSea: environmental pressures, human impacts, sourcesof marine coastal eutrophication, and the status ofimpacted areas are presented; (b) present the legislativeand administrative framework to address the problem;and (c) describe the implementation of monitoringprograms for the quantitative assessment of eutrophica-tion in Mediterranean coastal areas. The combination ofscientific knowledge, legislative framework, and adop-tion of coastal management practices for protecting thequality of Mediterranean waters are also examined.

The Mediterranean system

Physical description

The Mediterranean, being a semienclosed sea, issurrounded by Southern Europe, North Africa, and theMiddle East coastal zone (Fig. 1). The Gibraltar Strait,connecting the Mediterranean Sea with the Atlantic, isthe main opening of the basin. The Mediterranean Seais also connected with the Black Sea through the Straitsof Dardanelles and with the Red Sea through the man-made Suez Canal since 1889. The main morphologicalcharacteristics of the Mediterranean Sea are given inTable 1. The basin occupies an area of about 2.5 millionkm2; it is about 3,800 km wide from east to west,whereas the north to the south distance varies withlongitude, the widest part (about 900 km) being betweenFrance and Algeria (EEA 1999).The Mediterraneanbasin is divided into two sub-basins through a relativelynarrow opening between Tunisia and Sicily, which is150 km wide with a maximum depth of about 400 m(EEA 1999); each of the two sub-basins is different inresident algal and animal communities, indicating theirrelative isolation. The average depth of the Mediterra-nean is approximately 1,500 m whereas the greatestdepth is 5,267 m and is located at the Matapa Trench,off the SW coast of Peloponese, Greece. The Aegeanand the Adriatic Sea are semienclosed extensions from

the main body of the Eastern Mediterranean. Themaximum depth of the Western basin is 3,731 m locatedsouthwest of the Island of Ponza (Thyrrenian Sea).

The Strait of Gibraltar is approximately 15 km wideand 290 m deep; the Straits of Dardanelles have amaximum width of 7 km and an average depth of 55 m.The length of the Suez Canal is 190 km including theBitter Lakes, the maximum width being 200 m and themean depth 18 m. The shallowest part of the Mediter-ranean is the Northern Adriatic Sea, the maximum depthbeing <200 m. The Mediterranean water masses areinterrupted by big islands; Corsica, Sardinia, and theBalearic Islands in the western part and Cyprus, Crete,and Rhodes in the eastern part. There are about 700smaller islands in the Greek Archipelago.

The Mediterranean Sea has been divided into 10major sub-basins (Cruzado 1985; UNEP 2003b)shown in Fig. 2: I: The Alboran Sea surrounded bySpain, Morocco, and Algeria; II: The Northwesternbasin surrounded by Spain, France, Monaco, andItaly; III: The Southwestern basin surrounded bySpain, Italy, Algeria, and Tunisia; IV: The TyrrhenianSea surrounded by Italy, France, and Tunisia; V: TheAdriatic Sea surrounded by Italy, Croatia, andAlbania; VI: The Ionian Sea surrounded by Italy,Albania, and Greece; VII: The Central basin sur-rounded by Italy, Tunisia, Libya, Malta, and Greece;VIII: The Aegean Sea surrounded by Greece andTurkey; IX: The North Levantine Sea surrounded byGreece, Turkey, Cyprus, Syria, and Lebanon; and X:The South Levantine Sea surrounded by Greece,Lebanon, Israel, Egypt ,and Libya. The area of eachsub-basin as well as the area drained by each sub-basinis provided in Table 2.

Evaporation in the Mediterranean is approximatelythree times greater than freshwater inputs. The deficitis replenished by warm Atlantic water masses flowinginto the Mediterranean through the Strait of Gibraltar.These water masses move eastwards and, as thefreshwater inputs in the eastern part are negligible,salinity increases to the value of 39‰ in the southernpart of the Asia Minor coastal waters. The densesaline water sinks in the Sea of Levantine and returnsto Gibraltar as a deep current. Vertical mixing hasbeen observed for depths varying between 200 and600 m. The circulation pattern in the Mediterranean Seafollows an anticlockwise direction. The residence timeof the Mediterranean water masses varies between 80and 100 years (Turley 1999).

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The surface Atlantic water, already stripped of mostof its nutrient content, does not differ much to thenutrient balance in the Mediterranean. As the watermasses move eastwards, they become even poorer innutrients (Bethoux et al. 1992). Low nutrient concen-trations account for extreme oligotrophic blue waters.This oligotrophy increases eastwards, and a west toeast gradient in phytoplankton concentration has beenreported (Turley 1999). The estimated nitrogen inflow

to outflow ratio is 5.7–1.9 or about 3:1. However, theMediterranean blue waters are also enriched inphosphate which is transferred by the Saharan dustand deposited in the phosphate-deficient waters of thebasin (Krom et al. 1991, 2010).

In spite of the extreme oligotrophic character of theMediterranean in offshore water masses, it is knownfrom both local sampling and satellite images that highlevels of chlorophylls are observed in coastal areas nearriver deltas, lagoons, or large urban areas (UNEP 1999).These waters can get a greenish or brownish color,they lack transparency, and they negatively affectfisheries and near-shore activities.

Although the input of information from the Mediter-ranean countries shows heterogeneity and countriessuch as Albania, Syria, Libya, and Morocco provide aminimal amount of data (UNEP 1999), it is obvious thatthe most eutrophic areas are located in the NorthernMediterranean coasts (Fig. 3). The Gulf of Lion, theAdriatic Sea, and the Northern Aegean seem to be themost affected areas from nutrient inputs.

The Mediterranean climate and climate changes

The Mediterranean climate conditions range betweena subtropical (Northern Africa) and midlatitudeclimate (Southern Europe). Winters are windy, mild,and wet, whereas summer conditions are relativelycalm, hot, and dry (EEA 1999). The transition periods

Fig. 1 Morphological characteristics of the Mediterranean Sea. 1 Strait of Gibraltar, 2 Gulf of Lions, 3 Adriatic Sea, 4 Thyrrenian Sea, 5Northern Aegean, 6 Straits of Dardanelles, 7 Straits of Bosporus, 8 Nile estuarine area

Table 1 Morphological characteristics of the Mediterranean Sea

Morphology of the Mediterranean basin Dimensions

Area (km2) 2,500,000

Average depth (m) 1,500

Maximum depth (m) 5,267

East–west axis (km) 3,800

North–south width (km) 900

Total length of Mediterranean coastline (km) 46,000

Length of island coastline (km) 19,000

Width of Gibraltar (km) ~15

Depth of Gibraltar (m) 290

Strait of Dardanelles (length) (m) 97,000

Maximum width of Dardanelles (km) 7,000

Average depth of Dardanelles (m) 55

Maximum width of the Suez Canal (m) 200

Mean depth of the Suez Canal (m) 18

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from winter to summer (April–May) and fromsummer to winter (September–October) are rathershort to be considered as well-defined seasons. Localenvironmental conditions favor the development ofmicroclimates. Temperatures as low as 5°C can befound in the northern part of the Mediterranean, butalong the Libyan and Egyptian coasts, temperatures ashigh as 50°C are not rare. There is a contrast inrainfalls between summer and winter that becomesmore pronounced from the north to the south andfrom the east to the west. The orography is a crucialfactor not only for the distribution of the rainfalls in thebasin but also for the wind circulation. The strongestwind system is the Mistral and the Etesian winds. The

Mistral is characterized by intense, cold, and dry watermasses blowing during winter down the Rhone valleybetween the Pyrenees and the Alps, reaching the Gulf ofLion and spreading over a large area in the WesternMediterranean sub-basin. The Etesian winds (known asMeltems in Turkish), blow during the summer in theAegean Sea following a gap between the mountains ofthe Balkans and Anatolia.

Climate changes in the Mediterranean have alreadybecome apparent since the beginning of the twentiethcentury; a temperature increase by 2°C has beenobserved in the Southwestern Europe. The same trendhas been noticed in the North Africa. It is characteristicof the climate change that temperature raises more in

Fig. 2 The major sub-basins of the Mediterranean. I Alboran Sea,II Northwestern basin, III Southwestern basin, IV Tyrrhenian Sea,VAdriatic Sea, VI Ionian Sea, VII Central basin, VIII Aegean Sea,

IX North Levantine Sea, X South Levantine Sea. Source: EEA(1999)—modified

Sub-basin Sea area(103 km2)

Drainage area(103 km2)

I Alboran Sea 76 111

II Northwestern basin 270 129

III Southwestern basin 252 311

IV Tyrrhenian Sea 242 112

V Adriatic Sea 131 235

VI Ionian Sea 184 68

VII Central basin 606 1,135

VIII Aegean Sea 202 286

IX North Levantine Sea 111 131

X South Levantine Sea 436 3,010

Table 2 Area and drainagearea of the Mediterraneansub-basins (source of data:Ludwig et al. 2009)

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winter and for the minimum rather than the maximumtemperatures (UNEP 2009). It has also been observedthat the deep circulation of part of the MediterraneanSea has changed recently (Nicholls and Hoozemans1996), although it has not been quite established thatthis is due to climate changes. A 20% drop in rainfallhas also been recorded. The general trend indicatestemperature rise. A temperature increase between 2.2°Cand 5.1°C for 2080–2099 has been estimated. Thepossibility for a temperature rise between 4°C is about50%. The 4°C temperature increase is more likely tooccur in the Sub-Saharan region, whereas an increase of3°C is expected along the northern part of the basin.However, there is still some uncertainty about thesepredictions in spite of the recent improvements in theresolution of the climate models. The impacts areexpected to affect sea level rise, floods, and possiblethreats for the marine and coastal environment. Futureimpacts on eutrophication seem to be due to the sea levelrise and the storms. The sea level rise will impede riverfluxes in the sea and floods will cause uncontrollablenutrient transportation into the marine environment;both phenomena will influence the nutrient regime ofthe basin (UNEP 2003b).

Human pressures

The Mediterranean coastal zone is rather heavilypopulated with upward trends. The estimated populationof the Mediterranean coast in 1960 was about 250

million, increased to 380 in 1990 and 450 million in1997 (EEA 1999). It has been estimated that 37% ofthe population of the countries surrounding theMediterranean basin live on the coastal zone (AMBER1994). The population around the Mediterranean coastsis expected to reach 570 million by 2025 (Baric andGasparovic 1992). Population distribution between thenorthern and southern countries also changes drastically;the population of the northern coasts accounted for twothirds of the total population of the Mediterranean in1950, whereas today there is equality in populationdistribution between the north and the south. Predictionsfor the year 2025 account for one third of the populationof the northern coast and one quarter for the year 2050.Decrease in the birth rate in the northern part of theMediterranean countries is coupled with decrease inmortality rate but improved health care in the NorthernAfrica and the Middle East explains the reversion inpopulation density.

Urbanization increases pressures on the coastalzone: in 1950, rural populations in Lebanon andTurkey were 50% and 60% respectively; thesepercentages have been decreased to 13% and 32%by the year 1965. The number of cities withpopulation over than a million increased, the biggestbeing Istanbul and Cairo.

Tourist industry exercises pressures on the coastalzone since the Mediterranean environment is anattractive destination not only for Northern Europeansbut also from all over the world. Mass tourism started

Fig. 3 Eutrophic areas in the Mediterranean. Source: UNEP/FAO/WHO (1996)—modified

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to develop after the Second World War; the number oftourists in 1990 was estimated at 260 million and about500 million are expected by 2025 according to the BluePlan; 24% of the tourists came from Mediterraneancountries. Local as well as tourist population requiresenormous amounts of agricultural products, transporta-tion services, and consumption of oil. In addition, theamount of sewage, treated or untreated, disposed intothe marine environment increases.

Environmental pressures and eutrophication

Surface water eutrophication due to continental runoffin coastal waters is partitioned into industrial waste(25%), urban sewage (50%), and agricultural activi-ties (25%). Agricultural practices form a nonpointsource of pollution. The runoff water transportsnutrients (in addition to pesticides, heavy metals,and pathogens) that finally reach the sea, enrichingthe coastal system with nitrogen and phosphoruseither in dissolved form or absorbed by suspendedsolids. Agriculture is mostly intensive in the Mediter-ranean countries since about 1960 and the amounts offertilizers seem to increase (UNEP 2003a). Coastalareas as well as large river basins like the Po andRhone basins are subjected to intense cultivation. Theestimated annual minimum agricultural load (exclud-ing Croatia, Egypt, Libya, Malta, and Slovenia) toMediterranean waters is about 1.6 million t year−1 fornitrogen and 0.8 million t year−1 for phosphorus(EEA 2001).

Aquaculture, like urbanization and tourism, is also anexpanding activity showing an increase from 78,000t year−1 in 1984 to 248,000 t year−1 in 1996. However,the impact is still limited and localized (EEA 1999).The estimated fish farming nitrogen load is about 1.8million t year−1 that is almost the same quantity as thenitrogen released from terrestrial farming activities,whereas estimations for phosphorus (0.21 milliont year−1) added to the marine environment is onlyone fourth of the phosphorus released by land erosion(EEA 2001).

Domestic waste is another source of eutrophicationfor the Mediterranean. The magnitude of sewagepollution is not known with accuracy because there isno data for many Mediterranean cities, especially forcities with a population between 10,000 and 100,000inhabitants. A high percentage (about 40%) of thepopulation is not served by sewage treatment units.

However, data from 18Mediterranean countries (UNEP1999) provide an estimate of 260,000 t year−1 fornitrogen and 75,000 t year−1 for phosphorus outflowinto the marine environment.

Eutrophication problems in the Mediterranean

Eutrophication is caused by both regional sourcessuch as urban effluents, industrial discharges, andaquaculture activities as well as transboundary com-ponents such as agricultural runoffs, riverine out-flows, and airborne nutrient deposition. The variablesrelated to eutrophication are influenced by watercirculation, but it is only recently that the generalcirculation pattern has been connected to regionalsources of pollution including eutrophication (UNEP2003a). The growing interest for research in marineeutrophication is illustrated by the increase of thenumber of publications since 1990. A presentation ofthe records of publications on eutrophication main-tained by the Science Citation Index (SCI) Abstract-ing Service is given in Fig. 4. The number ofpublications is limited between the years 1970 and1990, the annual average value being 20 publicationsper year. Only a few (5–10) papers were published peryear on lake eutrophication and sporadic publicationsappeared in marine eutrophication and Mediterraneaneutrophication. Rapid increase in eutrophication stud-ies has been observed since 1970 to date. Thecumulative number of publications on eutrophicationduring 1970–2010 is 10,244: on marine eutrophica-tion 1,642, on lake eutrophication 2,831, and oneutrophication in the Mediterranean only 345. Asimilar trend was also observed based on theinformation retrieved from the Aquatic Science andFisheries Abstracts: Aquatic Pollution and Environ-mental Quality (ASFA-3) during the same period(Fig. 4).

The trophic status in the Mediterranean Sea:an overview

The highly populated coastal zone in the Mediterraneanand the riverine input from a draining area of 1.5 millionkm2 (Ludwig et al. 2009) induce eutrophic trends incoastal areas. The blue offshore waters of the Mediter-ranean have been characterized as extremely oligotro-phic with an increasing tendency for oligotrophy

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eastwards (Turley 1999). Eutrophication and oligo-trophy in the Mediterranean is illustrated as chlorophylldistribution in remote sensing imagery (Fig. 5). Sea-sonal satellite images (2009–2010) with spatial resolu-tion of 4 km show the surface phytoplankton annualcycle. It is observed that the Eastern Mediterranean Sea(EMS) during autumn (Fig. 5a), spring (Fig. 5c), andsummer (Fig. 5d) was ultraoligotrophic, whereasduring wintertime (Fig. 5b), EMS was still the mostoligotrophic area of the basin. The average annualphytoplankton productivity has been estimated to beabout 60–80 g C m−2 year−1 (Psarra et al. 2000) and isalmost half compared to the productivity in otheroligotrophic seas (Krom et al. 2010) such as theSargasso Sea (125 g C m−2 year−1) and the NortheastPacific (120–130 g C m−2 year−1). This is due to thelow nutrient content of EMS; the maximum concen-trations recorded for nitrate were about 6 μM, forphosphate 0.25 μM, and for silicate 10–12 μM, muchless compared to 20, 1.8, and 20 μM, respectively, in

the Atlantic. As the nitrate to phosphate ratio (N/P)is >20 and in deep waters is about 28:1, the EMS hasbeen characterized as the largest phosphorus-limitedbody of water in the global ocean. Although thegeneral scheme of annual phytoplankton blooms isbased on a short bloom during the spring and possiblyto a smaller peak in the autumn (EEA 1999), the majorphytoplankton blooms in EMS occur in winter(Fig. 5b). An explanation has been given by Kromet al. (2005): winter weather patterns consist of shortperiods of cool weather followed by periods of warmerclear weather. The warmer conditions allow phyto-plankton to bloom. This bloom that extends as deep as100 m decreases nutrient concentrations; phosphatelevels of the surface waters decrease to undetectableconcentrations ~20 nM (Krom et al. 2005), whereasmeasurable concentrations of nitrate (0.5–1.5 μM)remain, indicating the phosphorus limitation of EMS.The coastal area of the southeastern part of theMediterranean (Fig. 5) shows clearly eutrophic trends.

Fig. 4 Number of publications related to eutrophication (EUTRO), lake eutrophication (LAKE EUTRO), marine eutrophication (MAREUTRO), and eutrophication in the Mediterranean (MED EUTRO) retrieved from the databases a SCI and b ASFA-3

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Fig. 5 Chlα concentration (in milligrams per cubic meter) for a autumn (September–November) 2009, b winter (December–February)2009–2010, c spring (March–May) 2010, and d summer (June–August) 2010. Source: NASA Aqua MODIS

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Although the River Nile is the major water resource inthe area, its freshwater fluxes are getting limitedbecause of the Aswan Dam and increasing trends inanthropogenic water use in the lower Nile. Eutrophicconditions in the area are mainly induced by thesewage effluents of Kairo and Alexandria. TheNorthern Aegean shows mesotrophic to eutrophictrends. This can be explained by the river inputs fromnorthern Greece and the water inflow from the nutrient-rich Black Sea.

The nutrient regime and primary productivity in theWesternMediterranean Sea (WMS) are relatively highercompared to the EMS. There is limited nutrient supplythrough the Strait of Gibraltar due to different nutrientconcentrations between the Atlantic and Mediterraneanwaters. The surface water entering from the Atlanticcarries nutrients directly available for photosynthesis(EEA 1999) but at low concentrations. The phosphorus(phosphate) concentrations in the inflowing watersranges from 0.05 to 0.20 μM, the nitrogen (nitrate)concentrations being about 1–4 μM, and the silicon(silicate) concentration is about 1.2 μM (Coste et al.1988). The nutrients of the surface layer are reduced asthey propagate eastwards due to mixing with poorbasin water and nutrient use by phytoplankton.However, the primary productivity of the main WMS,away from the coastal areas and influenced by riversand urban agglomerations, is still higher than theprimary productivity in the EMS.

The main coastal areas in the Mediterranean withpermanent eutrophic trends are the Gulf of Lions, theAdriatic, Northern Aegean, and the SE Mediterranean(Nile–Levantine).

A recent work on nutrient and phytoplankton distri-bution along a large-scale longitudinal east–west transect(3,188 km) of the Mediterranean Sea extended over ninestations was published by Ignatiades et al. (2009). Theresults confirmed the oligotrophic character of the areaand the nutrient and chlorophyll gradient characterizedby decreasing concentrations from Gibraltar to the seaof Levantine. Phosphate maxima ranged from 0.05 to0.26 μM, nitrate from 4.04 to 1.87 μM, chlorophyll α(chlα) from 0.96 to 0.39 mg m−3, and primaryproductivity from 0.83 to 0.14 mg C m−3 h−1. Analysisof the phytoplankton community structure showed thatdiatom species were most numerous in the westernstations, whereas dinoflagellates and coccolithophoresdominate in the eastern stations. Reduced phytoplanktonconcentrations were observed in the surface layers of the

Mediterranean waters; among the possible factorsinducing phytoplankton-poor surface layers, the photo-degradation processes seem to be the most significant(Cuny et al. 2002).

Nutrient river discharges to the Mediterranean

The Mediterranean is a semienclosed ocean basin andthe ratio of the drainage area to the sea surface area ishigh; this means that rivers contribute significantly tothe sustainability of primary productivity in the area.The importance of river discharges is strengthenedbecause of the oligotrophic character of the sea: deepMediterranean waters export great amounts ofnutrients to the Atlantic Ocean (Hopkins 1985). Thisexplains the fact that the zones of high productivityare located along the coast, near estuaries as shown bysatellite images (Bosc et al. 2004). River discharges inthe Mediterranean went through quantitative andqualitative changes over the last decades (Ludwiget al. 2009). River water is either used for irrigation orretained in dams. There are also nutrient dischargesinto the rivers due to agricultural activities and urbaneffluents. The characteristics of the 10 largest riversof the Mediterranean Sea according to their annualwater discharge are given in Table 3. An importantcomponent in the Mediterranean water balance andpossible ecosystemic changes is the outflow of theBlack Sea into the Mediterranean. Ten large rivers inthe Black Sea (Danube, Dnieper, Don, Rioni, Kuban,Dniester, Coruh, Kizil Irmak, Sakaya, and Yesil Irmakrivers) carry about 85% of their freshwater into thesea (Jaosvilli 2002). Danube alone accounts for halfthe river discharges into the Black Sea. The overallfreshwater flux in the Black Sea is about 350–400 km3 year−1. Dam construction in the Danube in1970–1972 resulted in retention of silicate (H4SiO4),and therefore, silicate concentrations discharged intothe sea have been halved (Turley 1999). Nitrate inputwas increased sixfold, resulting into a Si/N ratiodecrease from 42 to 2.8 (Turley 1999). This shift innutrient ratios induces the phytoplankton communitysuccession from diatoms to dinoflagellates and coc-colithophores, i.e., species that do not require silica.The dominance of dinoflagellates in silica-deficientwaters could also account for the frequent occurrenceof toxic dinoflagellate blooms.

Total riverine effluents in the Mediterranean areestimated between 400 and 450 km3 year−1, with

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strong negative trends for half or two thirds of theMediterranean rivers. The Nile basin is a water resourcewith an estimated discharge of 89 km3 year−1 at the levelof the Aswan Dam but <5 km3 year−1 riverine fluxesinto the Mediterranean Sea (EEA 1999). This deficit inwater discharges obviously influences the nutrientbudgets in the South Levantine. Similar negative trendsdue to dam construction have been recorded with theEbro River in Spain and the Mouloya River inMorocco. On the contrary, two of the greatest riversin the Mediterranean, the Po and Rhone Rivers, do notshow any negative trends as far as their water dischargesare concerned (Ludwig et al. 2009).

Although the decrease in river fluxes results intonutrient reduction flowing into the sea, additionalinputs of P and N from human activities exceed thenutrient deficiency from natural sources (Smith et al.2003, 2005). Nitrate generally showed moderatespecific fluxes in most cases, indicating that nitrogenenrichments is not a major problem in Mediterraneanwaters (Ludwig et al. 2009). Nitrogen in agriculturalapplications varied between 30 and 70 kg N ha−1, arather satisfactory number compared to 180 kg N ha−1

in the Netherlands (Cruzet et al. 1999). However, highnitrate fluxes were found in the Adriatic Sea and theNorthwestern Mediterranean Sea (French coastalwaters). A steady increase in nitrate fluxes for theRhone, Po, and Ebro rivers was recorded between1970 and 1990, whereas during recent years, adecrease has been observed. Estimates reported onriver fluxes of nitrogen into the sea were 250,000 t

year−1 for the Adriatic Sea and 340,000 t year−1 forthe northern arc of the western basin, i.e., betweenGenoa and Valencia (Vukadin 1992).

Urban wastewater is the main source of phosphoruspollution. A negative concentration gradient observedfrom the north to the south reflects the gradient ofpopulation densities (Cruzet et al. 1999). The increasein phosphate fluxes in Mediterranean rivers was twiceas high as the increase of nitrate fluxes. In the late1990s, phosphate concentrations declined to the early1970s levels. Phosphorus values for the Adriatic Seawere 82,000 and 115,000 t year−1 for the western arc(Vukadin 1992).

Although silica fluxes influence phytoplankton com-munity structure and consequently the foodweb, there isnot much information because silica concentrationmeasurements are not included in monitoring programs;this is because silica itself is not considered as apollutant. The shift of primary production from diatomsto flagellates, often harmful to the ecological equilibri-um, has been stressed by Billen and Garnier (2007).Assessments of silica fluxes are carried out indirectlyby taking into account environmental factors thatcontrol silica dilution and transfer of silica into thesea. The average riverine Si concentration was found tobe about 4 mg l−1 of Si. Fluctuations around this valuewere due to different types of eroded material,retention time in the dam, and different temperatures.It has been estimated that damming of the Nile Riveralone could possibly reduce Si flux into the Mediterra-nean by 100,000 t year−1 (Nixon 1993).

Table 3 Characteristics of the 10 largest rivers of the Mediterranean Sea according to their annual water discharge

River Country Drainage basin (km2) Length (km) Average water fluxes (m3 s−1)

Ebro Spain 80,093 910 426

Rhone France, Switzerland 98,000 813 2,300

Po Italy 74,000 652 1,540

Tiber Italy 17,375 406 267

Adige Italy and Switzerland 12,100 410 200

Neretva Bosnia and Herzegovina, Croatia 10,380 230 341

Drin Albania 15,540 160 222

Evros Greece, Turkey, Bulgaria 53,000 480

Seyhan Turkey 20,600 560 317

Nile Egypt, Ethiopia, S. Sudan, Uganda, Tanzania, Rwanda 3,400,000 6,650 2,830

Atlantic ocean inflow–outflow=1,700 km3 year−1

Black Sea inflow–outflow=164 km3 year−1

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Algal blooms and toxic phytoplankton

The frequency of high biomass bloom occurrence ofphytoplanktonic species has increased over the last20 years (Maso and Garces 2006). A phytoplanktonbloom (also known as a “red tide” due to water colorchanges) has been defined by Maso and Garces(2006) as a sudden increase in the population ofmicroalgae that has encountered suitable conditionsfor growth that together with their adaptive strategiesand the appropriate physical conditions can reachconcentrations of 104–105 cells l−1 during certainperiod of time (commonly 1–3 weeks). Algal bloomsmay cause significant ecological problems concerningthe change of the structure of the biota but can alsothreaten human health if toxic species are involved. Itis now known that toxic events from phytoplanktoncan also result from low concentrations of the toxicspecies. It is, therefore, possible for a toxic event toappear without an algal bloom. Toxic events withalgal concentrations as low as 102–104 cells l−1 havebeen reported (Reguera et al. 1993). Certain phyto-plankton species produce toxic substances as adefense mechanism against herbivores. Most of themare particularly virulent toxins including saxitoxin,brevetoxin, okadaic acid, and domoic acid. Some ofthem are toxic to vertebrates only, whereas others aretoxic to crustaceans mainly shrimps and crabs.Human poisoning after consumption of shellfishcontaining dinoflagellate toxins is well known. Thereare four main categories of toxins according topathologists (Segar 1997); those that cause paralyticshellfish poisoning (PSP), neurotoxic shellfish poi-soning, diarrhetic shellfish poisoning (DSP), andamnestic shellfish poisoning. There is a concern aboutpublic health since the effects from toxic algae onhumans are particularly severe. Blooms of toxicdinoflagellates known as “harmful algal blooms”(HABs) have been reported (Graneli and Turner2008). According to Hallegraeff (1993), the effectson public health and economic impacts of HABs arenow showing signs of a truly global epidemic. Inaddition to deleterious effects to aquatic ecosystems,they also cause beach fouling, oxygen deficiency,clogging of fish gills, and in extreme conditions,oxygen deficiency in deep waters, resulting in massmortality of benthic animals and fish kills. HABshave been recorded over the last 20 years in manyMediterranean coastal areas.

Bravo et al. (1990) have reported significantquantities of Gymnodinium catenatum along theAndalusia coastal area during January–February1989. A large bloom (28,000,000 cells l−1) ofAlexandrium minutum (PSP toxin dinoflagellate) wasfound south of Ebro Delta during May 1989 (Delgadoet al. 1990). The presence of HABs has also beenreported in the French waters; Gymnodinium aerolumsince 1982 and A. minutum since 1988 (Belin et al.1989). Toxic Dinophysis species have also beenobserved in the south coast of France (Lassus et al.1991). A bloom of G. catenatum (PSP group toxins)was recorded at Fysano Lagoon near Naples withalgal concentrations approaching 6,000,000 cells l−1

(Carrada et al. 1988). Recurrent phenomena ofeutrophication observed in the Adriatic Sea increasethe possibility of HABs. The presence of Dinophysishas been reported in the coastal area of Emilia–Romagna (Boni et al. 1992) and Alexandriumtamarensis in the Northern Adriatic Sea (Honsell etal. 1992). There are reports of the occurrence of toxicmicroalgae in five gulfs of the Aegean Sea: SaronikosGulf, Evoikos Gulf, Pagassitikos Gulf, ThermaikosGulf, and Kavala Gulf (Ignatiades et al. 2007). Algalblooms in Saronikos Gulf are connected with thesewage outfall of the metropolitan area of Athens. Abloom of 10,000,000 cells l−1 of Gymnodinium brevein November 1977 has been reported (Pagou andIgnatiades 1990). The average cell concentration of A.minutum in Saronikos Gulf in 2002 was 1.1×103 cellsl-1 and the maximum concentration 6.8×103 cells l-1.In 2003 the average A. minutum values was 2.1×103

cells l-1 and the maximum value 2.2×104 cells l-1

(Ignatiades et al. 2007). The average and maximumabundance of A. minutum in Evoikos Gulf in 2002was 3.3×102 and 3.8×102 cells l−1, respectively, andduring 2003, the A. minutum cell concentrations were9.6×102 cells l−1 (average) and 5.7×103 cells l−1

(maximum).High trophic levels prevailing in the Pagassiti-

kos Gulf favor the development of toxic algalblooms: a red tide was caused by the dinoflagel-late G. catenatum; in eastern part of the gulf, highvalues of A. minutum were observed during 2002and 2003: 3.8×103 and 2.6×104 cells l−1 were theaverage values for 2002 and 2003, respectively, and2.4×104 and 2.1×105 cells l−1 were the maximumvalues during the 2-year sampling period (Ignatiadesand Gotsis-Skretas 2010).

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Occurrence of Dinophysis acuminata has beenreported in Thermaikos Gulf, affecting bivalve pop-ulations when cell concentrations exceeded 10,000cells l−1 (Reizopoulou et al. 2008). DSP due to toxicmussel consumption affected by the presence of highnumbers of D. acuminata were reported in January2000 (Economou et al. 2007). Okadaic acid frommussels in Thermaikos Gulf has been quantified andfound that okadaic acids concentrations reachedmaximum values of 36 μg g−1 in the hepatopancreasof mussels (Mouratidou et al. 2006). Concentrationsof A. minutumin in Thermaikos Gulf during 2002were 1.0×103 cells l−1 (average) and 4.2×103 cells l−1

(maximum) (Ignatiades et al. 2007). In the Gulf ofKavala, the average abundance of A. minutum was2.0×103 cells l−1 and the maximum cell concentrationwas 9.1×103 cells l−1 during 2002. Ignatiades andGotsis-Skretas (2010) in their recent review provide alist of 61 toxic, potentially toxic, and high biomassnuisance species observed in Greek coastal waters.Sixteen of them have caused toxic episodes.

High nutrient values in the Izmir Bay cause recurrentalgal blooms, sometimes containing large numbers of A.minutum approaching 10,000,000 cells l−1 (Koray et al.1992). The coastal waters of Lebanon, with theexception of harbor areas, are characterized as oligo-trophic; however, the presence of A. minutum, Gonyau-lax polyedra, and Dinophysis sp. has been recorded(Lakkis 1991). The same author claims that thesespecies have not caused health problems due to lowconcentrations.

High trophic levels have been observed along thecoastal area of Alexandria, Egypt, mainly near theoutflow of the main arms of the Nile, Rosetta, andDamietta. Eutrophication is more serious near the twoport areas, the eastern harbor and the western harbor.Zaghloul and Halim (1992) have recorded red tidescaused by the toxic dinoflagellate A. minutum in thearea of the eastern harbor. It must be noted that A.minutum was originally found in the Alexandriaharbor and identified by Halim (1960). Informationon toxic microalgae along the coastal areas of Libya,Tunisia, Algeria, and Morocco is scanty. The presenceof potentially toxic species has been reported forsome lagoons in Tunisia and Algeria (UNEP/FAO/WHO 1996). Hallegraeff et al. (2003) have reportedtoxic blooms of Prorocentrum minimum in Thermai-kos Bay, Greece, Alexandrium ssp. in the Alexandriaharbor, and A. minutum in the Bay of Izmir, Turkey.

Species frequently occurring in blooms in the Med-iterranean Sea that have caused toxic episodes aregiven in Table 4.

The N/P ratio

It is well established that the elemental atomic ratioO/C/N/P is 276:106:16:1 occurs in plankton, bothphytoplankton and zooplankton (Parsons et al. 1984).The N/P ratio is known as the Redfield ratio (Redfieldet al. 1963). As this ratio is expressing biomasscomposition, it was assumed that the nutrient concen-trations in seawater in a ratio nearly 16:1 wouldrepresent optimal conditions for plankton growth.Ryther and Dunstan (1971) reported that, althoughthe typical atomic ratio for the ocean can be nearly15:1, it is not so for the eutrophic zone whichrepresents 2% of the ocean volume. The same authorsconcluded that, in surface waters, nitrogen wasdepleted faster than phosphorus and, therefore, nitro-gen was considered as the limiting nutrient in themarine environment. In the Mediterranean, the SouthEast Ionian, Cretan, and Northwest Levantine Seashave shown that nitrate and phosphate levels rangedbetween 0.01–5.00 and 0.00–1.7 μM, respectively(Souvermezoglou et al. 1996). These results indicatethat nitrogen is the limiting factor in offshore waters;a slight tendency that nitrogen was the limiting factorhas also been reported for the Ligurian Sea (Bethouxet al. 1992). Contrary to this, Krom et al. (1991) havesupported the view that primary productivity inthe Eastern Mediterranean is limited by phosphorus.The phosphorus limitation concept in the Mediterra-nean has also been supported by various authors:Chiaudani et al. (1980) and Marchetti (1985) suggestthat phosphorus is the limiting nutrient in the AdriaticSea; Mingazzini et al. (1992) also found that phospho-rus was the limiting nutrient in Emilia–Romagna. It is,therefore, obvious that there is no conclusive evidenceas to the limiting nutrient in the Mediterranean Sea. Ithas been reported (EEA 1999) that several factorsinfluence the nutrient regime in Mediterranean waterson a seasonal basis: nutrient emissions from sedimentresuspension and nutrient inputs from the land aremainly responsible for the seasonal patterns in nutrientconcentrations. Research on phosphorus limitation inalgal cultures (Correll 1998) has contributed to theunderstanding of algal physiology in respect tophosphorus uptake; this situation has not been clarified

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as yet. Concluding on the limited nutrient in theMediterranean is not only a point of pure scientificinterest but it will also be a significant contribution topublic policies if measures are to be taken for mitigatingcoastal marine eutrophication.

Airborne nutrient deposition

The airborne pollutants related to eutrophication arenitrogen oxides (NOx) and phosphorus. These com-ponents can be transported miles from the originalsource. Although there are more data on N depositionthan for P, the estimation of N deposition is difficultdue to the various forms of nitrogen compoundspresent in the atmosphere. Average concentrations ofNO3

− and NH4+ in the Mediterranean rainwater were

36±20 and 30±11 μeq l−1, respectively (UNEP2003b). Information on gaseous forms of nitrogen,N2, NH3, and HNO3 is limited in the Mediterranean.Emissions-based data provided by Mediterraneancountries have been reported by Vestreng and Klein(2002). Total NOx, NH3, and total N emissions havebeen estimated to 1,800, 2,300, and 4,200 kt of nitrogen,respectively, in 1999. Based on data collected during1999, Tarrason et al. (2000) calculated nitrogen

deposition for the Mediterranean sub-basins (Table 5).These data include measurements of NO3

− and NH4+

in dry deposition, wet deposition, bulk deposition, andaerosols. It is obvious from Table 5 that total inorganicnitrogen deposition is much higher in the EasternMediterranean.

The measurements of phosphate depositions in theMediterranean Sea are very limited (Bergametti et al.1992). The atmospheric input of inorganic P was

Table 5 Forms of nitrogen compounds in the Mediterranean sub-basins (kilotons per year) according to Tarrason et al. (2000)

Mediterranean sub-basin Total N

Alboran Sea 5

Northwestern basin 48

Southwestern basin 48

Tyrrhenian Sea 226

Adriatic Sea 196

Ionian Sea 381

Central basin 554

Aegean Sea 460

North Levantine Sea 268

South Levantine Sea 483

Table 4 List of the most frequently occurring toxic species of phytoplankton in the Mediterranean Sea

Species Area Source

Alexandrium catenella Spain, France Vila and Maso (2005); Collos et al. (2009)

Alexandrium insuetum Greece Ignatiades and Gotsis-Skretas (2010)

Alexandrium minutum Spain, Italy, Greece Vila et al. (2005); Leonardi et al. (2006); Figueroa et al.(2008); Ignatiades et al. (2007)

Alexandrium ssp. Spain Sala et al. (2005)

Dinophysis acuninata Greece Ignatiades and Gotsis-Skretas (2010)

Dinophysis caudate Turkey Polat and Koray (2007)

Dinophysis succulus Algeria Illoul et al. (2008)

Dinophysis tripos Turkey Polat and Koray (2007)

Gymnodinium breve Greece Ignatiades and Gotsis-Skretas (2010)

Noctiluca scintilans Greece Ignatiades and Gotsis-Skretas (2010)

Phaeocystis puchetti Greece Ignatiades and Gotsis-Skretas (2010)

Prorocentrum micans Turkey Polat and Koray (2007)

Prorocentrum minutum Greece Ignatiades and Gotsis-Skretas (2010)

Pseudonitzschia calliantha S. Adriatic, Greece Caroppo et al. (2005); Spatharis et al. (2009)

Pseudonitzschia delicatissima Italy (Adriatic) Caroppo et al. (2005)

Pseudonitzschia galaxiae Italy Cerino et al. (2005)

Pseudonitzschia ssp. France, Adriatic, Spain, Tunisia Quiroga (2006); Buric et al. (2008); Quijano-Scheggia et al.(2008); Sahraoui et al. (2009); Loureiro et al. (2009)

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estimated to be about 40 mg P m−3 year−1 in theWestern Mediterranean and 2.0 mg P m−3 year−1 in theEastern Mediterranean. As the soluble part of Pparticles is 30%, it is obvious that the available P inthe marine environment through atmospheric transpor-tation is even less. However, even this small fraction ofP is of high ecological significance in the water body ofthe central part of the basin because there are noalternative sources for P new generation as it happenswith N through the mechanism of nitrogen fixation.

Eutrophication and eutrophic trendsin the Mediterranean: a sub-basin approach

The eutrophication problem of the Mediterranean Sea isinfluenced not only by climate change, land base

sources, atmospheric deposition, and human activitiesbut also by the overall basin topography, communica-tion of the Mediterranean Sea with the Atlantic and theBlack Sea, circulation pattern, as well as biogeochem-ical processes. However, each area (sub-basin) isshowing different trophic characteristics due to anumber of reasons: (a) the topography of the sub-basin, (b) the circulation within the sub-basin, (c) watermass exchange between the sub-basin and the mainwater mass of the Mediterranean, (d) anthropogenicpressures to the sub-basin, and (e) policies implementedin the sub-basin by the bordering countries. Thedistribution of eutrophic sites or sites being at risk tobecome eutrophic is highly heterogeneous (Table 6) notonly due to different economic, developmental, andcultural standards of the Mediterranean countries, but

Table 6 Sites characterized as eutrophic or as being at risk to become eutrophic according to reports from Mediterranean countries(source: UNEP/MAP 2009)

Sub-basin Eutrophic sites in the Mediterranean Basins

I. ALB Alboran Sea Estuaire de Qued Martil a Tetouan (E1), Lagune de Nador (L1),Foce Torrente Lelone (E1), Marinella-Foce Magra (E1)

II. NWE Northwestern basin Fiume Morto [Toscana] (E1), Etangs Palavasiens (L1), L’ Etang de l’ or (L1)

III. SWE Southwestern basin Laguna Coster del Mar Menor (E1)

IV. TYR Tyrrhenian Sea Foce di Sarno (E1), Napoli Piazza Vittoria (E1), Polici Pietrrsa (E1), Fiuicino[Lazio area] (E1), Gulf of Tunis (E2), Lagune Ghar Al Milh (L1),Lagunete Bizerte (L1)

V. ADR Adriatic Sea Drini Bay (E2), Rodoni Bay (E2), Karavasta Bay (E2), Ishmi Estuary (E2),Buna Estuary (E2), Drini Estuary (E2), Semani Estuary (E2), Koper Bay(E1), Rizana Estuary (E1), Seca Shellfish area (E1), Lido Adriano (E1),Cesenatico (E1), Porto Garibaldi (E1), Foglia [Marche area] (E1),Port Lido Nord [Cavallino] (E1), Duino-Baia di Panzano (E1),Porto Nogaro (E1)

VI. ION Ionian Sea Amvrakikos Gulf (E1), Messologi Lagoon (L1), Araxos Lagoon (L2)

VII. CEN Central basin Gulf of Gabes (E2), Estuaire Hergla (E2), Lagune Boughrara (L1),Lagune de Kheniss [Monastir] (L2), Lagune El Biban (L2)

VIII. AEG Aegean Sea Saronikos Gulf (E2), Thermaikos Gulf (E1), Pagassitikos Gulf (E1),Gulf of Kavala (E2), Gulf of Alexandroupolis (E1), ArgolikosGulf (E1), Gulf of Geras (E2), Gulf of Kalloni (E2),Izmir Bay (E1)

IX. NLE North Levantine Sea The south region of Cyprus (E2), the east region of Cyprus (E2),Antelias (E1), Ramlet el Baida (E1), Saida (E1), Port de Pecheet de Plaisance de Lattaquie (E2), Port de commercede Lattaquie (E2), River Al-Kabire Al Chimali estuary(E2), Mersin Bay (E1)

X. SLE South Levantine Sea El Mex (E1), Abu Qir East (E1), Port Said (E1), Abu Qir Bay (E1),Alexandria eastern Harbor (E2), Rashid (E2), Damietta (E2),Wedi Gaza (E1), Gaza Bay (E2)

E1 eutrophic coastal waters, E2 eutrophic coastal waters with a tendency to eutrophication, L1 eutrophic lagoons, L2 lagoons with atendency to eutrophication

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also because of the different information flow from theMember States of theMED POLmonitoring program toUNEP (UNEP/MAP 2009). It is, therefore, necessaryto briefly describe the trophic characteristics andhuman pressures on impacted sites of each sub-basin.

The Alboran Sea

The Alboran Sea is the westernmost sub-basin of theMediterranean Sea where intense hydrodynamic phe-nomena prevail (Ramirez et al. 2005). The circulation inthe Straits of Gibraltar is characterized by a surfaceinflow of Atlantic water relatively poor in nutrients anda deeper outflowing dense Mediterranean water rela-tively rich in nutrients. The exchange flows at the sillare 0.7 Sv (1 Sv=106 m3 s−1) with a net inflow of0.05 Sv. In the NWAlboran Sea, an intense geostrophicfront is generated associated with upwelling eventsinduced by westerlies, frequent along the Spanish coasts(Minas et al. 1991). These upwellings enrich the photiclayer with nutrients, leading to high chlα concentrations(Garcia-Gorriz and Carr 2001). A strong relationshipexists between biological, chemical, and hydrologicalprocesses in the area (Minas et al. 1991). Work onnutrients off the Spanish coasts (Ramirez et al. 2005)showed that nitrate was depleted at the top 20-m layer,whereas phosphate concentrations were ranging be-tween 0.11 and 0.15 μM. The N/P ratio in the upper20 m was less than 16:1, indicating nitrogen deficiency.Nutrient concentrations near the Strait of Gibraltarshowed high variations: nitrate concentrations outsidethe Strait ranged between 0.7 and 2.8 μmol l−1, whereasnitrate concentrations in the upper layer off the Straitwaters were high (up to 3 μmol l−1). On the contrary, inareas inside the Mediterranean, nitrate concentrationsvaried in space and time; this was attributed to theuptake of the very abundant phytoplankton community(Gomez et al. 2000). Phytoplankton (measured as chlα)has been found to follow the pattern of nutrientconcentrations and salinity (Ramirez et al. 2005). Chlαconcentrations in the top 100 m ranged between 0.01and 1.6 mg m−3. The same authors have reported thatchlα concentrations in the chlorophyll maximum layer(between 10 and 20 m) were 0.74±0.37 mg m−3.Recently, an average value of photosynthetic rates(142.38 mg C m−2 day−1) has been recorded in theAlboran Sea (Macias et al. 2009).

Apart from the high productivity which is relatedto hydrodynamic mechanisms and nutrient inputs

from the Atlantic, eutrophication phenomena havebeen located in coastal areas along the Spanish coasts;these have been reviewed in previous reports (UNEP/FAO/WHO 1996) and their main manifestations weretoxic algal blooms. Eutrophication phenomenahave also been reported from the Moroccan coast:urban development along the coastal zone (120inhabitants/km2), followed by industrial and agricul-tural development have caused serious eutrophicationproblems in the Lagune de Nador, the largest lagoon inMorocco.

The Northwestern basin

The Northwestern Mediterranean sub-basin is extendedfrom the Catalan-Balearic Sea (west) to the Ligurian Sea(east). The northern part of the NW sub-basin ischaracterized by cyclonic circulation which extends fromthe Gulf of Genova across the Ligurian Sea and theBalearic basins to the Gulf of Valencia (Estrada 1996).The hydrography of the area is influenced by the islandsCorsica, Sardinia, and Balearis, the shelf slope fronts,and the central dome of the NW sub-basin (Font et al.1988). The inshore water masses of the Catalan Frontare dominated by diatoms, whereas offshore of theCatalan Front, phytoplankton assemblages were domi-nated by coccolithophores (Estrada et al. 1999). Diatomdominance has been associated with herbivores of thefood chain that support the transfer of energy to highertrophic levels, whereas coccolithophores dominanceseems to enhance the microbial food (Wassman 1988).It is interesting that, in the Balearic Sea, the distributionof phytoplankton is closely related with hydrography.The diatom assemblages move seawards and follow thedistribution of the water bodies and the displacement ofthe North Balearic Front (Estrada et al. 1999).

The most eutrophic part of the area is the Gulf ofLions. The Gulf of Lions (Fig. 1) is the coastal regionbetween the Spanish–French border and the RhoneDelta. There are many lagoons along the coastal zonebut industrial activities are limited in the area. The Gulfof Lions has been characterized as the largest marginalsystem of the Mediterranean Sea. The Rhone River isthe most significant source of freshwater, nutrients,and organic matter of terrestrial origin in the area(Mojtahid et al. 2009) where various intense andvariable processes interact (Lefevre et al. 1997).Powerful circulation along the continental slope, deepwater formation, and seasonal stratification have been

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reported (Millot 1990). Stratification of the surfacewaters occurs between April and October, forming alayer 10–20 m thick. The depth of the thermoclineshifts to about 40 m in the open area. The temperaturebelow the thermocline remains constant at 13.5°C,whereas the water temperature in the surface layerranges between 20°C and 25°C. The mean flux of theRhone River is about 1,600 m3 s−1; it has beenreported (Lefevre et al. 1997) that the shape anddirection of the plume are wind-driven. The Liguro–Provençal Current (LPC) originates from the surfacewater of the Atlantic Ocean being 30–50 km wide and100–200 m thick following a cyclonic circulationpattern (Bethoux et al. 1988).

The main source of nutrients causing coastaleutrophication comes from the Rhone basin; an areaof about 95,000 km2 provides to the marine environ-ment 5,000,000 t of suspended solids (Leveau andCoste 1987). Nutrient fluxes into the sea have beenestimated to 76,000 t year−1 of inorganic nitrogenand 8,400 t year−1 of inorganic phosphorus (Costeet al. 1985). The plume of Rhone River is divertedwestwards, influenced by the LPC (Sournia et al.1990). High levels of nutrients in the area causediatom algal blooms during wintertime, whereasdinoflagellates dominate during the summer phyto-planktonic blooms favored by static waters and hightemperature (Perez et al. 1986).

The Gulf of Lions has been divided into four areasbased on hydrological features: (a) The Gulf ofMarseilles: the Rhone discharge in the area seems tohave limited impact. Nutrient concentrations are gener-ally low with a slight increase in winter due to verticalmixing. However, primary production increases 15-foldat the spring bloom (Lefevre et al. 1997); the summerseason is characterized by oligotrophy, the primaryproduction being <50 mg C m−2 day−1. There aresporadic deviations from the above values due to thehydrography of the area: the effect of wind can diluteRhone plume water, increasing the production above20 mg C m−2 day−1 near the surface. The upwellingdue to Mistral induces high production rates (263 mgC m−2 day−1), threefold higher than the surroundingarea which is 7,350 mg C m−2 day−1 (Minas 1968). Theaverage primary production is about 88 g C m−2 day−1

which is a typical value for many Mediterranean coastalareas (Lefevre et al. 1997). (b) The mouth of RhoneRiver and the Plume: constant chlα concentration atabout 1 mg m−3 has been reported relatively unaffected

by the shape and spread of the river plume (Morel andAndre 1991). (c) The dilution area: this area affected bythe dilution of the Rhone River water into theMediterranean Sea is generally characterized by a lowtransparency. Productivity measurements in the areaestimated an annual production to 86 g C m−2 year−1 in1967 and 142 g C m−2 year−1 in 1968 (Lefevre et al.1997). It has also been estimated that 50% of theproduction is new production due to the Rhone Riverand it has been estimated in terms of N–NO3: Tusseauand Monchel (1995) estimated values ranging between48.6×103 and 56.8×103 t of N–NO3 per annum. (d)The southern area: it occupies the largest area of theGulf of Lions and is influenced by the geostrophiccirculation of LPC. The LPC area is poor in nutrientsand primary production is below 200 mg C m−2 day−1.However, within the frontal zone, primary productionvalues as high as 500 mg C m−2 day−1 have beenrecorded (Coste et al. 1977). During the summer, theformation of the thermocline separates the surface layer,showing oligotrophic characteristics: chlα concentra-tion is below 0.2 mg m−3. During the spring, nutrientconcentrations resulting from winter mixing stimulateproduction rates as high as 250 g C m−2 day−1 and chlαvalues about 3 mg m−3 (Coste et al. 1972). Primaryproduction in the southern area is influenced byseasonality in the divergence area, whereas the frontalzone (Sournia et al. 1990) is characterized by constantlyhigh production. The annual primary production in thearea varies between 78 and 106 g C m−2 year−1.

Primary production annual estimates in the Gulf ofLions indicate that there is no significant increase overthe last 30 years (Lefevre et al. 1997); this suggests thatno systematic eutrophication is due to the Rhone Riveroutflow and, therefore, the Gulf of Lions seems to be abalanced ecosystem over a time scale of decades.

There are problems of coastal eutrophication alongthe French and Spanish coasts. Apart from the lagoons(Table 6), there are pressures from coastal citiesalthough all coastal cities have facilities for wastewatertreatment (UNEP/MAP 2009); in France, 62% of thefacilities provide secondary treatment and, in Spain,90% of the facilities provide secondary and tertiarytreatment (UNEP/MAP 2009).

The Southwestern basin

The Atlantic water that enters the Mediterranean Seaknown as Modified Atlantic Water (MAW) favors a

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system of anticyclonic structures not only in theAlboran Sea but also in the Algerian Basin that is thecentral part of the SW sub-basin; MAW results inanticyclonic eddies along the Algerian current pathand lasts between a few months and 3 years (Puillatet al. 2002; Siokou-Frangou et al. 2010). The relativelynutrient-rich incoming surface Atlantic water and thegyres in the Algerian Basin account, to a large extent,for the nutrient regime in the SW Mediterranean sub-basin. However, information on nutrients and phyto-plankton in the offshore waters of the SW Mediterra-nean sub-basin is limited. The limited information onpelagic ecosystems in the Algero–Provençal areamakes difficult the understanding of ecosystem func-tioning and especially the coupling of biological andhydrodynamic processes which are fundamental in thearea (Hafferssas and Seridji 2010; Olita et al. 2011).The Atlantic inflow causes a clear-cut boundary interms of physical and biological properties. Largehorizontal gradients are formed across the current,inducing a gradient in phytoplankton biomass andspecies composition (Hafferssas and Seridji 2010;Moran et al. 2001). The offshore band of the Atlanticcurrent is characterized by high biological productivityfrom the mixing of the MAW and offshore surfaceMediterranean water. Phytoplanktonic growth and chlαconcentrations are, therefore, linked with the interac-tions between these two water masses.

Nutrient concentrations (Table 7) in the area havebeen ranged between 0.03 and 0.25 μM for phosphateand between 0.08 and 4.59 μM for nitrate. Theaverage N/P ratio was 18.5, slightly higher than theRedfield ratio, indicating an equilibrium betweenphosphate and nitrate (Ignatiades et al. 2009). Fieldwork carried out in offshore waters in the Algero–Provençal basin has shown that nutrient concentra-tions in the upper layers were close to the detectionlimit (Lopez-Sandoval et al. 2011). Chlα concentra-tions recorded were <0.5 mg m−3 in the Algero–Provençal stations (Table 8) and primary productivitywas estimated to be 274 mg C m−2 day−1 (Table 9).Similar chlα values in the area have been reported byIgnatiades et al. (2009), the maximum values being0.49 mg m−3 (Table 8). The cell number in the arearanged between 1.2×102 and 5.1×103 cells l−1

and primary productivity rates were 0.01–0.34 mgC m−1 h−1. Phytoplankton community analysis in thearea has shown that 37% of the species were diatomsand 28% of the species were dinoflagellates, indicat-

ing a slight dominance of diatoms. The application ofShannon’s diversity index has shown higher values inthe diversity of diatoms compared to the EasternMediterranean and vice versa for diversity values ofdinoflagellates: the value of 1.5 in the Algero–Provençal area was half the value (3.0) observed inthe Levantine (Ignatiades et al. 2009). Applications ofremote sensing using the Coastal Zone Color Scanner(CZCS) images from the Western Mediterranean(Morel and Andre 1991) indicated that the centralpart of the Algerian Basin was steadily oligotrophic.The average chlα concentration of the upper layerswas 0.25 mg l−1 and the mean annual carbon fixationrate for the Algerian basin was estimated to be about87 g C m−2 year−1. It is obvious that the character ofthe main water masses in the SW Mediterranean sub-basin is rather oligotrophic, but there are eutrophica-tion problems along the coastal zone. The westernsector of the Algerian coastline receives continentalrunoff and has been characterized as highly eutrophic(UNEP/MAP 2009). Eutrophication problems alsooccur along the Tunisian coasts. A total of 36treatment plants are serving 22 cities (some of themdischarging into the central Mediterranean sub-basin).It has been reported that 63% of the wastewater istreated. Effluents from both treated plants anduntreated wastewater from the sewage system aredirectly disposed into the marine environment. TheBizerte Lagoon located in Northern Tunesia covers anarea of about 150 km2 with an average depth of 8 m.Human pressures on the lagoon are urban, agricul-tural, and industrial; the lagoon supports fisheries aswell as aquaculture activities and has been characterizedas eutrophic (Hlaili et al. 2007). Chlα concentrationsrange from 3.05 to 4.52 mg l−1 (Hlaili et al. 2006).High chlorophyll concentrations up to 6.0 mg l−1 havebeen recorded, reflecting high nutrient availability.Diatom blooms of Pseudonitszchia sp. often occur,the genus Pseudonitzschia accounting for 70% ofphytoplankton cells which ranged between 1.5×105

and 11.1×105 cells l−1 during the period 2004–2005(Sahraoui et al. 2009).

The Tyrrhenian Sea

The Tyrrhenian Sea is defined by the west coast of theItalian Peninsula, the northern part of Sicily, the northernpart of Tunisia, and the Eastern coasts of Sardinia andCorsica. It exchanges water masses with the NW

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Mediterranean and the Central Mediterranean sub-basin.There is also a limited exchange with the Southern IonianSea through the Straits of Messina (between Sicily andthe Italian mainland). The Tyrrhenian Sea covers an areaof 203,000 km2 and the central part of the southern zoneis an abyssal plain (>3,000 m depth). The upper layer(200 m) is water of Atlantic origin (MAW), whereas the

intermediate layer (700 m–bottom) is the Mediterraneandeep water (Hopkins 1988; Sparnocchia et al. 1999).The surface layer, which is the most important from thepoint of view of eutrophication, shows seasonalvariability; wind-driven mixing is the main wintercharacteristic followed by strong stratification duringthe summer. The hydrographic pattern is affecting

Table 7 Nutrient concentrations reported in the Mediterranean Sea

Sub-basin Area Nitrate (μM) Phosphate (μM) N/P ratio References

Alboran Sea NW Alboran 1.66–0.75 0.90–2.01 10–13 Mercado et al. (2005)

Northwestern Basin Balearic Sea 0.07–4.40 0.01–0.26 18.0 Ignatiades et al. (2009)

Ligurian Sea 1.7±1.8 (DIN) 0.10±0.20 Pettine et al. (2007)

Ligurian Sea 5.00 0.15 Coste (1987)

Gulf of Lions 1.0–2.00 Cruzado and Velasquez (1990)

Southwestern Basin Central part 0.08–4.59 0.03–0.25 18.5 Ignatiades et al. (2009)

Tyrrhenian Sea N Tyrrhenian 4.9±3.3 (DIN) 0.20±0.20 Pettine et al. (2007)

Sicily (trans. wat) 0.005–4.35 1.8–15.2 Caruso et al. (2010)

Gulf of Naples 0.75 0.09 2.87 Innamorati and Giovanardi (1992)

Tuscany coastal waters 2.96 0.39 7.55 Innamorati andGiovanardi (1992)

Adriatic Sea N Adriatic 8.0±7.9 (DIN) 0.20±0.20 Pettine et al. (2007)

NW Adriatic 3.07±1.36a 0.09 ±0.05a 34.4±9.33 Innamorati andGiovanardi (1992)

Surface water (winter) 2.3±0.7 0.05±0.02 Sokal et al. (1999)

Western coastal 0.3±0.2 0.02±0.02 Zoppini et al. (1995)

NW Adriatic (Feb) 6.88±0.76 0.12±0.44 Giordani et al. (1997)

Ionian Sea Sicily (trans. wat) 0.2–14.3 4.6–23.7 Caruso et al. (2010)

Surface water (winter) 1.3±1.5 0.05±0.05 Sokal et al. (1999)

Northern Ionian (surface layer) 0.5–1.5 21–25 Civitarese et al. (1998)

Northern Ionian (50–200 m layer) 0.5–5.0 0.05–0.22 Civitarese et al. (1998)

Central basin Gulf of Sirteb 0.03–2.61 0.01–0.07 22.0 Ignatiades et al. (2009)

Gulf of Sirtec 0.08–2.40 0.02–0.18 19.7 Ignatiades et al. (2009)

Gulf of Gabes (coastal) 1.45±0.21 0.06±0.02 47.3±17.64 Drira et al. (2010)

Gulf of Gabes (offshore) 1.36±0.23 0.07±0.03 38.7±9.8 Drira et al. (2010)

Aegean Sea SE Aegean 0.25±0.13 0.05±0.04 Ignatiades et al. (1995)

NE Aegean 0.05–1.6 0.02–0.08 Siokou–Frangou et al. (2002)

S Aegean 0.05–2.5 0.02–0.06 Siokou–Frangou et al. (2002)

S Aegean 0.1–1.9 ≈0.05 18–24 Souvermezoglou et al. (1999)

North Levantine Sea SE of Rhodes 0.04–1.87 0.01–0.05 26.3 Ignatiades et al. (2009)

Offshore waters 0.006±0.001 0.004±0.002 Aktan (2011)

Coastal waters 0.040±0.069 0.015±0.009 Aktan (2011)

South Levantine Sea South of Cyprus 0.08–1.57 0.01–0.04 31.0 Ignatiades et al. (2009)

Central part 0.10–1.72 0.01–0.04 25.5 Ignatiades et al. (2009)

Off the Nile 0.03–0.06 Downing (1984)

a N=N/NO3+N/NO2b Station TM5c Station TM6

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phytoplankton seasonality: the area is characterized asoligotrophic with tendency to mesotrophy during thesummer (Claustre et al. 1989; Morel and Andre 1991).

Chlα concentrations in the upper layer (0–100 m)have not shown seasonality, their average values being0.09±0.04 and 0.08±0.4 mg m−3 in December and July2005, respectively (Decembrini et al. 2009). On thecontrary, primary productivity rates differed in the twoseasons, being 0.25±0.08 mg C m−3 h−1 in July and0.65±0.25 mg C m−3 h−1 in December (Decembrini et

al. 2009). Eutrophication phenomena in the TyrrhenianSea are rather episodic and not widespread; possiblesecondary effects (i.e., hypoxia) are not significant.Most of the effects are due to coastal activities and, to asmaller extent, to river discharges. The majority of thecoastal cities in Italy nowadays are served by sewagetreatment plants. Some places in Campania (Foce delSarno, Napoli Piazza Vittoria, and Portici Pietrasta) aresuffering from human pressures due to discharges ofdomestic sewage, industrial wastes, and in some cases,

Table 8 Chlorophyll concentrations and phytoplankton abundance reported in the Mediterranean

Sub-basin Area Chlα (mg m−3) Phytoplankton abundance (cells l−1) References

Alboran Sea NW Alboran Sea −1.60 Ramirez et al. (2005)

NW Alboran Sea 2.05±0.89 Mercado et al. (2008)

W Alboran Sea >1–7.9 Arin et al. (2002)

Northwestern basin Balearic Sea 0.08–0.96 1.5×102–7.5×103 Ignatiades et al. (2009)

Balearic Sea 0.63±0.15 Lopez-Sandoval et al. (2011)

Catalano-Balearic Sea 0.2–1.8 Estrada et al. (1999)

Ligurian Sea 0.7±0.4 Pettine et al. (2007)

Ligurian Sea 3.0 Coste (1987)

Southwestern basin Central part 0.03–0.49 1.2×102–5.1×103 Ignatiades et al. (2009)

Tyrrhenian Sea N Tyrrhenian 0.6±0.4 Pettine et al. (2007)

Gulf of Naples 3.78±2.52 Innamorati and Giovanardi (1992)

Tuscany coastal waters Innamorati and Giovanardi (1992)

Gulf of Tunis 3.9–23.8 3.6×107–3.4×108 Turki et al. (2009)

Adriatic Sea SE Adriatic 7.0×104 Vilicic et al. (2011)

N Adriatic 1.2±1.5 Pettine et al. (2007)

Surface water 0.4±0.3 Sokal et al. (1999)

Western coastal 0.45±0.25 Zoppini et al. (1995)

Ionian Sea Southern Ionian 0.23±0.08 Lopez-Sandoval et al. (2011)

Surface water 0.3±0.1 Sokal et al. (1999)

Central basin Gulf of Sirtea 0.06–0.41 1.4×102–5.1×103 Ignatiades et al. (2009)

Gulf of Sirteb 0.06–0.34 1.7×102–5.1×103 Ignatiades et al. (2009)

Gulf of Gabes (coastal) 0.05±0.05 2.4×103–23.1×104 Drira et al. (2010)

Gulf of Gabes (offshore) 0.03±0.04 1.6×104–1.2×104 Drira et al. (2010)

Aegean Sea SE Aegean 0.07–0.27 6.6×103 Ignatiades et al. (1995)

Cretan Sea (S Aegean) 4.87 Ignatiades (1998)

North Levantine Sea SE of Rhodes 0.08–0.39 1.4×102–1.1×103 Ignatiades et al. (2009)

Offshore waters 0.56±0.40 Aktan (2011)

Coastal waters 0.87±0.69 Aktan (2011)

South Levantine Sea South of Cyprus 0.03–0.22 1.3×102–3.2×103 Ignatiades et al. (2009)

Central part 0.03–0.18 2.1×102–5.3×103 Ignatiades et al. (2009)

Off the Nile Delta 0.84 (avr) Dowidar (1984)

Central part 0.56±0.17 Lopez-Sandoval et al. (2011)

a Station TM5b Station TM6

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agricultural activities. In Lazio, the area of Fiumicino isenriched in N and P from the Tevere River (UNEP/MAP 2009). The Gulf of Tunis is receiving sewageeffluents from the urban area of Tunis, which has causedserious eutrophication problems (UNEP 2009). Nutrientconcentrations were measured in the Gulf of Tunisduring 1993–1995 (Souissi et al. 2000); nitrate concen-trations varied between 0.21 and 0.68 μMand phosphatevalues ranged between 0.13 and 0.60μM. Phytoplanktondistribution has shown a south–west gradient as well as a

north–west gradient. The N/P ratio was generally high,indicating phosphorus limitation. Chlα values rangedbetween 0.05 and 1.15 mg m−3 (Souissi et al. 2000).

The Adriatic Sea

The Adriatic Sea is an elongated north to south basin(800 km long) and 100–200 km wide (Fig. 1). Theconnection to the Ionian Sea is through the Straits ofOtrando, 75 km wide. Most of the area is characterized

Table 9 Primary productivity values measured in the Mediterranean

Sub-basin Area Primary productivity Units References

Alboran Sea 142.38 mg C m−2 day−1 Macias et al. (2009)

Front area 880 mg C m−2 day−1 Lorenz et al. (1998)

Nonfront area 480 mg C m−2 day−1 Lorenz et al. (1998)

Northwestern Basin Balearic 0.01–0.83 mg C m−3 h−1 Ignatiades et al. (2009)

Gulf of Lions 78–106 g C m−2 year−1 Lefevre et al. (1997)

Gulf of Lions 140–150 g C m−2 year−1 Conan et al. (1998)

Ligurian Sea 240–716 mg C m−2

(14 h)−1Vidussi et al. (2000)

Gulf of Lions 60–120 g C m−2 year−1 Cruzado and Velasquez (1990)

Ligurian Sea 2.00 g C m−2 day−1 Coste (1987)

Ligurian Sea 80.0 g C m−2 year−1 Minas et al. (1993)

Southwestern Basin Algerian Basin 186–636 mg C m−2 day−1 Moran et al. (2001)

Algero–Provençal 274 mg C m−2 day−1 Lopez-Sandoval et al. (2011)

Tyrrhenian Sea 398 mg C m−2 day−1 Moutin and Raimbault (2002)

Southern Tyrrhenian 273 mg C m−2 day−1 Decembrini et al. (2009)

Adriatic Sea Southern Adriatic 97.3 g C m−2 year−1 Boldrin et al. (2002)

NE Adriatic 55 g C m−2 year−1 Justic (1987)

NW Adriatic 120 g C m−2 year−1 Justic (1987)

Whole Adriatic Sea 26–70 g C m−2 year−1 Dugdale and Wilkerson (1988)

Western Coastal Adriatic 120 g C m−2 year−1 Zoppini et al. (1995)

Ionian Sea 61.8 g C m−2 year−1 Boldrin et al. (2002)

Eastern Ionian 285.26 g C m−2 year−1 Pagou and Gotsis-Skretas (1990)

Central basin Gulf of Sirtea 0.02–0.17 mg C m−3 h−1 Ignatiades et al. (2009)

Gulf of Sirteb 0.01–0.23 mg C m−3 h−1 Ignatiades et al. (2009)

Central part 304 mg C m−2 day−1 Lopez-Sandoval et al. (2011)

Aegean Sea Northern Aegean 0.62±0.45 mg C m−3 h−1 Ignatiades (2005)

Southern Aegean 0.30±0.21 mg C m−3 h−1 Ignatiades (2005)

Cretan Sea 5.73–7.98 g C m−2 day−1 Gotsis-Skretas et al. (1999)

NE Aegean 221±13 mg C m−2 day−1 Siokou-Frangou et al. (2002)

S Aegean 218±63 mg C m−2 day−1 Siokou-Frangou et al. (2002)

North Levantine Sea SE of Rhodes 0.02–0.14 mg C m−3 h−1 Ignatiades et al. (2009)

All values are based on in situ 14 C measurementsa Station TM5b Station TM6

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by shallow waters, the maximum depth in the NorthernAdriatic being about 70 m. The circulation pattern isimportant because it is influencing nutrient distributionand transport processes as well as phytoplanktonicgrowth. In winter, intense turbulent diffusion andadvective transport are the prevailing conditions (Francoand Michelato 1992). This results in a complete renewalof the Adriatic water mass. However, during the rest ofthe year, stratification of the water masses slow downtransport processes and reduces water mass exchanges. Inthe coastal zone, nutrient drainage creates conditions thatfinally alter the ecosystem structure and function.Phenomena of anoxia of bottom waters have beenreported several times (UNEP 1999). These phenomenaresulted in considerable reduction in benthic popula-tions. Recurring dystrophic episodes have led to thedisappearance of about 15 species of mollusks andcrustaceans. A decrease in the bottom biomass stock ofother species has been observed (Rinaldi et al. 1993);this affects fisheries activities in the Adriatic. There arealso manifestations of blooms characterized as nui-sance. Three basic nuisance categories have beenreported that enhance bloom-forming phytoplanktontaxa: water quality deterioration related to trophicchanges; health hazards; loss of esthetic values andnegative effects on recreational activities. In addition, thehigh concentration of phytoplankton biomass, the re-duced water transparency, and the “smelly waters” due toputrefaction processes make the coastal water unattrac-tive for tourism, bathing, and recreational activities. As aconsequence, these extreme eutrophication problems inthe Adriatic negatively affect the economy of the region.

The Ionian Sea

The Ionian sub-basin is located in the central part of theMediterranean Sea between the Italian and the Balkanpeninsulas. Bordering countries are Italy, Albania, andGreece. It communicates with the Adriatic Sea throughthe Strait of Otranto and with the Tyrrhenian Sea throughthe Strait of Messina. The bathymetry of the Ionian Seafollows a gradient from the Otranto Straits (shallow part,800 m) to the southern part of the sea (near the Gulf ofSirte, Libya), reaching a depth of about 4,100 m. Nearthe west coast of Peloponese (Southern Greece) is thedeepest depression (depression Vavilov), 5,151 m.

Surface water temperature varies between 15°C inwinter and 25°C during the summer, the averagetemperature being about 19°C. Below 100 m depth, the

temperature is about 13°C and does not vary with theseason. Salinity is generally stable at about 38.5%. TheStrait of Otranto is characterized by four main watermasses: (a) the Adriatic surface water, (b) the Ioniansurface water, (c) the Levantine intermediate water (LIW),and (d) the Adriatic deep water, which flows out of theAdriatic Sea, feeding the deep layers of the MediterraneanSea (Civitarese et al. 1998). The Eastern Mediterraneandeep water formed in the Adriatic Sea leaves the Adriaticas a bottom current through the Straits of Otranto andmoves along the deep western boundary of the IonianSea (Robinson et al. 1992). Hydrographic surveys for theentire Eastern Mediterranean Sea have shown that thedominant source of water in the East Mediterranean Seabelow 1,200 m came from the Adriatic (EEA 1999).Estimates of surface waters transformed into deepwater in the Adriatic are 1,500 km3/year (EEA 1999).The intermediate water is flowing throughout theIonian basin. The surface Atlantic water entering theSicily Straits follows a northeastern course in winterbut changes the course to a northward direction in theIonian Sea, forming large meanders during summer-time (Robinson et al. 1992).

The first 50 m of the water column in the IonianSea show a significant variability in nutrient concen-trations. There is an east–west gradient for nitrateranging between 0.5 and 1.5 μM. Deeper zones(50–200 m) show higher concentrations of nitrate(0.5–5.0 μM) and phosphate (0.05–0.22 μM). Highervalues of the N/P ratio (21–25) indicate that excessivenitrogen has originated from the formation of theEastern Mediterranean deep water sites due toselective enrichment of nitrates from land-basedsources (Civitarese et al. 1998). Primary productivityvalues in the NE Ionian Sea have been estimated to be285.26 g C m−3 year−1 (Chiara et al. 2010). Primaryproductivity in the NE Ionian Sea is low andphytoplankton abundance among the lowest in theEastern Mediterranean (Pagou and Gotsis-Skretas1990). Work on nutrients and phytoplankton in thephotic zone of the northern part of the Ionian Sea hasshown average nutrient concentrations of 1.3 μM fornitrate and 0.05 μM for phosphate during winter(February 1994), whereas average concentrations fornitrate and for phosphate during the summer (August1994) were 1.7 and 0.08 μM, respectively; chlαconcentrations were 0.3 mg m−3 for both seasons.Eutrophication problems have been reported in enclosedbays (i.e., Amvrakikos Gulf) and lagoons (Table 6).

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The Central basin

The Central Mediterranean sub-basin is bordered(Fig. 2) by the southern coasts of Sicily, the easterncoast of Tunisia, and the coastline of Libya. The areaextends to the SW part of Crete (Greece). Informationfrom scientific literature regarding coastal marineeutrophication is rather scanty. The Tunisian author-ities conduct monitoring projects on nutrient, phyto-plankton, and harmful algae along the Tunisian coast(UNEP/MAP 2009). However, most of the work hasbeen carried out in the Gulf of Tunis (SW Mediter-ranean). The Gulf of Gabes is the most studied areaalong the eastern Tunisian coastline (Drira et al. 2008;Drira et al. 2010). Relatively high nutrient concen-trations were found along the coastal zone; coastalphytoplankton community was dominated by oppor-tunistic species such as Dictyocha fibula, possibly dueto high nutrient availability of the coastal waters(Drira et al. 2010). In addition, the identification ofeight toxic dinoflagellates has been reported; the toxicmicroalga Karenia c.f. selliformis accounted foralmost 40% of the total toxic dinoflagellate cells.Information from scientific journals on eutrophicationalong the Libyan coastline is lacking (UNEP/MAP2009). However, it is known that 17 coastal citieswith a total population of about 4,062,000 habitats areserved by 16 wastewater treatment plants (UNEP/MAP/WHO 2004). Information is also missing for theIsland of Malta located in the western part of theCentral Mediterranean sub-basin. Pressures on themarine environment of Malta are due to the develop-ment of finfish farming (Stephanis and Divanach 1993)as well as sewage effluents, treated or untreated(UNEP/MAP 2009). However, it was estimated thatfairly shortly all sewage will be treated (UNEP/MAP/WHO 2004). During a survey in Sicilian waters, somepotentially toxic dinoflagellates in the Malta channelhave been recorded (Giacobbe et al. 1995).

Nutrient and phytoplankton regime of the main watermass in the Central Mediterranean is characterized asextremely oligotrophic (Drira et al. 2010; Ignatiadeset al. 2009; Siokou-Frangou et al. 2010). The SE areaof the Central Mediterranean is dominated by the Gulfof Gabes. The hydrodynamic state of the Gulf ofGabes is influenced by the Atlantic water currents andflows in between two layers with similar properties,i.e., high salinity and water density (Drira et al. 2010).A survey carried out during 2005 along a transect

about 180 mi long with 33 coast-to-offshore stationsshowed the oligotrophic character of the area (Driraet al. 2010); average nitrate and phosphate concen-trations (Table 7) in the open sea were 1.36±0.23 and0.07±0.03 μM, respectively. Average chlα concentra-tion was 0.03±0.04 mg m−3 and average phytoplank-ton cell number was 1.60×104−1.2×104. N/P ratiovaried from 14 to 53 (average value, 38.66±9.80),clearly indicating phosphorus limitation. The low chlαconcentrations combined with N/P ratio values muchhigher than the Redfield ratio indicate that this ecosystemis oligotrophic (OECD 1982; Vollenweider et al. 1998).Dinophyceae seem to be a dominant group of thephytoplankton community in the Gulf of Gabes (Driraet al. 2008). Similar results have been reported byIgnatiades et al. (2009) in three offshore sampling sites inthe Central Mediterranean. The authors also estimatedhigh N/P ratios, suggesting higher nitrogen and phos-phorus budget, a characteristic of oligotrophication in theEastern Mediterranean. An integrated survey to study thestoichiometry of C, N, and P along a west to east transectin the Mediterranean (Pujo-Pay et al. 2011) showed verylow values of phosphate, nitrate, and nitrite in the CentralMediterranean. The decreased gradient shown for theabove-mentioned nutrients was not observed for otherphysicochemical parameters. Work on a longitudinaltransect in the Mediterranean Sea during the summerstratification period (Lopez-Sandoval et al. 2011) hasshown very low chlα values in the Central Mediterra-nean, the average value being 0.23±0.08 mg m−3. Allthese data derived from oceanographic surveys coveringthe whole Mediterranean basin lead to the followingconclusions: (a) the Central Mediterranean sub-basin isinfluenced by the Atlantic current which also transfersphytoplanktonic organisms from the Atlantic and theWestern Mediterranean, (b) the trophic character of thearea varies between oligotrophic and extremely oligotro-phic in terms of nutrients and chlα concentrations, (c) theN/P ratio indicates phosphorus limitation in the CentralMediterranean sub-basin, and (d) dinoflagellates form animportant group within the phytoplanktonic community.

The Aegean Sea

The Aegean Sea is the third major sea of the EasternMediterranean, having a volume of 7.4×104 km3

(Stergiou et al. 1997). The Northern Aegean Seacommunicates with the Black Sea through theBosporus Straits, the Marmara Sea, and the Strait of

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Dardanelles (Fig. 1). It is characterized by an irregularcoastline and the presence of many islands, Thasos,Samothraki, Limnos, Tenedos, Imbros, Lesvos, Chios,and Samos being the largest. There are also threeplateaus (Thermaikos, Samothraki, and Limnos) as wellas a deep basin, the North Aegeanwith amaximum depthof 1,600 m and the Chios basin 1,160 m deep. Severalrivers flow in the Northern Aegean: Pinios, Axios,Nestos, Strymon, and Evros are the largest. The maininput of water masses in the Aegean come from the BlackSea water (BSW). The flow of BSW into the Aegean islarger than the subsurface water flow from the NorthernAegean to the Black Sea. The BSW is characterized byrelatively low salinity, varying between 24 and 35 psu.Winter circulation pattern is well known (Theocharis andGeorgopoulos 1993): BSW masses move westwardsand then towards the north and finally southwards alongthe Hellenic mainland. Further circulation of the BSW isinfluenced by the existence of a thermohaline frontbetween Evia and Andros Islands. When the Androsfront disappears, the BSW is split; one water massmoves along the northern part of Cyclades plateau,whereas the other water mass moves southwards intothe Saronikos Gulf. The BSW is moving furthersouthwards and is detected as far as Kithira Straits,south Peloponese (Theocharis et al. 1988).

The hydrodynamics of the southern part of the AegeanSea is influenced by the LIW. LIW is generated in variousareas of the Levantine Basin and the Southern Aegeanduring February and March under specific meteorologicalconditions (Theocharis et al. 1993). LIW water massesmove westward and enter the Aegean Sea through theEastern Straits of the Aegean Arc (Stergiou et al. 1997).On the other hand, the MAW also enters the Aegean Seathrough the Western Straits of the Cretan Arc and can bedetected between 50 and 200 m deep. It must be notedthat intensive vertical mixing takes place in many areas inthe Aegean Sea (Theocharis and Georgopoulos 1993).

The main water mass of the Northern Aegean ischaracterized by low nutrient concentrations (McGill1961); these are significantly lower (about 12 times)compared to the nutrient concentrations in the AtlanticOcean. Recent field work carried out in five stationslocated in the Northern Aegean (Ignatiades 2005)showed also low nutrient concentrations; mean con-centration values for phosphates were 0.03±0.01 μM,for nitrate and nitrite 0.45±0.13 μM, for ammonia0.12±0.05 μM, for silicate 1.67±0.40 μM, and forchlα 0.32±0.17 μg l−1. According to the scaling

proposed by Ignatiades et al. (1992), these nutrientconcentrations characterize oligotrophic or slightlyeutrophic water masses. Similar results were obtainedin primary productivity measurements. Average valuesof 0.62±0.45 mg C m−3 h−1 indicate oligotrophicconditions, as the range for oligotrophy proposed byIgnatiades (2005) varies between 0.30 and 1.97 mgC m−3 h−1. However, many coastal areas have beencharacterized as eutrophic, mainly influenced by riverdischarges. Thermaikos Gulf, located in the NW part ofthe Aegean Sea, is a shallow elongated embayment; thecity of Thessaloniki is located on the northern part ofthe bay. Three rivers flow into the bay along the westerncoast: Axios River, Loudias River, and Aliakmon River.These rivers supply a total freshwater input into the bayvarying between 50 and 350 m3 s−1, depending on theseason as well as the water extraction for irrigation anddam supply. Bathymetry in the region is generally flatwith a depth gradient from 30 m in the northern part to130 m in the south (Lykonis and Chronis 1989).

The Thracian Sea, located on the Eastern part of theAegean, receives the inputs of two major rivers:Strymon River and Nestos River. Strymonikos Gulf isreceiving water fluxes mainly from the Strymon riverwith a meanwater flow of 60m3 s−1 and catchment areaof 21,017 km2 (Stamatis et al. 2001). The gulf isreceiving nutrients from agricultural activities andsewage effluents. It has been reported (Stamatis et al.2001) that total inorganic nutrient concentrationsvaried between 51.8 and 144.3 μg l−1. Chlα concen-tration values varied between 0.24 and 1.6 μg l−1. Thesame authors report that, although the inshore area ofStrymonikos Gulf was eutrophic, the offshore watersof the Gulf could not be characterized as eutrophic.The Nestos River rises from the Bulgarian mountainswith an overall length of 234 km and ends in theNorthern Aegean. Several hydroelectric power damshave been built along the Nestos River interrupting thewater supply. In addition, the river water is used forirrigation and, therefore, water discharges into the seagreatly fluctuate according to the season and demand.During 1998–1999, nutrient concentrations variedbetween 0.03 and 0.05 μM for phosphate, between0.01 and 11.2 μM for nitrate, 0.09–3.22 μM forammonia, and 0.01–0.25 μM for nitrite (Pavlidou et al.2001). The authors concluded that nutrient levels nearthe river outflow indicated rather eutrophic conditions.

The Evros River is the longest river of the BalkanPeninsula after the Danube, with a total length of

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515 km. The Evros estuary is characterized by a delta12 km wide, covering an area of about 100 km2. Theannual mean flow rate is 103 m3 s−1 (Therianos 1974).The gulf of Alexandroupolis is the main recipient ofthe Evros River fluxes and is a relatively shallow area.Nutrient concentrations have been rather high especiallyin Evros’s plume, ranging between 0.12 and 0.25 μMfor phosphate, 0.38 and 2.92 μM for nitrate, 0.07 and0.23 μM for nitrite, and 4.97 and 5.22 μM forammonium. Chlα values ranged from 0.36 to 9.75 μMand phytoplankton abundance ranged from 7.2×104 to1.04×107 cells l−1 (Friligos and Karydis 1988). Thearea was characterized as eutrophic.

Izmir Bay on the Eastern part of the Northern Aegeanis also characterized as eutrophic. The waters of IzmirBay are influenced by the Gediz River and the effluentsfrom Izmir Metropolitan Municipality. The area of thebay is about 500 km2 and the water volume about 11.5billion m3 (Kucuksezgin et al. 2006). Nutrient concen-trations in the outer bay, measured during 1996–2003,ranged between 0.01 and 0.40 μM for phosphate andbetween 0.12 and 2.0 μM for nitrate. Nitrite concen-trations ranged between 0.01 and 0.95 μM. Chlαconcentration ranged between 0.01 and 4.3 μg l−1,whereas nutrient and chlorophyll concentrations in theinner Izmir Bay were much higher, characterizingeutrophic conditions (Kucuksezgin et al. 2006).

The Southern Aegean Sea (Cretan Sea) is even moreoligotrophic than the Northern Aegean. Nutrient deple-tion in the Aegean and the Eastern Mediterranean Seahad been noticed a long time ago (McGill 1961). McGillpointed out that nutrient concentrations in the AegeanSea were 12 times lower than the Atlantic Ocean,8 times lower than nutrient concentrations in theAlboran Sea, and 3 times lower than in the Ionianand Levantine Seas. The chemical characteristicsof the water masses have been investigated bySouvermezoglou et al. (1999). Nutrient concentrationsin the Cretan deep water (CDW), the transitionMediterranean water (TMW) which occupied theintermediate layer of the Cretan Waters, as well asthe surface layer were measured. Nutrient compensa-tion in the CDW by the intrusion of TMWwas found.Nutrient concentrations from the same survey werealso provided by Ignatiades (1998). Nutrient valuesranged between 0.09 and 1.9 μM for nitrate, 0.01 and0.10 μM for nitrite, 0.01 and 0.08 μM for phosphate,and 0.7 and 2.4 μM for silicate, showing theoligotrophic character of the area. The N/P ratio ranged

between 18 and 24 (Table 7), which is higher than theAtlantic Redfield’s ratio (N/P=16), indicating phos-phorus limitation. Seasonal sampling in the SE AegeanSea (off the Island of Rhodes) was also carried outduring 1983–1984 (Ignatiades et al. 1995). The lowestconcentrations were measured during August 1983;average nutrient values of 0.05±0.10 μM for phos-phate, 0.19±0.13 μM for nitrate, 0.04±0.08 μΜ fornitrite, and 0.69±0.46 μΜ for ammonia were recorded.The area was characterized as oligotrophic.

Chlα concentrations in the Cretan Sea ranged between0.10 and 0.11 mg m−3; in the SE Aegean Sea, chlαconcentrations showed significant seasonal variation(0.04–0.25 mg m−3). In the same survey, phytoplanktoncell number ranged between 1.1×103 and 6.3×104; thehighest cell density was observed during the summercruise. Primary productivity values in the Cretan Seawere between 0.094 and 0.128 mg C m−3 h−1 (Ignatiadeset al. 1995). According to Ignatiades (1998), productivityvalues and light attenuation data clearly show that theSouthern Aegean could be classified as the mostoligotrophic areas of the Mediterranean Sea.

The North Levantine Sea

The North Levantine sub-basin extends over theeastern part of the Mediterranean and is bordered bythe southern coasts of Turkey (Asia Minor) and theSyrian and Lebanese coastlines. The western part ofthe North Levantine extends as far as the eastern partof Crete, Greece (Fig. 2). The biggest islands in thearea are Cyprus (eastern part), Rhodes, Kasos, andKarpathos (western part). The circulation pattern inthe area is influenced by the water of Atlantic origin(AW) entering the Straits of Sicily. As the surfacewater mass moves eastwards (driven by wind andother forces), evaporation gradually exceeds precipi-tation and the water mass becomes more saline anddense (Robinson et al. 1992). In the Levantine duringstorm events, the LIW is formed between 200 and500 m depth. LIW circulates and disperses down-wards to depths of a few hundred meters. Althoughthe dominant view for many years was that LIWwas formed in a limited region between Rhodes,Cyprus, and the south coast of Asia Minor, it is nowknown that it occurs over a larger area, involvingprocesses that include gyres (Robinson et al. 1992).The most important is the Rhodes Gyre (NWLevantine Sea), with connective events during winter

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leading to the formation of the intermediate watermasses (Siokou-Frangou et al. 2010). It has also beenconfirmed (Roether and Schlitzer 1991) that thethermohaline circulation consists of a single verticalcell throughout the Eastern Mediterranean flowingthrough the Ionian and Levantine basins.

The circulation pattern described in the previousparagraph greatly affects the nutrient regimes andprimary productivity in the area. The main reason forthe oligotrophic character of the area is that nutrient-depleted surface water flows westwards through theStraits of Sicily; on the other hand, the LIW flows out atintermediate depths (200–500 m) rich in dissolvednutrients, mainly nitrate and phosphate (Krom et al.2010). As there are short periods of cool and wetweather during winter favoring deep water mixing,phytoplankton blooms can take place provided thatmixing is followed by a short period of warm clearweather (Krom et al. 1991). Nutrient and phytoplanktondistribution in NE Levantine was studied by Aktan(2011) during 2007–2008 in both inshore waters (depth<200 m) and offshore environment. Nutrient concen-trations in the open sea were very low: average values of0.006±0.001 μM of dissolved inorganic nitrogen (N–NO3+N–NO2+N–NH4), 0.004±0.001 μM of ortho-phosphates, and 0.003±0.001 μM of silicates wererecorded. Average nutrient concentrations in the inshoreenvironment were 0.040±0.069 μM of N, 0.015±0.009 μM of P, and 0.002±0.001 μM of Si, respec-tively. Chlα values were 0.56±0.40 mg m−3 in theinshore area and 0.87±0.69 mg m−3 in the open sea.Analysis of phytoplankton community structure (105species in total) showed dominance of diatoms in termsof abundance; the most dominant species being thediatom Dactyliosolen fragilissima (>500×103 cells l−1

in total phytoplankton). Thalassionema nitzschioideswas the most frequently occurring diatom. Averagevalues of phytoplankton abundance in the area were187±269 cells l−1 in the coastal waters, indicating theoligotrophic character of the area. Previous nitrogen–phytoplankton studies in the Mediterranean (Ignatiadeset al. 2009) had shown ranges in nutrient concentrationsof 0.04–1.87 μM for N–NO3, 0.01–0.05 μM for P–PO4, and 0.89–4.82 μM for silicates. Average N/P ratiovalue was 26.3 (Table 7), whereas chlα concentrationsranged between 0.08 and 0.39 mg m−3 and primaryproductivity between 0.02 and 0.14 mg C m−3 h−1.

In spite of the general oligotrophic character of theoffshore water masses of the North Levantine, there

are several coastal areas with eutrophication prob-lems. The Mersin Bay (Table 6) is nutrient enrichedby riverine inputs, industrial effluents, and domesticsewage (UNEP/MAP 2009). In addition, algal bloomsof Prorocentrum micans (Eker and Kideys 2000) andof the dinoflagellate Heterocapsa pygmea (Uysalet al. 2003) in the area of the Mersin Bay have beenrecorded. Along the Syrian coast, a population ofabout 1,000,000 habitats is served by septic tanks andsewage systems. Untreated sewage water is dis-charged into the sea through small submarine outfallscausing eutrophication (UNEP/MAP 2009). Althoughthe sites with eutrophication pressures are known(Table 6), no information is found in literaturedescribing coastal marine eutrophication. Similardeficit in scientific information is also encounteredwith the coastal area of Lebanon; the residentpopulation of the coastal cities of Lebanon is about2,500,000 and, although most of the population isserved through sewage systems, only 32% of thepopulation is served by sewage treatment plants(UNEP/MAP/WHO 2004). Literature on eutrophica-tion is lacking and two papers referring to coastaleutrophication induced by sewage effluents (Hardy andJubayli 1976; Taslakian and Hardy 1976) are obsolete.Eutrophication problems in Cyprus are limited as mostof the sewage water is treated and reused (UNEP/MAP/WHO 2004). However, some eutrophicationproblems are connected with fish farm activities;nutrient release from the cages induces marine eutro-phication (Pusceddu et al. 2007).

The South Levantine Sea

The South Levantine is bordered by the south coastsof Lebanon, the Israeli coast, the Egyptian coast, andpart of the Cyrenaica coast of Libya. There are watermass exchanges with the Central and the NorthLevantine sub-basins. The main water mass ofthe South Levantine has been characterized asoligotrophic. Sampling along an east–west transectof 3,000 km across the Mediterranean Sea was carriedout (Pujo-Pay et al. 2011) during the period ofstratification and nutrient distributions were studied.Nutrient concentrations in the area of the SouthLevantine in the biogenic layer (surface layer) were0.01±0.02 μM for phosphate, 0.56±0.88 μM ofnitrate and nitrite, and 0.008±0.008 μM for ammonium,indicating the oligotrophic regime of the area. Nutrient

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ranges in the area reported by Ignatiades et al.(2009) were 0.01–0.04 μM for P–PO4 and 0.10–1.72 μM for N–NO3; chlα ranged between 0.03 and0.18 mg m−3, primary productivity 0.04–0.07 mgC m−3 h−1, and the average value of the N/P ratiowas 25.5, indicating phosphorus limitation. Kromet al. (2005) have also reported depletion ofphosphate and nitrate in the photic zone of theSoutheastern Levantine. They have also reported thatthe phytoplankton community in the open sea wasdominated by nanoplankton and picoplankton, ac-counting for the 80% of the total chlα in the area.The spatial distribution of chlα concentrations werestudied in the Eastern Levantine during 1991 (Yacobiet al. 1995) at almost 95 stations spaced out in a gridand covering most of the South Levantine sub-basin.Chlα concentrations ranged between 9.2 and 430 ng l−1

with an average value of 126±85.6 ng l−1 in the surfacelayer of the water column (200 m deep). The overallaverage chlα value in the same area was 67 ng l−1.Density chlorophyll maxima were located between 90and 110 m, chlα concentrations being 250 ng l−1.Nutrient concentrations ranged from <0.05 to 6.0 μMfor nitrate, <0.01 to 0.28 μM for orthophosphate, and1.0 to 12.0 μM for silic acid. The low chlα values arewithin the range of low chlα concentrations (<1 μg l−1)previously reported by various authors working in theSouth Levantine (Berman et al. 1984; Dowidar 1984;Azov 1986; Abdel-Moati 1990), characterizing ex-tremely oligotrophic waters (Yacobi et al. 1995).

The southeastern part of the Mediterranean isinfluenced by the outflow of the River Nile. The Nileoutflow before the construction of the Aswan Damwas estimated to 90 km2 year−1. The “Nile Stream”was moving eastwards and northward and its effectwas extended far beyond Bayreuth (Halim et al.1967). The nutrient outflow was estimated between 7and 11×103 t of biologically available phosphorus, atleast 7×103 t of inorganic nitrogen, and 110×103 t ofsilica in the Mediterranean coastal waters of Egypt(Nixon 2003). Chlα concentrations in the offshorewater masses beyond the continental edge rangedbetween 0.02 and 0.16 mg m−3. Coastal waterssustain four times higher chlα concentrations; thenearer to the coast, the higher the chlα content of theseawater (Halim et al. 1995). A seasonal peak isobserved during the cold season (December to March),whereas minimal biomass is observed during thesummer. Phytoplankton is dominated by picoplankton

smaller than 3 μm, while microalgae (>20 μm)dominate for short periods. Chlorophyll maxima wereobserved in depths of 50 and 150 m. The coastal areain Egypt suffers from eutrophication (UNEP/MAP2009), especially near the ports of the coastal watersoff Alexandria as well as from the lagoons of the NileDelta. The deterioration of water quality in the areareflects the combination of several factors: (a) largeamount of nutrients from urban, industrial, andagricultural sources (b) long residence time in thelagoons, (c) stratification due to salinity, and (d) highwater temperatures. In the eastern harbor of Alexandria,chlα concentrations as high as 23 mg m−3 (June 1985)have been recorded (Dowidar and Aboul-Kassim1986). Red tides caused by the toxic dinoflagellate A.minutum have been reported (Labib and Halim 1995).Eutrophication problems along the Israeli coast havenot been reported as the impact of urban effluents. Themajor coastal cities are served by wastewater treatmentplans and most of them provide secondary treatment.As 93% of the treated wastewater is reused, it does notappear to be a problem with discharges into the coastalmarine environment (UNEP/MAP/WHO 2004). Thismay be the reason that no serious eutrophicationproblems have been reported in literature along theIsraeli coast.

Eutrophication thresholds and regime shiftsin the Mediterranean Sea

Ecological discontinuities, also known as regimeshifts, can be defined as a sudden change in anyproperty of an ecological system driven by externalperturbations or by the system’s internal dynamics(Muradian 2001); however, the exact mechanism isoften unclear (deYoung et al. 2008). Eutrophication isconsidered as a type of regime shift; in particular,eutrophication of freshwater lakes is a well-knowntype of regime shift caused by the excessive fertiliza-tion of aquatic ecosystems by phosphorus (Carpenter2003). Regime shifts are difficult to analyze sincethey usually involve multiple causes acting at multi-ple scales (Peters et al. 2007). Their prediction andpossible management depends upon their character-istics such as their drivers, scale, and potential formanagement action (deYoung et al. 2008). Driverscan include both natural and anthropogenic compo-nents whose influences are difficult to separate, suchas climate, global warming, or large-scale oscillations

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in the interface of the atmosphere/ocean, introductionof exotic species, and overfishing. Schramm (1999)stated that light and temperature are the key abioticfactors controlling algal growth; however, nutrientloading is one of the most important drivers of regimeshifts in transitional waters.

As far as scale is concerned, Muradian (2001)argued that the most suitable spatiotemporal scale toaddress regime shifts varies broadly, depending notonly on the specific characteristics of the systeminvolved, but also on the dynamics of the environ-mental services provided by the system. Eutrophicationregime shifts are difficult to detect, predict, and managesince they vary not only in scale and drivers, but also ontheir effects on the different components of the marineecosystem.

Ecological discontinuities imply critical values of keyvariables around which the system flips from one state toanother, known as thresholds (Carpenter and Lathrop2008). Definition of the numerical values of thresholdsis not easy and could be arbitrary, since it depends onthe spatiotemporal scale adopted. However, thresholdsare important and should be defined because they allowthe estimation of benefits and costs of alternativeactions, the estimation of risks, the evaluation ofscenarios, and the development of appropriate modelsfor effective ecosystem management.

Various methodologies have been applied to assessregime shifts. Stolte and Graneli (2006) carried outcorrelations of bloom indicators with nutrient concen-trations during different years to detect regime shiftsand determine the thresholds of nutrient levels forharmful algal events in some European coastal waters.Scheffer et al. (2003) developed a model for assessingregime shifts in shallow aquatic ecosystems. Amodeling approach for analyzing regime shifts ofprimary production in shallow coastal ecosystemsand identifying nutrient thresholds causing regimeshifts has been proposed by Zaldívar et al. (2009).The approach was based on previous existing andvalidated models developed for Mediterranean coastallagoons and focused on the analysis of differentscenarios for ecosystems subjected to strong anthro-pogenic pressures. In addition, autoregressive movingaverage models and vector autoregressive modeling,which both require the availability of large ecologicaltime series, have been applied to detect regime shiftsin large marine ecosystems (Mantua 2004). Zaldívaret al. (2008a) presented three case studies of assessing

regime shifts in different marine ecosystems; lakeeutrophication by excessive phosphorus, regime shiftin Ringkobing Fjord, Denmark, and oxygen dynamicsin the Mediterranean coastal lagoon Sacca di Goro inItaly. For the Sacca di Goro coastal lagoon, theydetected the existence of two distinct periods in thecalculated oxygen saturation; the first coincided withthe exponential growth of Ulva and the second wascorrelated with its decay. Dissolved oxygen concen-tration seemed to depend on the hydrodynamicbehavior of the lagoon, which is affected by windspeed and tidal-induced flows. The results indicatedthe existence of a regime shift in the data set afterapproximately 60 days that coincides with the end ofthe Ulva growth phase and the beginning of thedecomposition phase.

Conversi et al. (2010) analyzed and reviewed long-term records of Mediterranean ecological and hydro-climate variables and showed that all point to asynchronous change in the late 1980s. A quantitativesynthesis of the literature (including observed oceanicdata, models, and satellite analyses) guided theauthors to reveal the existence of the MediterraneanSea regime shift at the end of the 1980s. According totheir results, the Mediterranean Sea underwent amajor change during this period that encompassedatmospheric, hydrological, and ecological systems.This change was linked to the shifts that affected theNorth, Baltic, and Black Seas at the same period andwere attributed to a northern hemisphere change. Theauthors argued that these regime shifts could hardlybe considered as a coincidence and that they could beattributed to a larger-scale phenomenon. A review ofthe Mediterranean physical oceanography literatureprovided evidence to support this argument byindicating the existence of peculiar conditions at theend of the 1980s. In fact, based on Demirov andPinardi’s (2002) simulations of the interannual surfaceMediterranean circulation, 1987 appears to be a yearof change for the entire basin surface circulation; from1979 to 1993, they identified two periods, 1981–1987and 1988–1993, which differ in precipitation andwinter wind regimes.

According to Gavrilova and Dolan (2007), shifts inthe Black Sea began with eutrophication from the1960s to the 1980s, followed by blooms of thecarnivorous comb jelly Mnemiopsis in the late 1980sto the early 1990s, and finally de-eutrophication andthe decline of the comb jelly since the mid-1990s.

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Based on their approach, the authors suggested thatabrupt changes in planktonic ecosystems could bedetectable with a very crude metric of planktoncommunity composition lists of apparent species.Molinero et al. (2008) focused on the Ligurian Sea(Northwestern Mediterranean), a generally oligotrophicarea, and showed that large-scale climate forcing hasaltered the pelagic food web dynamics through changesin biological interactions, leading to substantial changessuch as bursts or collapses in zooplankton populations,and finally to a major change around 1987. Theyconcluded that the environmental modifications and theresults provided by their research are indicators of aregime change pointing to a more regeneration-dominated system in the study area. According toBethoux et al. (1990), the anthropogenic influence onthe observed changes in the Mediterranean marineenvironment cannot be underestimated; however, therole of plankton as indicator of climate-driven changesof the marine ecosystem is of major importance.

New technologies used in assessing eutrophicationin the Mediterranean

The contribution of new technologies, especially remotesensing, to marine eutrophication assessment is invalu-able. Ocean color is a unique property, measured fromsatellite sensors, providing information on oceano-graphic parameters from the sea surface to a few tensof meters depth (Maritorena and Siegel 2005). It hasbecome a strong asset of marine studies by supportingthe derivation of synoptic fields of biogeochemicalvariables, including phytoplankton stocks, primaryproduction (Longhurst et al. 1995), and the concentra-tion of particulate organic carbon (Loisel et al. 2002).As a result, surface patterns of phytoplankton biomassdistribution at large spatial scales can become available(Garcia et al. 2005) and near real-time, long-term,synoptic, global estimates of marine eutrophicationtrends can be carried out. Modeling is also of greatvalue in marine eutrophication studies, since it allowsthe exploration of the relationships between causes andeffects and the understanding and simulation of thephysical, biogeochemical, and biological processes andtheir interactions.

Volpe et al. (2007) tried to define the most suitableocean color algorithm in order to assess the opticalproperties of the Mediterranean Sea for estimatingchlorophyll concentrations. They evaluated the uncer-

tainties in the retrieval of satellite surface chlorophyllconcentrations using both regional and global oceancolor algorithms. The results of their research sup-ported the illustration of the spatial distribution ofchlorophyll concentrations in the Mediterranean Seaon high accuracy maps. Furthermore, Mélin et al.(2009) focused on the development and analysis ofmerged series of water, leaving radiances at the scaleof the Mediterranean basin by combining temporallyoverlapping satellite data sets. As a result, a synopticview of ocean color can become available and besubsequently used as input to existent bio-opticalalgorithms for evaluating parameters related to marineeutrophication. Barale et al. (2008) used SeaWiFSdata from 1998 to 2003 to monitor algal bloomingpatterns and anomalies in the Mediterranean basin.They concluded that the spatiotemporal pattern of thechlα field appeared to concur with the Mediterraneangeneral oceanographic climate. In addition, theobserved chlα anomalies proved able to describetrends and “hot spots” of algal blooming. Fontanaet al. (2009) used also SeaWiFS data in order topredict eutrophication events in coastal areas. For thispurpose, they carried out assimilation of SeaWiFSchlorophyll data into a 3D-coupled physical–biogeo-chemical model using a shallow area located in theNorthwestern Mediterranean Sea, the Rhone Delta–Gulf of Fos region, as the case study area. High ratesof primary production in this area are due to nutrientsfrom Rhone River inputs. The described procedurewas found to be extremely useful in assessing thebiogeochemical dynamics of the study area anddevelop accurate surface chlα concentration maps.

Satellite data derived from the Landsat 7 ETM+were used to assess the water quality in the coastalarea of Tripoli (Lebanon). Empirical algorithms forchlα concentration were derived based on thecombination of the satellite data with sea truth datacollected in the study area 6 h before/after the time ofthe satellite overpass (Kabbara et al. 2008). A set ofthematic maps illustrating the spatial distribution ofwater quality parameters in the coastal area of Tripoliwere produced. The results indicated that the areaunder study is exposed to the risk of developingeutrophic conditions. A similar study was carried outin the Haifa Bay (SE Mediterranean) in order toquantify chlα and SPM concentrations in coastal andestuarine waters (Herut et al. 1999). The hyperspectralCompact Airborne Spectrographic Imager was used to

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monitor water quality in a transitional zone frompolluted to clean seawater in Haifa Bay. Maps of thespatial distribution of chlα were developed, clearlyillustrating the eutrophic trends in the study area. Skliriset al. (2010) studied the variability of the Aegean Seaecohydrodynamics, focusing on investigating keyprocesses affecting the spatiotemporal variability ofchlα and SST. They combined SeaWiFS chlα datafrom 1998 to 2005 and analyzed them by applying theEmpirical Orthogonal Function. The combination ofsuch tools can be of great value to studies where longtime series of satellite data are available, in order tomake clear and accurate conclusions.

Crispi et al. (2002) presented a coupled Mediterra-nean ecomodel of the phosphorus and nitrogen cycles.The time series of the modeled results were wellcorrelated with available satellite data from the CZCSsensor. As a result, thematic maps illustrating thespatial distribution of chlα concentrations were pro-duced and further study of the existing trends wascarried out. Petihakis et al. (2009) stated that theirmodel was able to reproduce the full range of scales ofvariability of chlα in the Eastern Mediterranean Sea.

The MerMex Group (2011) carried out an extendedreview on the marine ecosystem’s responses to climaticand anthropogenic forcings in the Mediterranean. Theystate that, in the future, observational strategies shouldbe specially designed in order to calibrate and validatethe models at different time scales and selected sites inthe Mediterranean Sea representative of specificprocesses.

Mediterranean policy on marine eutrophication

Barcelona Convention

The Mediterranean countries adopted in 1976 theconvention for the protection of the Mediterranean Seaagainst pollution known as the “Barcelona Convention”(Table 10). The Convention entered into force on 12February 1978. The objective of the Convention is toreduce pollution in the Mediterranean Sea, protect andimprove the marine environment in the area, therebycontributing to its sustainable development. Theoriginal convention has been modified by amendmentsadopted in 1995. The amended Convention, recordedas the “Convention for the Protection of the MarineEnvironment and the Coastal Region of the Mediterra-

nean” has entered into force in 2004. Among thecommitments of the Member States is the adoption ofmeasures against land-based pollution, protection ofbiological diversity, and pollution monitoring. Land-based sources include outfalls discharging into the sea,indirect discharges through rivers, and nonpoint pollutionthrough runoff. Nutrient fluxes and eutrophication prob-lems are connected with these forms of pollution. Theamended Barcelona Convention has taken into accountthe experience from the MAP, the United NationsConference on Environment and Development held inRio de Janeiro in 1992 as well as the United NationsConvention on the Law of the Sea. The BarcelonaConvention and its protocols, together with the MAP,form part of the UNEP Regional Seas Program.

The Mediterranean Action Plan

The Mediterranean countries and the EU (then EEC)adopted the MAP in 1975 (Table 10). Although theinitial objective of the MAP was to eliminate marinepollution, socioeconomic aspects were taken intoaccount and integrated in coastal zone planning(EEA 1999). The new phase MAP II was approvedin 1995. The objectives focused on sustainablemanagement, reduction of pollutant inputs, andprotection of the coastal zone with the intention toimprove the quality of life. The Environment RemoteSensing Regional Activity Centre’s main task was tocontribute to the understanding of environmentalchanges in the Mediterranean by applying remotesensing techniques. As chlorophyll distributions can beeasily illustrated in satellite imagery, the importance ofthis activity in monitoring eutrophication trends in theMediterranean becomes obvious.

Eutrophication monitoring within the MED POLframework

The MED POL program is the scientific and technicalpart of the MAP. Although the emphasis was placed onoil pollution, heavy metals (mercury, cadmium, copper,and zinc), organohalogen compounds (PCBs andDDTs), and organotins (TBTs), eutrophication was alsoa component of the program. MED POL has beendeplored in four phases differing in their objectives: Themain objective of phase I (1975–1981) was aiming atupgrading technical infrastructure and expertise of thenetwork of institutions involved in the program. The

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second phase (1982–1996) was focused on developingand coordinating national monitoring programs carriedout according to MED POL protocols. Commonmeasures for mitigating pollution were also adopted bythe Member States of the Mediterranean. During thethird phase (1997–2004), the emphasis of MED POLobjectives were shifted to pollution control; thisobjective was implemented through a number ofactions: (a) the assessment and quantification of allland-based sources as well as uses of marine coastalwaters (b) to support efforts of Mediterranean countriesto implement plans for limiting pollution mainly fromland-based sources (c) to monitor the implementation ofthe above action plans. MED POL has already enteredphase IV; this phase was approved in December 2005 bythe 14th Ordinary Meeting of Contracting Parties to theBarcelona Convention (UNEP/MAP 2009). The mainobjective is now ecosystem quality; how it is impactedby human activities as well as the implementation ofintegrated management practices by the contractingparties. The short-term monitoring applied duringphases I–III, with emphasis to chemical parametersreferring to nutrient loads, does not provide informa-tion on any effects on ecosystem structure and functionespecially as far as the nutrient effects are concerned. Itwas, therefore, realized that the emphasis should beplaced on water quality and biological monitoring(UNEP/MAP 2009). In addition to mandatory varia-bles (Table 11) including some physical variables,nutrient concentrations, and phytoplankton variables, anumber of supplementary variables was also suggested.These include suspended particulate matter, totalorganic carbon (TOC), water color, biomass of eachphytoplankton species, total phytoplankton biomass,total zooplankton biomass, number of neustoniccopepods and number of polychaeta larvae, averagebiomass of jellyfish–ctenophore species, and totalprimary production of macrophytes (UNEP 2003a).Most of the supplementary variables are particularlyimportant in coastal areas where eutrophication phe-nomena are far more pronounced in the benthic systemrather than the water column (Zaldívar et al. 2008b).

The Mediterranean countries involved in the MEDPOL monitoring program differ in the quality of theirresearch facilities, the expertise of their scientificmanpower, and the availability of national funds tocarry out monitoring. This situation does not producegood quality of data: analytical equipment is obsoletein many laboratories and needs replacement (EEAT

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Environ Monit Assess (2012) 184:4931–4984 4961

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2001) and there is always a problem concerning thereliability of the measurements in spite of theintercalibration exercises carried out among theparticipants. There are also many geographical gapsin regional databases. Station locations are changed;new stations are added, moved, or canceled (Fig. 6).As the program is materialized at a multinational scale(more than 20 Mediterranean countries participate),the number and severity of impacted sites depends onthe reports submitted to UNEP from the MemberStates. The sites have been classified into fourcategories: (a) eutrophic coastal sites, (b) coastal siteswith a tendency to eutrophication, (c) eutrophiclagoons, and (d) lagoons with a tendency to eutrophi-cation. Table 6 provides information on the Mediter-ranean sites reported for eutrophic problems or trends.

Complex indices and methods for assessingeutrophication

A working group of MED POL experts has stressedthe importance of ecological indices for describing

and integrating community structure and function(UNEP/MAP 2009). An extensive review on ecolog-ical indices with special reference on aquatic ecosys-tems and pollution effects has been given byWashington (1984). A review on eutrophicationassessment (Karydis 2009) focuses on ecologicalindices suitable for describing marine eutrophication.A number of more complex indices describingecosystem integrity are also provided. Recently, aEuropean Commission task group evaluated the mainmethodologies (Ferreira et al. 2011) that could beused for coastal marine eutrophication assessment inEuropean waters within the scope of the EuropeanMarine Strategy Framework Directive (MSFD-2008/56EC). The group emphasized the need for integratedapproaches that would incorporate the physical,chemical and biological components of the coastalsystem; both pelagic and benthic symptoms ofeutrophication should also be combined. This leadsto the use of more complex indicators with numerousbuilt-in ecosystemic variables. Table 12 provides a listof indices used for eutrophication assessment in theMediterranean waters. Among the indices listed inTable 12, the Trophic Index (TRIX) is the mostwidely used in Mediterranean waters over the last10 years (Primpas and Karydis 2010). This index wasdeveloped to assess the trophic status in the AdriaticSea (Vollenweider et al. 1998) and soon wasimplemented in the national legislation of Italy forprotecting water quality (Parlamento Italiano 1999).Although the use of TRIX for the whole Mediterra-nean has been recommended at a MED POL nationalcoordinators meeting in Athens (UNEP 2003a), thereis skepticism concerning the index use in watermasses characterized by different hydrographic andreference conditions (Painting et al. 2005). In addi-tion, it not compatible to the European WFD 2000/60/EC (EC 2000) as the index incorporates watersquality variables (nutrients) and ecological variables(chlorophyll as a proxy for phytoplankton biomass).

An index specialized to evaluate trophic status intransitional aquatic environments in Mediterraneanwaters has been proposed by Giordani et al. (2009).This index known as Transitional Water Quality Index(TWQI) was developed using six variables: (a)dissolved oxygen, (b) phytoplankton chlorophyll(chlα), (c) dissolved inorganic nitrogen, (d) dissolvedinorganic phosphorus, (e) concentration/coverage ofbenthic communities, and (f) opportunistic macroalgal

Table 11 Mandatory variables used for monitoring eutrophicationwithin the MED POL framework (UNEP 2003a)

Variable Units

Physical variables

Temperature °C

Transparency

Salinity psu

Dissolved oxygen ml l−1

Chemical variables

pH

Orthophosphate μg-at PO4 l−1

Total phosphorus μg-at P l−1

Silicate μg-at SiO2 l−1

Nitrate μg-at NO3 l−1

Nitrite μg-at NO2 l−1

Ammonium μg-at NH4 l−1

Total nitrogen μg-at N l−1

Biological variables

Chlorophyll α μg l−1

Phytoplankton—total abundance cells l−1

Phytoplankton—abundance of major groups cells l−1

Phytoplankton—dominant speciesa

Remote sensinga

a As revised in 2007 (UNEP/MAP 2007)

4962 Environ Monit Assess (2012) 184:4931–4984

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species. These variables are a combination of causaleffects (inorganic nutrients), key biological components(photosynthetic organisms), and indicator effects ofeutrophication (dissolved oxygen). TWQI was foundsuitable for eutrophication assessment in transitionalwaters where primary productivity is mainly controlledby benthic vegetation rather than phytoplankton. Fromthis point of view, TWQI accomplishes the potentialityof TRIX: TRIX seem to be suitable for areas dominatedby marine phytoplankton, whereas TWQI is morerepresentative of shallow coastal areas dominated byrich phytobenthic communities. A review on indicatorson Mediterranean transitional aquatic ecosystems hasbeen given by Zaldívar et al. (2008b).

The Statistical Trophic Index proposed by Ignatiades(2005) had limited use so far; however, it was recentlyrecommended by the EU group of experts (Ferreira etal. 2011). The popularity of the Integrated Phytoplank-ton Index and Eutrophication Index of Table 12remains to be proved as they have been publishedrecently; however, they have been designed forassessing eutrophication in Mediterranean waters.

Integrated methods on eutrophication assessment:a step towards coastal management

The global dimension of the eutrophication phenom-enon and the complex interactions between humanpressures and ecosystem response require a moreintegrated approach that eutrophication should beconsidered as a component of more complex process-es (Duarte 2009a, b; Kitsiou and Karydis 2011). InFig. 7, the interaction between the assessment ofenvironmental quality and science/policy develop-ment focusing on the limitation of coastal marineeutrophication is presented. Although complex as-sessment methods have rarely been applied in theMediterranean (Ferreira et al. 2009), they form apowerful tool for decision making and implementationof coastal management practices as a result of integratedmethodology.

A promising method is the Assessment of Estua-rine Trophic Status (ASSETS); this procedure pro-vides a ranking of different eutrophic areas but alsomeans to address management options. The methodhas been applied in many estuaries of the UnitedStates and EU (Ferreira et al. 2007). The method isdescribed in detail by Bricker et al. (2003) and theconcepts underlining this approach are based on theT

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Environ Monit Assess (2012) 184:4931–4984 4963

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United States Estuarine Eutrophication Assessment(NEEA). The NEEA approach combines the OverallEutrophic Condition Index (expressing the state of theenvironment) with the Overall Human Influence(expressing pressure) and assesses the response(Determining Future Outlook). This approach isfurther extended by applying modeling to get anestimate of pressure induced by nutrients of anthro-pogenic origin. In addition, relational databases,Geographical Information Systems (GIS) and Statis-tical Criteria are used to quantify the trophic state(Bricker et al. 2003). ASSETS uses a simple model

suitable for estuarine as well as coastal systems(Bricker et al. 2003):

dMw

dt¼ Min þMef �Mout þMex

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CB

A

D

Fig. 6 Main station locations of the MED POL program. Source: UNEP (2003a)—modified

4964 Environ Monit Assess (2012) 184:4931–4984

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per second), and Mex is the nutrient exchange betweenthe ocean and the coastal system due to dispersion (inkilograms per second). Among the parameters required,macroalgae are determined heuristically, while sub-merged aquatic vegetation is determined by estimatingspatial coverage. Chlα and HABs are determined bystandard laboratory techniques. Among the requiredvariables, macroalgae are determined heuristically,

while submerged aquatic vegetation is determined byestimating spatial coverage. Chlα and HABs are deter-mined by standard laboratory techniques.

The countries bordering the Baltic Sea havedeveloped the HELCOM Eutrophication AssessmentTool (HEAT) method which is an integrated indica-tor’s base eutrophication assessment tool (HELCOM2009). HEAT is a composite assessment tool integrat-

Fig. 7 Interaction between the assessment of environmental quality and science/policy development focusing on the mitigation of coastalmarine eutrophication

Environ Monit Assess (2012) 184:4931–4984 4965

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ing eutrophication standard to the pressures on themarine environment; this holistic assessment usesbiological indicators including chlα, primary produc-tion, seagrass, benthic invertebrates, harmful algae, andmacroalgae (Ferreira et al. 2011).

The OSPAR organization has adopted a set ofEcological Quality Objectives (EcoQOs) as a tool forecosystemic approach as well as for the managementof human activities; the EcoQOs is aiming (a) tomitigate the anthropogenic effects and (b) to definethe desired quality of the coastal marine environment(OSPAR 2009). The variables used in EcoQOs arechlα concentrations, macroalgae, seagrass, and phy-toplankton indicator species.

An integrated procedure within the OSPAR frame-work known as Compehensive Procedure has beendeveloped for assessing eutrophication (Claussen et al.2009). The method discriminates three water types: (a)nonproblem areas (clean waters), (b) potential problemareas (unclassified waters due to a deficit in scientificinformation), and (c) problem areas (nutrient-richwaters or waters affected by transboundary nutrienttransport). The method uses chlα, macroalgae, sea-grass, and phytoplankton indicator species (biologicalcomponents) as well as water transparency measure-ments and nutrient concentrations (physicochemicalindicators). These variables are falling into fourclasses: (a) nutrient enrichment, (b) direct effects (algalblooms), (c) indirect effects (oxygen deficiency), and(d) other effects (algal toxins). This method has notbeen applied so far in Mediterranean waters. However,as the method takes into account synergies andharmonization with the EU WFD and has formed theEU eutrophication guidance, it should form a furtherpowerful tool for eutrophication assessment andmanagement in the Mediterranean waters.

European Union policy on eutrophicationand the Mediterranean Sea

The European Environment Agency (EEA) considerseutrophication as a major environmental problem; inan EEA report on Europe’s environment (EEA 1995),the European dimension of the eutrophication prob-lem was recognized and was considered as a majorenvironmental issue for both inland and marinewaters. Mediterranean countries and members of theEU implement environmental policy on marine

eutrophication based on EU Directives (Table 10).Other Mediterranean countries that are not MemberStates have also modeled their legislation on theprotection of the marine environment according tothose Directives (Saliba 1995). Although the EUDirectives are aiming at controlling point and non-point nutrient inputs to the coastal environment toreduce the impacts of eutrophication, they are specificto: the Urban Waste Water Directive (91/271/EEC)which addresses phosphate and nitrate inputs fromsewage treatment facilities for cities with a population>10,000 (EEC 1991a). The Nitrate Directive (91/676/EEC) addresses the input to the marine environmentof nitrogenous compounds used in agriculture (EEC1991b). The Habitats Directive (92/43/EEC) refers tocontrols concerning quality assurance of waters ofhigh nature conservation value; this includes nutrientcontrol in industrial and municipal discharges (EEC1992). The WFD (2000/60/EC) focuses on point anddiffuse source nutrient control in catchment areas andcoastal marine systems. The EC Directive on bathingwaters (EC 2006) aims at bathing water qualityassessment and focuses on the protection of humanhealth; however, monitoring of water pollution andthe assessment of the potential for proliferation ofphytoplankton is a subject of concern. Eutrophicationassessment is, therefore, an indirect complementaryobjective. The Directives mentioned above aim atnutrient control at the points of discharge, protectingcoastal waters from eutrophication. They are, there-fore, indirect drivers for reducing nutrient inputs towater. On the other hand, the MSFD (2008/56/EC) isaiming at monitoring and assessing marine waters andrequires from the Member States development ofstrategies and measures for good environmental statusof marine waters (EC 2008). This Directive alsointegrates environmental objectives of the Directivesmentioned above as well as the EEC Directive onBiological Diversity (EEC 1993). A list of the EUDirectives directly or indirectly related to eutrophica-tion is given in Table 10. A summary of theirobjectives and the measures concerning mitigation ofeutrophic conditions is also given in the same table.

European Marine Strategy

The implementation of the thematic strategy of theMSFD (EC 2008) should aim at the conservation of themarine ecosystems. This objective requires protected

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areas to be of concern and human activities that haveimpact on the marine environment to be addressed. Afurther step of the Marine European Strategy Frame-work Directive (EMS) is the division of the Europeanmarine waters into four marine ecoregions: (a) theBaltic Sea, (b) the NA Atlantic Ocean, (c) theMediterranean Sea, and (d) the Black Sea. Thisecoregion approach seems to support the developmentof eutrophication criteria and assessment procedures onecosystem quality appropriate for the Mediterraneanecosystem. The “Mediterranean” approach can helpscientific and marine policy integration among Medi-terranean States as it allows non-EU States to adoptcriteria and policy tools developed in other marineregions of Europe. Although many problems on coastaleutrophication originated from activities on land, theEMS deals only with issues relevant to the marineenvironment. Eutrophication is addressed as a priorityissue and a common approach on marine monitoringand assessment is developed (ECOSTAT 2004).However, if coastal areas are characterized as eutro-phic, measures to be taken may include the entireupstream catchment area. Member States should takethe necessary measures to achieve or maintain goodenvironmental status in the marine environment by theyear 2020 at the latest (EC 2008). This objectiverequires good policy which is based on high-qualityinformation. Mediterranean countries should use theexisting scientific information on eutrophication fromthe MED POL program to design marine monitoringthat will fill possible gaps; replication and harmoniza-tion, dissemination, and use of marine science andassociated data should also be promoted (Borja 2006).In addition, GIS-based tools can provide valuableinformation on the spatial structure of marine eutro-phication (Kitsiou and Karydis 1998; Kitsiou andKarydis 2000). The EMS states that human inducedeutrophication is minimized, especially adverse effectsthereof, such as losses in biodiversity ecosystemdeficiency in bottom waters. This approach assumesthat, in addition to nutrients, a description of thebiological communities associated with the seabedand the column water habitats including informa-tion on phytoplankton is required. The finalobjective is to adopt measures for improvingecological state; these measures are practical andrelatively easy to apply in order to achieve themanagement goals. The MED POL experienceindicates that the Mediterranean States respond

admittedly to a different degree to the research andprotection of the marine environment (Jeftic 1993).

The Water Framework Directive

The WFD provides an integrated and coordinatedframework to ensure “enhanced protection and im-provement of the aquatic environment” (EC 2000).The ecological status is classified into five levels:“high,” “good,” “moderate,” “poor,” and “bad,” basedon the deviation from specific reference conditions. Atgood ecological status, quality of biological communi-ties (phytoplankton, plants, etc.) should “deviate onlyslightly from those normally associated with thesurface water body under undisturbed conditions”(Annex V 1.2). Boundary values between good andmoderate conditions are critical because this is themargin determining that restoration measures should betaken. The main objective of WFD is to achieve atleast a good status for the water bodies by 2015.

Eutrophication is considered as a process wherenutrient enrichments cause adverse changes in themarine environment. As nutrients form part of thephysicochemical quality elements, they should bemeasured and ensure that their level does not affectmarine ecosystem functioning. This requires (a) refer-ence values and (b) nutrient scaling characterizingoligotrophy, mesotrophy, and eutrophication. Referencevalues and scaling should be based on data fromMediterranean waters (Ignatiades et al. 1992; Stefanouet al. 2000). On the other hand, ecosystem qualityelements characterizing eutrophication can be expressedas “composition, abundance and biomass of phyto-plankton.” If the ecological status of the biochemicalquality element is good, biomass or diversity deviationfrom reference values should be slight.

Urban Waste Water Treatment Directive

The Urban Waste Water Treatment (UWWT) Direc-tive “concerns the collection, treatment and dis-charge of urban waste water aiming at theprotection of the environment from adverse effects,results of waste water discharges” (EEC 1991a). Ifcoastal areas are identified as eutrophic, nutrientreduction is included, referring to the removal ofphosphorus and/ or nitrogen. Although the eutrophi-cation problem is not the only objective in UWWT,the Directive contributes to the protection of coastal

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waters from “accelerated growth of algae, undesir-able disturbance to the balance of organisms and tothe quality of the water” (Article 2 §11). Article 1(11)defines eutrophication, whereas Article 5 focuses onthe identification of sensitive areas and treatmentrequirements.

Nitrates Directive

The objective of the Nitrates Directive (91/676/EEC) is toreduce eutrophication caused by nitrates from agriculturalsources (EEC 1991b). Coastal marine eutrophication isalso referred explicitly; Article 6 of the Directiverequires from the Member States to review the eutrophicstate of coastal waters every 4 years. It introduces twomanagement tools to reduce eutrophication: (a) desig-nate vulnerable and sensitive zones and (b) developgood agricultural practices; some of the recommendedpractices are crop rotation systems, procedures for landapplication by taking into account the land slope, theperiod of applying fertilizers, and the proximity of watercourses (Annex II). A water monitoring program mustalso be established to designate and revise the nitrate-vulnerable zones. As the Directive does not specify anyanalytical methods or critical values for assessingeutrophication, Member States can develop their ownassessment criteria in reporting “eutrophication levels”that is “ultraoligotrophic,” “oligotrophic,” “mesotro-phic,” “eutrophic,” and “hypertrophic” (Karydis 2009;Primpas et al. 2010).

Habitats Directive

The objective of the Habitat Directive (92/43/EEC) isthe protection of biodiversity through “the conservationof natural habitats and relevant measures have to betaken to maintain or restore at favorable conservationstatus natural habitats” (EEC 1992). The conservationstatus of marine habitats is highly influenced by pointand diffuse pollution by nutrients; it is, therefore,obvious the need for monitoring nutrient levels, asnutrient enrichment leading to eutrophication can inducestress to aquatic species and habitats.

Shellfish Waters Directive

The Shellfish Waters Directive (79/923/EEC) aims atprotecting the quality of coastal waters used for thecultivation of shellfish (EEC 1979). Although the

Directive does not refer to an assessment of eutrophica-tion per se, it sets physical, chemical, andmicrobiologicalrequirements that shellfish waters have to comply with.Good water quality for shellfish will provide adequateprotection from the problem of eutrophication. Concen-tration measurements of dissolved oxygen and saxitoxin(produced by dinoflagellates) as well as coloration(reported in the Annex) are relevant to assessments ofeutrophication (EEC 1979).

Bathing Water Directive

The objective of the BWD, 2006/7/EC, is to ensuregood coastal water quality suitable for bathing, protect-ing public health (EC 2006). It is not directly involvedwith eutrophication but the close coordination with theUWWT Directive and the Nitrates Directive fromagricultural sources is recommended (EC 2006).

Discussion

The interaction between science and policy process iscontinuous and becomes more apparent when anenvironmental issue is at a mature phase. According tothe policy process developed by Winsemius (1986), thepolicy life cycle consists of three phases. (a) Thediscovery phase: the issue is recognized as a problem.This phase is characterized by controversy regardingthe importance of the problem. (b) The political ordecision-making phase: the problem at this phase isplaced on political dimensions; at this stage, legislativeframework is usually set. (c) The management phase:at this phase, political decisions and managementpractices are implemented. Research, data collection,and assessment are the main tools during the firstphase. They contribute to the assembly of the problemthat is discovery, problem formulation, and establish-ment of the main parameters (de Jong 2006). Allphases can be served by science but aim at differentobjectives. Research at the initial phase defines theproblem. Further research during the second phaseprovides the scientific background for political deci-sions. Science during the third phase provides thenecessary information for management practices andcontrol (Van Koningsveld et al. 2005). The mainscientific tools at the third phase focus on monitoring(data collection on a routine basis) and prediction(modeling to foresee future eutrophication trends).

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Research on marine eutrophication started in 1950sand 1960s, mainly in the USA (Barlow et al. 1963) andNorthern Europe (Rodhe 1969). The main themes were(a) inputs and sources (Taslakian and Hardy 1976), (b)limiting factors (Dugdale 1967; Ryther and Dunstan1971), (c) the N/P ratios (Ryther and Dunstan 1971),(d) the influence of eutrophication on planktonblooms (Pomeroy et al. 1956), (e) ecosystem effects(Livingston 2001), (g) oxygen depletion (Colomboet al. 1992), and (h) nutrient uptake and cycling(Dugdale and Goering 1967). However, there wascontroversy about the causes of eutrophication: thelimiting factor was the main question in marineeutrophication during the 1960s. The argument wasfocused on the nutrient that should be reduced orremoved in order to control eutrophication trends.Although it is generally accepted that phosphorus is thelimiting factor in lakes (Goldman and Horne 1983),Ryther and Dunstan (1971), working on the East Coastof the USA, concluded that nitrogen was the limitingnutrient for marine phytoplankton. Dugdale (1967)proposed a mathematical model based on the Michaeliskinetics to describe nitrogen limitation in the sea. Inspite of the recent indications that phosphorus may bethe limiting nutrient in the Eastern Mediterranean(Krom et al. 1991), nitrogen seems to hold a centralrole in nutrient limitation in the marine environment.Eutrophic trends in the Mediterranean were locatednear estuaries, embayments, and later in some gulfsmentioned in the present review. The geographicdistribution of eutrophication in the MediterraneanSea is limited as it occurs in densely populated areascharacterized by intensive economic activities and, atthe same time, the need for good water quality suitablefor swimming, recreation, and shellfish aquaculture isrequired. Eutrophication has been identified as one ofthe emerging problems in the coastal zone for thetwenty-first century together with exotic algal blooms,plastics, estrogens, nonindigenous organisms in ballastwaters, and pathogens (Goldberg 1995). The authorsuggests that eutrophication studies should be based onmeasurements over large geographical areas and over atime scale of decades. The Committee of the MarineBoard of the US National Research Council hasproposed, in addition to nutrient, chlorophyll, anddissolved organic matter concentrations measurements,the recording of physical and biological parameters:current speeds, density fields, light fields, primaryproductivity, phytoplankton species composition, and

bacterial mass production. Similar eutrophication strat-egy has been adopted by UNEP (2003b), proposingtwo lists of parameters: the list of mandatory param-eters and the list of supplementary parameters. Theformer list includes variables directly related to theproblem of eutrophication (nutrients, chlorophyll,transparency, pH, phytoplankton cell number, andphytoplankton species composition) and the supple-mentary list includes suspended particulate matter,TOC, H2S, zooplankton, primary productivity, andmacrophyte biomass. However, during the first phasesof the MED POL, country responses were almostrestricted to the Northern Mediterranean countries.Sampling frequency, sampling pretreatment, analyticalmethods, and reporting formats were highly heteroge-neous (UNEP 2003b). There is, therefore, lack ofevenness in scientific information that decreases fromthe west to the east and from the north to the south ofthe Mediterranean. The problem becomes more serioussince the southern side of the Mediterranean regiondevelops at a large expense of the marine environment.Criteria for sampling frequency and spatial coveragehave also been proposed. It is obvious that eutrophi-cation projects carrying out all these measurements willbe expensive to run. However, as relatively highermean nutrient concentrations, higher productivity, andfrequent algal blooms occur in few areas, i.e., theAdriatic Sea, the Gulf of Lions, and the NorthernAegean Sea (UNEP 2003a), projects should also betargeted to hot spots.

Eutrophication assessment is an interdisciplinary task(Kitsiou and Karydis 2011). It requires the cooperationamong different disciplines such as plant, animal, andmicrobial ecology, physical oceanography, marinechemistry, climatology, biogeochemistry, urban infra-structure, demography, and nutrition (Nixon 2009).Synthesis of this information should be carried outnowadays at a large scale since eutrophication has beenrecognized as a problem of global character. Thisobjective can be achieved by using satellite imageryand simulation models. Both tools have been applied inthe Mediterranean marine environment and they havecontributed up to an extent to the understanding of theprocesses that shape the expression of eutrophication(Antoine et al. 1995; Bricaud et al. 2002; Crispi et al.1998; Llebot et al. 2010).

Optical remote sensing allows the monitoring ofthe heterogeneity of phytoplankton growth at spatio-temporal scale in marginal and enclosed seas and has

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been widely used in eutrophication studies in theMediterranean Sea. However, in some cases, thecontribution of satellite data to eutrophication studiesis not effective unless they are combined with in situmeasurements carried out by oceanographic vessels.Remote sensing cannot substitute classical oceano-graphic methods since the electromagnetic radiation isvery poor at penetrating water and is often hamperedby clouds. In addition, during eutrophication, assess-ment at low spatial scales, such as bays of limitedgeographical extent, there is a need for satellite data ofvery high spatial resolution; therefore, additional in situmeasurements are required.

Since the time that Redfield (Redfield 1934;Redfield et al. 1963) proposed the N/P ratio, hundredsof publications appeared dealing with the N/P byatom ratio in the marine environment. Ryther andDunstan (1971) have indicated that the averageconcentrations of dissolved nitrogen and phosphorusin the seawater are near the Redfield ratio. Theauthors claim that this is not a case that couldcharacterize a nutrient balance on a short-term basis.On the grounds of available data, the authors foundthat nitrogen was, in most cases, the limiting nutrient.Later work (Smith 1984; Howarth and Marino 2006)concluded that nitrogen is most probably the nutrientcausing eutrophication in the temperate zone. Al-though it is now well established that marineecosystems with molar ratios less than 16:1 arecharacterized as nitrogen limited and with ratios >16:1as phosphorus limited, this N/P ratio does not seem to bea good indicator describing eutrophic conditions(Karydis et al. 1983). In addition, the N/P ratio inareas where both nutrients are abundant does not seemto be a critical factor supporting eutrophic conditions.Since the 1990s, both scientists and internationalenvironmental agencies seem to follow practices andimplement measures to control nitrogen inputs in themarine environment (Nixon 1995). Apart from the EUlegislation, reports from the Ecological Society ofAmerica (Vitousek et al. 1997; Carpenter et al. 1998;Howarth et al. 2000) as well as from an expertscommittee of the US National Academy of Scienceshave been presented (NRC 1993, 2000). These reportshad an influence on the US Government, and in thereport Nutrient Criteria Technical Manual GuidanceManual for Estuarine and Coastal Marine Waters(EPA 2001), the need for nitrogen input reduction hasbeen recognized. The EPA report was mainly based on

the NRC (2000) report and accepted the conclusionthat nitrogen was the nutrient causing coastal eutro-phication. Nitrogen can also enrich the marine envi-ronment through the mechanism of atmosphericdeposition. Nitrogen can be deposited in the form ofemitted compounds (NOx), oxidized nitrogen com-pounds (NOy), and ammonia (NH3)/ammonium(NH4

+). Reduction of nitrogen deposition in the seaacquires nitrogen reduction of the emissions at thesource, whereas if nitrogenous compounds from theatmosphere are deposited in the watershed, there arevarious approaches for the nutrient control (NRC2000). NOx reduction assumes consumption of lessfossil fuel or removal of the nitrogen oxides from theexhaust system of the vehicles. Legislation on car fueleconomy and tailpipe emissions implemented inthe USA and EU to control atmospheric pollutionand reduce the greenhouse effect seems to beeffective for the reduction of airborne nitrogendeposition. On the contrary, efforts to reduce ammonia/ammonium airborne pollution would have limitedsuccess since both forms originate from farming activitiesand fertilizers.

High rates in fertilizer production since 1960coincided with the increase of eutrophication problems.The intensity of the use of fertilizers can vary by 1,000-fold, ranging from 1 kg ha year−1 of cultivated land to1,000 kg ha year−1 (Nixon 1995). The increasingdemand for fertilizers is due to increased nutritionalrequirements of the exponentially expanding humanpopulation. Since 1830, when the first billion mark wasreached, the Earth’s population has increased rapidlyand the estimate for 2011 is about seven million people(Bremner et al. 2010). This indicates that, in spite ofany regulations, the actual needs for fertilizers willcontinue to increase and, therefore, policies in theMediterranean with reference to the mitigation of theimpact from fertilizers can only be effective as far asthe excessive use of fertilizers is concerned.

The effects of sewage infrastructure and national/European regulations on the use of fertilizers aregoing to reduce nutrient discharges in the Mediterra-nean environment although the actual reduction willnot be easy to be determined. However, a trendreversal, as it is called in Europe, is expected withinthe next 10 years (Carstersen et al. 2006). Thisphenomenon has also been characterized as oligotro-phication (Nixon 2009). There is now limitedknowledge concerning changes in ecosystem structure

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and function that undergo the oligotrophicationprocesses. So far, this experience is limited in fresh-waters where decrease in phytoplankton biomass,changes in taxonomic compositions, increases in theratios of zooplankton/ phytoplankton biomass, andincreases in the abundance of piscivorus fishes havebeen observed (Nixon 2009). This productivity reduc-tion may lead to a relative reduction of biologicalsources in the Mediterranean but will certainly improvethe quality of coastal waters used for recreation.

Eutrophic trends seem to favor HAB formation.HABs are clearly affected by human activities, butcauses and mechanisms are not always clear. Interna-tional bodies such as GEOHAB, ECOHAB, andEUROHAB study the processes and problems relatedto HABs to improve the understanding of factorsleading to toxic blooms (Graneli and Lipiatou 2002).Possible factors favoring toxic bloom formations are(a) the distribution of resting cysts by humanactivities, (b) the overenrichment of coastal waters,(c) human-induced climatic change, and (d) thedecreasing biomass of filter-feeding organisms (Masoand Garces 2006). Concrete evidence exists only forthe role of cultural overenrichment in the growth oftoxic algal species (Zingone and Enevoldsen 2000).The ways that human activities contribute to theformation of toxic blooms are diverse and difficult tocontrol (NRC 2000; UNEP/FAO/WHO 1996). River-ine inputs are a crucial factor especially whencombined with low discharge rates; this is the casewith the Nile, boosting A. minutum blooms in theMediterranean (Vila et al. 2005). HABs seem to be arecurrent problem in the Mediterranean recreationalwaters. The development of coastal construction suchas port, breakwaters, and semienclosed beaches inhighly populated coastal areas increases the possibil-ity for HABs growth. From the management point ofview, in addition to any legal measures (Conventions,Directives, and National Legislation), a number ofobjectives should be set (Maso and Garces 2006):development of monitoring schemes for HABs,reliable databases, information exchange, and theimplementation of the medical sector (public healthand epidemiological studies).

Eutrophication indicators (Karydis 2009) or valuesderived from variables provide information about theseriousness of the eutrophication problem in an areaand have further implications in assessment studies.The definition of an indicator according to OECD

(1993) is: Indicator/parameter or a value derivedfrom parameters, which points to, provides informa-tion about/describes the state of the phenomenon/environment/area and has further implications for theenvironment. The indicator is not necessarily anenvironmental parameter, but it could be an expres-sion of a parameter or a pool of environmentalparameters. A good indicator has to meet a set ofcriteria. Within the context of the definition, anumber of indicators used for scaling eutrophicationlevels have been proposed. Ignatiades et al. (1992) aswell as Giovanardi and Tromellini (1992) have usednutrient and chlorophyll distributions to developscales characterizing oligotrophy and eutrophication.Vollenweider et al. (1998) proposed a multimetriceutrophication index the “TRIX” based on nutrient,oxygen, and chlorophyll concentrations for assessingeutrophication in the Mediterranean. However, thisindex has mainly been tested in the Adriatic Sea andmore work is needed in the Mediterranean waters forthe definition of a scale suitable for oligotrophic waters(Primpas and Karydis 2010). A recent development inassessing eutrophication levels, based on principalcomponent analysis, has also been proposed (Primpaset al. 2010). It introduces an index based on nutrientand chlorophyll concentrations. Environmental indica-tors can mainly be used for three purposes (UNEP2003a): (a) to compile information useful for environ-mental assessment, (b) to identify key factors that cansupport policy development and priority setting, and(c) to monitor the effects of policy responses. Theparameters/indicators that can be used for eutrophica-tion studies, coastal management, and policy shouldsatisfy the following criteria: (a) to be relevant toMediterranean country policies, (b) to be relevant tothe coastal zone, (c) to provide adequate informationboth in space and time, and (d) reference values shouldbe available for the parameters to be used.

Over the last 20 years, there is an interest ofindicators for the marine environment by internationalorganizations beyond the Mediterranean policies. TheEU WFD encourages the use of indicators. Thisencouragement is not the result of academic interestfor understanding eutrophic processes but the require-ment of legislation and policy to identify andeventually reduce eutrophic trends. The UnitedNations Conference on Environmental Developmentin 1992 known as the Rio Summit encouraged the useof indicators in its publication Agenda 21. These

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indicators would encourage not only environmentalbut also economic and social aspects since it has beenrecognized that these disciplines formed the basis ofsustainable development (Gubbay 2004). This inte-grated approach using indicators has also beenadopted by the UK Government properly constructed[indicators] could measure performance againstagreed targets and objectives and assist governmentsand the public to evaluate how well nationalenvironmental policies and international commit-ments are being met (Anon 2002). The Organizationof Economic Cooperation and Development (OECD1993) encouraged the development of environmentalindicators as early as the 1990s and looked for waysof integrating environmental and economic decisionmaking. It was realized that environmental indicatorswould improve the overall performance in environ-mental management. The introduction of environmen-tal matters into OECD policies can satisfy therequirements for sustainable development. OECDhas adopted the Pressure–State–Response approach:human activities exert pressures on the environmentthat change the state (quality) and they are correctedby the response of the society in environmental,social, and economic policies. A similar approach hasbeen adopted by the EEA (1998) which is the DrivingForce–Pressure–State–Impact–Response (DPSIR) andprovides an overall framework for analyzing environ-mental issues. EEA has categorized indicators intofour types: descriptive indicators (e.g., diversityindices), performance indicators linked to referenceconditions (e.g., nutrient concentrations), efficiencyindicators (production and consumption processes),and total welfare indicators that need be defined. TheOSPAR (Oslo Paris Convention) has developedEcoQOs and the North Sea Ministers in the 3rd NorthSea Conference have agreed to elaborate techniquesfor the development of ecological objectives for theNorth Sea and its coastal waters. The ecosystemproperties concerning EcoQOs are resilience, stability,productivity, diversity, and trophic structure. Howev-er, it is likely that a suite of indicators rather than asingle one will be needed to adequately report onecosystem health, structure and function (Gubbay2004). Many international organizations such as EEA(1998), OECD (1993, 2004), UNEP (2003c, 2004),and United Nations Committee of Sustainable Develop-ment (Anon 2002) have proposed indicator lists onenvironmental quality, most of them linked with

sustainable development in terms of marine eutrophi-cation. EEA has focused on the classification of coastalwaters, mean trophic level, and water quality, UK(DETR 1999) has focused on biodiversity, estuarinewater quality, marine inputs, and bathing water quality,and OSPAR (Anon 2002) has focused on phytoplank-ton, chlα, and phytoplanktonic indicator species foreutrophication. In spite of the indicator lists and thelarge number of criteria for assessing marine eutrophi-cation, they seem to be the outcome of administrativenegotiations rather than the result of scientific expertise.Science is simply used as an authoritative basis for thecontinuation of the nutrient reduction policies (de Jong2006). It is generally accepted that the more theinformation collected, the better defined and scientifi-cally sound the measures and policies will be. However,in international marine eutrophication policy, thegeneration of knowledge has not reduced the uncer-tainty but rather increased it (de Jong 2006). Inaddition, criteria have been simplified to critical valuesof few variables, mainly nutrients, neglecting effects,consequences, and linkages with other effects in themarine ecosystem. Since a policy on eutrophication isestablished, new knowledge cannot be easily assimilat-ed in the existing legal framework. The management ofmarine eutrophication does not seem to suffer from lackof information and policies but rather the implementa-tion of these policies by the signatory parties. This ismore noticeable in the Mediterranean region where theMediterranean countries differ in economic develop-ment and environmental awareness to a great extent.The next 10 years will be critical in evaluating theeffectiveness of the various national and internationalpolicies in the Mediterranean.

Hugget (2005) suggested the use of thresholds as aconceptual framework for the development of strate-gies for sustainable natural resources management.Therefore, researchers should focus on contributingquantitative evidence of eutrophication thresholds forfuture environmental policymaking. However, severaltimes, thresholds have to “be crossed” to be detected,which means that they cannot always be used to helpprevent abrupt changes in ecosystems. In addition todelays in recognizing the shifts, the implementation ofmanagement actions could be also delayed by scientificuncertainty or stakeholder pressure.

Perrings and Walker (1997) pointed out thatoptimal management should be sensitive to keyvariables conditioning long-term resilience of the

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system. However, attention should be paid during theprocess of identifying regime shifts, since there is therisk of detecting thresholds which are just randomfluctuations. In addition, there is in general amismatch between the geographical and temporalscales of management actions and ecosystem changepoints. Eutrophication shifts driven by climaticchanges will become quite common in the future,making the definition of fixed management zonesbased on geographic boundaries ineffective. Conse-quently, a prerequisite for successful managementshould be the flexibility to adapt to novel andunexpected events through management strategies.Thus, adaptive management should focus on theintegration of existing interdisciplinary information intodynamic models capable of making predictions aboutthe impacts of alternative policies.

Policy making requires a wide range of indicatorscovering a wide range of environmental, economic,and social aspects of the coastal system. This is alsoin agreement with the objectives of the modifiedBarcelona Convention in 1995: The contractingparties shall commit themselves to promote theintegrated management of the coastal zones, takinginto account the protection areas of ecological andlandscape interest and the rational use of naturalresources (Article 4[e]). Similar concepts of integrat-ed coastal approach have been included in the EUDirective on Marine Strategy (EC 2008): It is crucialfor the achievement of the objectives, managementmeasures, monitoring and assessment activities ….The integration of descriptors referring to social,economic, and environmental values is not an easytask. Different scales of measurements, nominal,ordinal, interval, and ratio scales of measurements(Sharma 1996) complicate the assimilation of all thesevariables in an integrated classification and data-processing system: this approach requires drasticmanipulation of the variables (Kitsiou et al. 2002).

In 2009, Duarte stated that a proper assessment ofeutrophication should consider the phenomenon as acomponent of global change regarding both its causesand consequences. Consequently, the use of appro-priate methodologies to assess and manage eutrophi-cation should consider the interactions with variouscomponents such as climate change (Lloret et al.2008), overfishing, and habitat loss. Cloern (2001) inhis description of the phase III conceptual model ofthe coastal eutrophication problem argued that eutro-

phication assessment needs sustained programs ofintegrated research and monitoring. Research effortsshould, therefore, incorporate the social and anthro-pogenic pressures than focus only on the understand-ing of the environmental and ecosystem processes. Aparticipatory approach has been proposed by Nunneriand Hofmann (2005) based on the DPSIR analyticaltool in order to evaluate different measures forreducing the input of nutrients and preventing marineeutrophication. DPSIR uses a core set of indicators forenvironmental performance, including eutrophicationissues, and considering human activities as an integralpart of the ecosystem. Zaldívar et al. (2008b) gives adetailed description of the DPSIR framework and itsapplication to marine eutrophication. Scientistsshould, therefore, work in a cross-disciplinary basisand convey their outputs to coastal managers andlegislators in a simplified way. In this framework,marine eutrophication is addressed in a number ofsystems of global character, such as Land–OceanInteractions in the Coastal Zone (LOICZ), GlobalOcean Observing System (GOOS), and CoastalModule of the Global Terrestrial Observing System(C-GTOS). The LOICZ approach is a core project ofthe International Geosphere–Biosphere Programmeand the International Human Dimensions Programmeon Global Environmental Change that deals with thestudy of global environmental change. LOICZ focuson the investigation of changes in the biology,chemistry, and physics of the coastal zone and thedevelopment of tools that allow the assessment ofsite-specific and global coastal processes. The LOICZbiogeochemical model that is based on the massbalance of water and materials (Crossland et al. 2005)has been applied by Giordani et al. (2008) at differenttemporal and spatial scales in 17 Italian lagoons; theresults indicated that this model is capable of represent-ing the wide range of trophic conditions associated withshallow coastal ecosystems.

The GOOS is a permanent global system forobservations, modeling, and analysis of marine andocean variables to support the accurate description ofthe current state of the sea and forecasts based onmarine environmental conditions and social impacts.EuroGOOS is an association of national governmentalagencies and research organizations committed toEuropean-scale operational oceanography within thecontext of the intergovernmental GOOS. EuroGOOShas 35 members from 18 European countries and

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focuses on 6 regional sea areas: the Arctic, the Baltic,the North West Shelf, the Biscay–Iberian area, theMediterranean, and the Black Sea. The MediterraneanOperational Oceanography Network is the coordinat-ing body of the EuroGOOS Mediterranean TaskTeam. The Chlorophyll Global Integrated Networksponsored by GOOS aims to promote in situmeasurement of chlorophyll in combination withsatellite estimates. Finally, C-GTOS was developedin the framework of the Global Terrestrial ObservingSystem, a program for observations, modeling, andanalysis of terrestrial ecosystems to support sustain-able development, including issues related to humandimensions and habitat alteration, water cycle, andwater quality.

Over the last 20 years, large-scale research activ-ities covering the whole of the Mediterranean basinhave significantly contributed to the understanding ofthe mechanisms and processes in the marine environ-ment, providing a sound scientific background for thepolicy makers. In the 1990s, the POEM and MarineScience and Technology programs had focused onhydrographic surveys with chemical and biologicalstudies and set priorities for further marine research inthe Mediterranean Sea. In addition, other EU pro-grams (FAIR, LIFE, TERRA, and INTERREG),although their main objectives are not in oceanography,have provided valuable information for the protectionand management of the coastal Mediterranean marineenvironment (EEA 1999).

An attempt to integrate economic, social, andecological data of a coastal system has been reported(Moriki et al. 1996). The variables were standardizedand the Island of Rhodes, Greece was divided intofive zones. Different scenarios were tested, placingpriority on (a) economic development, (b) agriculturaldevelopment, and (c) sustainability using multicriteriachoice methods to quantify the outcome from eachpriority. Similar work was carried out in Rhodes usingGIS techniques (Kitsiou et al. 2002). It was shownthat the developed methodology is useful in assessingspatial data, either to evaluate the current situation orto assess possible impact from future development.Multiple criteria analysis seems to be a powerful toolfor the management practices of the coastal zonewhere quantitative and qualitative variables areinvolved. However, the use of multicriteria techniquesin the Mediterranean coastal zone is rather limited(Karydis 2001). There is growing concern about the

sustainability of the coastal area of the Mediterranean.Sustainability requires a number of actions (Davos1998): (a) clearly defined policy objectives: theseobjectives have been clarified in the BarcelonaConvention, the MAP, the MED POL, the Blue PlanProgram, as well as in the EU Directive on MarineStrategy and (b) integration and harmonization ofsectoral policies: the MSFD encourages MemberStates to integrate measures relevant to EU legislationespecially the Directive concerning urban wastewatertreatment and the Directive concerning the manage-ment of bathing water quality (Article 13 §2). Withinthe framework of the Strategic Action Program,measures for cleanup procedures have been takenwhere all the signatories have undertaken the samepercentage of responsibility for the reduction of thepollution effects; targets of 50% over a 10-year periodfor activities related with nutrient enrichments frommunicipal sewage and agriculture runoff seems to bea realistic objective.

Overview

The main water body of the Mediterranean Sea isoligotrophic. However, there are coastal areas, embay-ments, and estuaries characterized by distinct eutrophictrends. Monitoring is required to establish eutrophicationimpacts in the marine environment since eutrophicationwas established as a problem in certain Mediterraneancoastal areas about 30 years ago.

Measures for the environmental protection of theMediterranean Sea were taken as early as 1975 basedon the Barcelona Convention. This convention wasfurther implemented through the MAP, the Blue Plan,and the MED POL program (monitoring and re-search). A database of environmental variables hasbeen formed for the Mediterranean Sea over the last40 years; many of the parameters measured are relatedto eutrophication; although the spatial and temporaldistribution of sampling showed heterogeneity espe-cially between the northern and southern parts of theMediterranean, it is a valuable source of environmen-tal information, useful for assessments setting thresh-old/critical values concerning effluents, discharges,and water quality. The existing data, the numeroustechnical reports and papers in international journalson various aspects of eutrophication in the Mediter-ranean, provide a sound scientific background for the

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National Legislation of many Mediterranean States aswell as EU Directives on the quality and protection ofthe marine environment. These Directives are applicableto most Mediterranean countries of the northern coast ofthe Mediterranean as they are EU Member States.However, many other non-EU Member States of theMediterranean are adapting their legislation to EUstandards. Legislation, marine monitoring, and marineresearch are interdependent in the Mediterranean ascommon marine policy provides the framework and themeans to materialize research/monitoring on eutrophi-cation under a common scheme (MED POL monitor-ing) or common specifications (research requirements ofthe EU Directives) and the outcome forms the platformfor targeted legislation measures, environmental policy,and coastal management practices in the Mediterraneancoastal zone. In addition to the legislation, the existingscientific information and the collaboration and theinterchange of experience among Mediterranean labo-ratories and other competent authorities working underinternational schemes will provide a sound basis formanagement practices aiming at environmental protec-tion and sustainable development of the coastal zone.

Acknowledgement The authors wish to thank Dr. M.A.Efstratiou for her constructive comments on an earlier version ofthe manuscript.

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